Sanitary program to reduce embryonic mortality associated with infectious diseases in cattle

Amauri Alcindo Alfieri Raquel Arruda Leme Alais Maria Dall Agnol Alice Fernandes Alfieri About the authors

Abstract

Among reproductive disorders in dairy and beef cattle worldwide, embryonic mortalities stand out as one of the most frequent. Because of the multifactorial etiology, the clinical and laboratory diagnoses of embryonic mortality causes in cattle are quite complex. Often, infectious causes may account for up to 50% of bovine embryonic mortality rates after 30 days of conception. This review will address the main causes of early and late embryonic mortality, with emphasis on infectious causes and, particularly, those more frequent in the Brazilian cattle herds. In addition, we will discuss ways of controlling and prophylaxis including those related to reproductive and sanitary management, with emphasis on immunoprophylaxis of the three most frequent reproductive infectious diseases in Brazilian dairy and beef cattle herds.

Keywords:
bovine; reproduction; IBR; BVD; leptospirosis; vaccination

Introduction

In a recent past of Brazilian cattle breeding, and especially of beef cattle, the embryonic mortality rate was a reproductive parameter that was very little evaluated in the production systems. The lack of information regarding this parameter was general both to part of producers and technicians responsible for the reproduction of the herds. However, with the advent and more recurrent use of reproductive biotechniques, primarily the Fixed-Time Artificial Insemination (FTAI), this important parameter of reproduction in cattle has been evaluated more frequently. The establishment of more standardized FTAI protocols suitable for different geographic regions and different production conditions enabled to compare results that facilitate the identification and quantification of reproductive failures and, in particular, embryonic mortalities. In this review, we approach sanitary programs focused on reducing embryonic mortality associated with infectious diseases. Features of embryonic mortality, related infectious causes, epidemiological profile of infectious reproductive diseases, sanitary programs, vaccination, and biosecurity are addressed.

Embryonic mortality

In the bovine species, the embryo is defined as the product obtained up to approximately 42-45 days after conception, which refers to the cell differentiation period (Committee on Reproductive Nomenclature, 1972Committee on Reproductive Nomenclature Recommendations for standardizing bovine reproductive terms. 1972. Cornell University College of Veterinary Medicine. 62:216-237.). Consequently, this is the period used to evaluate the embryonic mortality rate in beef and dairy cattle herds. In practice, the return to estrus in an interval longer than 17-25 days reflects the occurrence of embryonic mortality (Ayalon, 1978Ayalon N. 1978. A review of embryonic mortality in cattle. J Reprod Fert, 54: 483-493.; Abdalla et al., 2017Abdalla H, Elghafghuf A, Elsohaby I, Nasr MAF. 2017. Maternal and non-maternal factors associated with late embryonic and early fetal losses in dairy cows. Theriogenology, 15(100):16-23.). It should be emphasized that in the analysis of the embryonic mortality rate, one must eliminate fertilization failures.

In cattle, embryonic mortality is a multifactorial event that may involve genetic and environmental factors. Genetic factors are intrinsic to the embryo, and the most frequent are those caused by genetic defects, individual genes and genetic interactions that can lead to chromosomal abnormalities. In cattle, genetic defects may account for up to 20% of embryonic and fetal mortalities (Vanroose et al., 2000Vanroose G, de Kruif A, Van Soom A. 2000. Embryonic mortality and embryo-pathogen interactions. Anim Reprod Sci, 60-61:131-43.; Diskin and Morris, 2008Diskin MG, Morris DG. 2008. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim, 43(2):260-267.).

A range of causes can be included as environmental factors of embryonic mortalities in cattle. Among the several causes, the following stand out: age; climate; hormonal imbalance; uterine environment, among others that can cause physiological and endocrine disorders that can lead to the death of the embryo (Chebel et al., 2004Chebel RC, Santos JEP, Reynolds JP, Cerri RL, Juchem SO, Overton M. 2004. Factors affecting conception rate after artificial insemination and pregnancy loss in lactating dairy cows. Anim Reprod Sci, 84(3-4): 239-255.; Inskeep and Dailey, 2005Inskeep EK, Dailey RA. 2005. Embryonic death in cattle. Vet Clin North Am Food Anim Pract, 21(2):437-641.; Walsh et al., 2011Walsh SW, Williams EJ, Evans AC. 2011. A review of the causes of poor fertility in high milk producing dairy cows. Anim Reprod Sci, 123(3-4):127-138.; Abdalla et al., 2017Abdalla H, Elghafghuf A, Elsohaby I, Nasr MAF. 2017. Maternal and non-maternal factors associated with late embryonic and early fetal losses in dairy cows. Theriogenology, 15(100):16-23.; Sánchez et al., 2018Sánchez JM, Mathew DJ, Passaro C, Fair T, Lonergan P. 2018. Embryonic maternal interaction in cattle and its relationship with fertility. Reprod Domest Anim, 53(2):20-27.). In addition, the nutrition factor is also important, especially considering the possibility of postpartum cows present a negative energy balance that may impact the follicular dynamics due to changes in the gene expression of dairy cow granulosa cells at 60 days post-partum, reducing the reproductive performance of this animal category. Therefore, the effects of the negative energy balance may be felt even after the resolution of the problem (Butler, 2003Butler WR. 2003. Energy balance relationships with follicular development, ovulation and fertility in postpartum dairy cows. Livest Prod Sci, 83(2-3): 211-218.; Girard et al., 2015Girardi A, Dufort I, Sirard MA. 2015. The effect of energy balance on the transcriptome of bovinegranulosa cells at 60 days postpartum. Theriogenology, 84:1350-1361.; Lonergan et al., 2016Lonergan P, Fair T, Forde N, Rizos D. 2016. Embryo development in dairy cattle. Theriogenology, 86(1):270-277.; Rani et al., 2018Rani P, Dutt R, Singh G, Chandolia RK. 2018. Embryonic mortality in cattle – A review. Int J Curr Microbiol App Sci, 7(7):1501-1516.). Also in regards to environmental factors, we will highlight the infectious causes.

Embryonic mortality can also be classified into two types based on the time elapsed after conception. Those mortalities that occur before 15 days post-conception are termed early embryonic mortalities and mortalities of 16 to 42-45 days are termed late embryonic mortalities (Inskeep and Dailey, 2005Inskeep EK, Dailey RA. 2005. Embryonic death in cattle. Vet Clin North Am Food Anim Pract, 21(2):437-641.). Comparatively, early embryonic mortalities are more frequent than the late ones (Dunne et al., 2000Dunne LD, Diskin MG, Sreenan JM. 2000. Embryo and foetal loss in beef heifers between day 14 of gestation and full term. Anim Reprod Sci, 58(1-2):39-44.; Inskeep and Dailey, 2005Inskeep EK, Dailey RA. 2005. Embryonic death in cattle. Vet Clin North Am Food Anim Pract, 21(2):437-641.). In cases of early embryonic mortality there will be no change in the period of the estrous cycle. It means that early embryonic mortalities are accompanied by a return to estrus at regular intervals. Conversely, one of the main clinical features of late embryonic mortalities is the return to estrus at irregular intervals (Silke et al., 2002Silke V, Diskin MG, Kenny DA, Boland MP, Dillon P, Mee JF, Sreenan JM. 2002. Extent, pattern and factors associated with lateembryonic loss in dairy cows. Anim Reprod Sci, 71(1-2):1-12.).

Infectious causes of embryonic mortality in cattle

In this category we can include nonspecific causes, represented by a series of bacteria that can cause ascending infections. That is, these bacteria can be present in the vaginal mucosa itself or else in the penis, in cases of reproduction by natural mating, or in the semen in cases of artificial insemination. Often, these opportunistic bacteria cause inflammation in the uterus, resulting in endometritis, which can render the uterine environment inhospitable to the embryo (Bielanski et al., 2000Bielanski A, Devenish J, Phipps-Todd B. 2000. Effect of Mycoplasma bovis and Mycoplasma bovigenitaliumin semen on fertilization and association with in vitro produced morula and blastocyst stage embryos. Theriogenology, 53(6):1213-1223.; Vanroose et al., 2000Vanroose G, de Kruif A, Van Soom A. 2000. Embryonic mortality and embryo-pathogen interactions. Anim Reprod Sci, 60-61:131-43.; Silva et al., 2016Silva JR, Ferreira LF, Oliveira PV, Nunes IV, Pereira ÍS, Timenetsky J, Marques LM, Figueiredo TB, Silva RA. 2016. Intra-uterine experimental infection by Ureaplasma diversum induces TNF-α mediated womb inflammation in mice. An Acad Bras Cienc, 88(1):643-652.; Sheldon and Owens, 2017Sheldon IM and Owens. 2017. Postpartum uterine infection and endometritis in dairy cattle. In Proceedings of the 33rd Annual Scientific Meeting of the European Embryo Transfer Association (AETE), 2017, Bath, United Kingdom. Anim Reprod, 14(3):622-629.; Rani et al., 2018Rani P, Dutt R, Singh G, Chandolia RK. 2018. Embryonic mortality in cattle – A review. Int J Curr Microbiol App Sci, 7(7):1501-1516.). The frequency of nonspecific infections in bovine females that result in embryonic mortalities in dairy herds is low (Vanroose et al., 2000Vanroose G, de Kruif A, Van Soom A. 2000. Embryonic mortality and embryo-pathogen interactions. Anim Reprod Sci, 60-61:131-43.; Sheldon and Owens, 2017Sheldon IM and Owens. 2017. Postpartum uterine infection and endometritis in dairy cattle. In Proceedings of the 33rd Annual Scientific Meeting of the European Embryo Transfer Association (AETE), 2017, Bath, United Kingdom. Anim Reprod, 14(3):622-629.). As cases are sporadic, in general, specific measures for the control and prophylaxis of these infections are rarely adopted.

However, the reproductive tract of the bovine female is susceptible to a series of infectious processes caused by pathogenic organisms specific to the reproductive sphere. Infections can be caused by different classes of microorganisms, such as bacteria, viruses, and protozoa (Tab. 1). Although it is possible, fungal infections are rarely a problem of great magnitude in the reproduction of cattle (Vanroose et al., 2000Vanroose G, de Kruif A, Van Soom A. 2000. Embryonic mortality and embryo-pathogen interactions. Anim Reprod Sci, 60-61:131-43.; Givens and Marley, 2008Givens MD, Marley MS. 2008. Infectious causes of embryonic and fetal mortality. Theriogenology, 70(3):270-285.; Walsh et al., 2011Walsh SW, Williams EJ, Evans AC. 2011. A review of the causes of poor fertility in high milk producing dairy cows. Anim Reprod Sci, 123(3-4):127-138.).

Table 1
Frequency of embryonic death associated with different infectious agents in beef and dairy cattle herds.

Infections caused by specific microorganisms can be venereally transmitted, occurring in cases that the organisms are present in the genital tract of the female or male, and by the hematogenous route, which occurs with those organisms that reach the uterus through the bloodstream (Vanroose et al., 2000Vanroose G, de Kruif A, Van Soom A. 2000. Embryonic mortality and embryo-pathogen interactions. Anim Reprod Sci, 60-61:131-43.). The epidemic or endemic presentation of the diseases depends on the geographical region, epidemiological scenario, reproductive management, vaccination and health status of the herds. In epidemiological terms, specific infections of the reproductive tract may present in an epidemic form or, more frequently in Brazil, in an endemic manner. The epidemic form prevails in specific pathogen-free herds, that is, they have never been in contact with the microorganism, either by active infection or vaccination. Since these animals lack the active humoral or cellular response specific to the target microorganism, the tendency is the development of the epidemic form of the infection (Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.). In this form, several animals can simultaneously manifest specific clinical signs of disease. In general, they are symptomatic and therefore easier to identify. However, those animals that had the previous infection or those that were previously vaccinated have specific immunological memory, which means that the infection likely will occur in the endemic form. In the endemic presentation, the clinical problems, primarily the embryonic mortalities, may compromise a smaller number of animals for a longer period of time (Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.).

The most important endemic infectious diseases in Brazil are infectious bovine rhinotracheitis, IBR (caused by Alphaherpesvirus 1 - BoHV-1), bovine viral diarrhea, BVD (caused by bovine viral diarrhea virus – BVDV), leptospirosis (cause by Leptospira spp.), vulvovaginitis (caused by Mycoplasma bovigenitalium and Ureaplasma diversum), campylobacteriosis – caused by Campylobacter fetus), trichomoniasis (caused by Tritrichomonas foetus), and neosporosis (caused by Neospora caninum) (Vanroose et al., 2000Vanroose G, de Kruif A, Van Soom A. 2000. Embryonic mortality and embryo-pathogen interactions. Anim Reprod Sci, 60-61:131-43.; Grooms, 2006Grooms DL. 2006. Reproductive losses caused by bovine viral diarrhea virus and leptospirosis. Theriogenology, 66(3):624-628.; Givens and Marley, 2008Givens MD, Marley MS. 2008. Infectious causes of embryonic and fetal mortality. Theriogenology, 70(3):270-285.; Kumar et al., 2011Kumar A, Verma AK, Rahal A. 2011. Mycoplasma bovis, a multi disease producing pathogen: na overview. Asian J Anim Vet Adv, 6(6):537-546.; Almería and López-Gatius, 2013Almería S, López-Gatius F. 2013. Bovine neosporosis: clinical and practical aspects. Res Vet Sci, 95(2):303-309.; Gates et al., 2013Gates MC, Humphry RW, Gunn GJ. 2013. Associations between bovine viral diarrhoea virus (BVDV) seropositivity and performance indicators in beef suckler and dairy herds. Vet J, 198(3):631-637.; Sanhueza et al., 2013Sanhueza JM, Heuer C, West D. 2013. Contribution of Leptospira, Neospora caninum and bovine viral diarrhea virus to fetal loss of beef cattle in New Zealand. Prev Vet Med, 112(1-2):90-98.; Michi et al., 2016Michi AN, Favetto PH, Kastelic J, Cobo ER. 2016. A review of sexually transmitted bovine trichomoniasis and campylobacteriosis affecting cattle reproductive health. Theriogenology, 85(5):781-791.; Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.; Fischer et al., 2018Fischer G, Rodrigues R, Pappen FG, Zanela MB, Ribiero MER, Almeida LL, Souza GN, Weissheimer CF, Pegoraro LMC, Pradieé J. 2018. Principais doenças da bovinocultura leiteira. [In Portuguese]. In Pegoraro, LMC (Ed.). Biosecurity in dairy cattle. Pelotas, BR: Embrapa. pp. 13-27.; Rani et al., 2018Rani P, Dutt R, Singh G, Chandolia RK. 2018. Embryonic mortality in cattle – A review. Int J Curr Microbiol App Sci, 7(7):1501-1516.). However, regardless of the form of presentation, epidemic or endemic, both cause considerable economic losses for both dairy and beef cattle (Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.).

Animal category in a herd

IBR, BVD, and leptospirosis are the three main and most frequent reproductive infectious diseases in the Brazilian cattle herds (Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.; Fischer et al., 2018Fischer G, Rodrigues R, Pappen FG, Zanela MB, Ribiero MER, Almeida LL, Souza GN, Weissheimer CF, Pegoraro LMC, Pradieé J. 2018. Principais doenças da bovinocultura leiteira. [In Portuguese]. In Pegoraro, LMC (Ed.). Biosecurity in dairy cattle. Pelotas, BR: Embrapa. pp. 13-27.). Particularly in relation to beef cattle, the serological profile for these three infectious diseases in a Brazilian cattle herd differs considerably due to the animal category. In most herds the percentages of non-vaccinated and seropositive animals for BoHV-1, BVDV, and Leptospira spp. increase according to the age of the animals. Therefore, the average percentage of nulliparous (heifers) seropositive for these three microorganisms can be considered smaller than the average percentage of primiparous, which is smaller than the average percentage of multiparous cows (Médici et al., 2000Médici KC, Alfieri AA, Alfieri AF. 2000. Prevalence of neutralizing antibodies against bovine herpesvirus type 1, due natural infection, in herds with reproductive problems [In Portuguese]. Cienc Rural, 30(2):347-350.; Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.). In other words, the percentage of animals susceptible to field prime-infection in a breeding season is higher in heifers than in primiparous and multiparous cows, meaning that the two categories composed by the youngest animals in the herd are the most vulnerable. Consequently, sanitary management for reproductive infectious problems in beef cattle should focus on both heifers and primiparous, particularly when evaluating a vaccination program.

Epidemiological profile of infectious reproductive diseases

An action of special importance, particularly directed to the control of reproductive diseases, is to obtain information aiming to define the epidemiological profile of the animals and, mainly, stratifying them according to the animal categories. Serological tests should be performed in a percentage of animals that enable defining the seroepidemiology of IBR, BVD, and leptospirosis, for example. Some tests, including the enzyme-linked immunosorbent assay (ELISA) for viruses are qualitative and enable determining the presence/absence of infection in the herd and/or categories of animals that compose the herd. Other diagnostic tests have additional advantages. This applies to the virus neutralization test, especially because of its simultaneous qualitative and quantitative feature, which means that based on the tritation it is possible to establish the magnitude of antibody titers present in the blood serum. High titers evidence recent infection or viral circulation in the herd (Dubovi, 2013Dubovi EJ. 2013. Laboratory diagnosis of bovine viral diarrhea virus. Biologicals, 41(1):8-13.; Lanyon et al., 2014Lanyon SR, Hill FI, Reichel MP, Brownlie J. 2014. Bovine viral diarrhoea: pathogenesis and diagnosis. Vet J, 199(2):201-209.; Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.).

Even as distinct epidemiological situations the presence of infectious risk factors can influence the occurrence of reproductive problems (Souza et al., 2017Souza, GN; Pegoraro, LMC; Weissheimer, CF; Fischer, G; Dellagostin, O; Bialves, TS; Gindri, P; Lucas, RM; Muller, L; Cavalcanti, F; Weiller, OH. 2017. Situação epidemiológica e fatores de risco para problemas reprodutivos em bovinos leiteiros localizados em diferentes mesorregiões do Estado do Rio Grande do Sul 2016/2017. Embrapa Gado de Leite. Boletim de Pesquisa e Desenvolvimento, 36. Juiz de Fora: Embrapa Gado de Leite, 2017. 22p.). The risk of non-infectious early fetal loss appears to increase under the conditions of intensive management systems (Forar et al., 1995Forar AL, Gay JM, Hancock DD. 1995. The frequency of endemic fetal loss in dairy cattle: a review. Theriogenology, 43(6):989-1000.; Hanzen et al., 1999Hanzen C, Drion PV, Loutrie O, Depierreux C, Christians E. 1999. Embryonic mortality. Part 1. Clinical aspects and etiological factors on the bovine species. Ann Med Vet, 143(2):91-118.). The non-infectious risk factors, such as nutritional disorders, management failures, and environmental conditions, isolated or in association with infectious causes, may play important role in changes of the main parameters used to evaluate the reproductive efficiency in cattle herds (García-Ispierto et al., 2006García-Ispierto I, López-Gatius F, Santolaria P, Yániz JL, Nogareda C, López-Béjar M, De Rensis F. 2006. Relationship between heat stress during the peri-implantation period and early fetal loss in dairy cattle. Theriogenology, 65(4):799-807., 2007aGarcía-Ispierto I, López-Gatius, F, Bech-Sabat G, Santolaria P, Yániz JL, Nogareda C, De Rensis F, López-Béjar M. 2007a. Climate factors affecting conception rate of high producing dairy cows in northeastern Spain. Theriogenology, 67(8):1379-1385.,bGarcía-Ispierto I, López-Gatius F, Santolaria P, Yániz JL, Nogareda C, López-Béjar M. 2007b. Factors affecting the fertility of high producing dairy herds in northeastern Spain. Theriogenology, 67(3):632-638.). The technical level used in the reproductive activity can influence the presence, frequency, and intensity of health problems, and can generate negative results in a production unit. Therefore, all possible causes of reproductive failures, including infectious, non-infectious, current and previous herd health status, and local and regional epidemiological features should be carefully considered for the resolution/control of the problems.

Furthermore, although the considerable benefits, the indiscriminate use of the biotechnologies of reproduction can generate undesirable consequences, especially when used without a careful analysis of the risk factors inherent to the management. Some factors may compromise the health of the herd, such as the intensive use of parturition areas, increased animal population density at certain periods, abundance and agglomeration of young animals, which are more susceptible to infections (Pegoraro et al., 2018Pegoraro LMC, Nunes e Souza G, Pradieé J, Weissheimer CF, Dereti RM, Viegas DP, Saalfed MH, Zanela MB, Almeida LL. 2018. Biosecurity measures - internal and external. [In Portuguese]. In Pegoraro, LMC (Ed.). Biosecurity in dairy cattle. Pelotas, BR: Embrapa. pp.28-41.). In these situations, the risks of environmental contamination with the main reproductive pathogens, that can be eliminated at the time of birth, are higher than those in traditional breeding systems and facilitate the spread of infections that compromise the reproductive system of cattle. As well, the purchase and sale of genetic material (semen, oocytes, and embryos) should follow some safety principles (Carvalho et al., 2007Carvalho LFR, Melo CB, Drummond VO. 2007. Procedures for the exportation and importation of genetic animal material to Brazil. [In Portuguese]. Rev Bras Reprod Anim, 31(3):415-422.). When the material is imported/exported, clinical isolation and observation of donors, and serological and microbiological tests should be performed to ensure the absence of relevant diseases. These also include epidemiological surveillance in areas where artificial insemination is practiced with imported semen. With regard to embryos, proper collection, manipulation, and transfer techniques can prevent many pathogens of concern (Rufino et al., 2006Rufino FA, Seneda MM, Alfieri AA. 2006. Bovine herpesvirus 1 and bovine viral diarrhea virus impact in the embryo transfer [In Portuguese]. Arch Vet Sci, 11(1):78-84.; Carvalho et al., 2007Carvalho LFR, Melo CB, Drummond VO. 2007. Procedures for the exportation and importation of genetic animal material to Brazil. [In Portuguese]. Rev Bras Reprod Anim, 31(3):415-422.). These are some of the examples of non-infectious risks that might be associated with embryonic mortality and other reproductive failures.

Before decision making regarding the health problems causing embryonic mortalities in bovine females, some issues should be raised, such as i) what is the history of the disease in the region and/or in the herd?; ii) how does the microorganism enter the herd?; iii) how is the infection transmitted?; iv) how does the disease remain or how is it kept in the herd (carriers)?; v) are there vectors?; vi) is there an effective treatment?, vii) is there a vaccine to control and prophylaxis?; viii) if it exists, is the vaccine effective?; ix) when and why to vaccinate?; x) are there other controlling forms? Only with answers to these questions is it possible to design an efficient Sanitary Program to reduce the rate of embryonic mortality in beef or dairy bovine herds.

Sanitary program

In animal production “Sanitary Program” can be defined as a thematic unit constituted by a set of actions developed aiming to promote and maintain the animal health. Unfortunately, particularly for cattle, it is usual to summarize or confuse Sanitary Program with Vaccination Program. When available, vaccines areundoubtedly one of the main actions to be implemented in a Sanitary Program. However, besides the importance of prophylaxis as good practices in vaccinations, there are other important issues, specially the control of disease risk factors. Vaccination prophylaxis strategies may loss efficiency due to the maintenance of the risk factors within the herds. Therefore, complementary actions that promote or preserve animal health are of fundamental importance to obtain quantitative and, mainly, qualitative increase in the beef and dairy production chains. This is directly associated with the financial efficiency of production chains.

One of the main tools that, when available and depending on the epidemiological profile of infections, should be included in a Sanitary Program is the vaccine. In the context of a Sanitary Program for the control of embryonic mortalities in bovine herds, some vaccines should be used not as an additional and emergency measure, but should form a “Vaccination Program”.

Considering the herd animal density and intensive management of a dairy herd and aiming to reduce the embryonic mortality caused by viruses (IBR and BVD), a “Vaccination Program” should be applied to all the females of the herd, regardless of the animal category they belong. Although most of the vaccine manufacturers indicate annual revaccination, biannual revaccinations can be recommended (Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.). It depends on the monitoring results of some reproductive parameters, as well as the qualitative and quantitative (titration) epidemiological profile of the herd. Similarly, the manufacturers' revaccination recommendation for leptospirosis control is biannual. However, in our personal experience and on the basis of epidemiological profile and, mainly, on the antibody titers of the seropositive animals we recommend quarterly revaccinations. Also in the regards of leptospirosis, in very specific situations such as high-producing beef and dairy herds, the therapeutic use of antibiotics may also be prescribed in addition to vaccine prophylaxis in order to reduce the time to control the infection in the herd (Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.).

Commercial vaccines against most of the infections associated with bovine embryonic mortality are available in Brazil. As the epidemiological profile of these infections varies considerably, “Vaccination Programs” should consider the individual variations of each herd. It is important to consider the nutritional management with body score analysis when defining a Vaccination Program, since optimal nutrition is important to enhance immunity and mount an appropriate response to vaccination. Therefore, sufficient protein, energy, minerals, and vitamins are all required to develop and maintain a strong immune system (Berge and Vertenten, 2017Berge AC, Vertenten G. 2017. Whitepaper: The importance of preventive health and vaccination programmes in ruminant production. Available from https://www.timetovaccinate.com/. Accessed in: July 7th. 2019.
https://www.timetovaccinate.com/...
). As well, the type of reproductive management should also be considered in the establishment of a Vaccination Program, since pre-breeding vaccination program may improve the health of cows by preventing BVD, trichomoniasis, campylobacteriosis, and leptospirosis (Daly, 2006Daly R. 2006. Timing of reproductive vaccinations in beef cattle herds. In: Proceedings of Applied Reproductive Strategies in Beef Cattle, 2006, Rapid City, South Dakota, USA. p.190-195.; Vasconcelos et al., 2017Vasconcelos, JLM, Carvalho R, Peres RFG, Rodrigues ADP, Junior IC, Meneghetti M, Aono FH, Costa WM, Lopes CN, Cooke RF, Pohler KG. 2017. Reproductive programs for beef cattle: incorporating management and reproductive techniques for better fertility. In Proceedings of the 31st Annual Meeting of the Brazilian Embryo Technology Society (SBTE); Cabo de Santo Agostinho, PE, Brazil, 2017, Anim Reprod, 14(3):547-557.), for example. Vaccinating cows against BoHV-1, BVDV, and Leptospira spp., particularly when both doses are administered before AI or FTAI improve cow reproductive performance (Pereira et al., 2013Pereira MH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of lactating dairy cows submitted to AI. Anim Reprod Sci, 37(3-4):156-162.; Vasconcelos et al., 2017Vasconcelos, JLM, Carvalho R, Peres RFG, Rodrigues ADP, Junior IC, Meneghetti M, Aono FH, Costa WM, Lopes CN, Cooke RF, Pohler KG. 2017. Reproductive programs for beef cattle: incorporating management and reproductive techniques for better fertility. In Proceedings of the 31st Annual Meeting of the Brazilian Embryo Technology Society (SBTE); Cabo de Santo Agostinho, PE, Brazil, 2017, Anim Reprod, 14(3):547-557.). Therefore, a pre-breeding vaccination program aims to increase the chances the cow will breed and ultimately deliver a calf; help the cow become pregnant early in the breeding season; and protect the calf from becoming persistently infected with BVD (Campbell, 2011Campbell J. 2011. Pre-breeding vaccinations. Available from https://www.drovers.com/article/pre-breeding-vaccinations. Accessed in July 8th. 2019.
https://www.drovers.com/article/pre-bree...
).

However, in general, infections with BoHV-1, BVDV and Leptospira spp. are widely disseminated in Brazilian beef cattle (Junqueira and Alfieri, 2006Junqueira JRC, Alfieri AA. 2006. Reproductive failures in beef cattle breeding herds with emphasis for infectious causes [In Portuguese]. Semin Cienc Agr, 27(2):289-298.). Thus, these reproductive infectious diseases are more frequently manifested as endemic and only sporadically as epidemic. As mentioned earlier, in most of the herds, the infection rates among females of different categories vary considerably. It is observed a decreasing percentage rate of seronegative animals and, consequently, more susceptible animals in the nulliparous, primiparous, and multiparous female categories (Junqueira and Alfieri, 2006Junqueira JRC, Alfieri AA. 2006. Reproductive failures in beef cattle breeding herds with emphasis for infectious causes [In Portuguese]. Semin Cienc Agr, 27(2):289-298.).

Another important aspect inherent to the pathogenesis of these three bovine reproductive infectious diseases is the tendency to chronicity. Throughout evolution, the etiological agents responsible for these infections have developed strategies to remain in the herds (Alfieri and Alfieri, 2017Alfieri AA, Alfieri AF. 2017. Infectious diseases that impact the bovine reproduction [In Portuguese]. Rev Bras Reprod Anim, 41(1):133-9.). BoHV-1, by means of viral latency mechanism (Nandi et al., 2009Nandi S, Kumar M, Manohar M, Chauhan RS. 2009. Bovine herpes virus infections in cattle. Anim Health Res Ver,10(1):85-98), is able to maintain the viral genome in the nucleus of infected cells, as provirus. Under this viral condition, the infected animal may remain without clinical signs of infection for a long period (Nandi et al., 2009Nandi S, Kumar M, Manohar M, Chauhan RS. 2009. Bovine herpes virus infections in cattle. Anim Health Res Ver,10(1):85-98). Eventually, the viral latency is broken and the infected animal may present clinical manifestations accompanied by viral re-excretion, perpetuating the infection in the herds (Jones and Chowdhury, 2007Jones C, Chowdhury S. 2007. A review of the biology of bovine herpesvirus type 1 (BHV-1), its role as a cofactor in the bovine respiratory disease complex and development of improved vaccines. Anim Health Res Ver, 8(2):187-205.; Biswas et al., 2013Biswas S, Bandyopadhyay S, Dimri U, Patra PH. 2013. Bovine herpesvirus-1 (BHV-1) - a re-emerging concern in livestock: a revisit to its biology, epidemiology, diagnosis, and prophylaxis. Vet J, 33(2):68-81.). Regarding BVDV, this viral agent is able to persistently infect (PI) calves, which eliminate high BVDV titers throughout their productive lives, contributing to perpetuate the infectious process in a herd (Hamers et al., 1998Hamers C, Lecomte C, Kulcsar G, Lambot M, Pastoret PP. 1998. Persistently infected cattle stabilise bovine viral diarrhea virus leading to herd specific strains. Vet Microbiol, 61(3):177-82.; Moennig and Becher, 2018Moennig V, Becher P. 2018. Control of Bovine ViralDiarrhea. Pathogens, 7(1). pii: E29.). Finally, bovine leptospirosis is considered a chronic infection since most of the times it evolves to chronic kidney disease. The clinical features of the infection, such as the immunological exclusion and intermittent bacterial shedding, make the infection control an important challenge in the herd, especially the serovar Hardjo, which is the most adapted to the bovine species (Adler, 2015Adler B. 2015. History of leptospirosis and leptospira. Curr Top Microbiol Immunol, 387:1-9.; Balamurugan et al., 2018Balamurugan V, Alamuri A, Bharathkumar K, Patil SS, Govindaraj GN, Nagalingam M, Krishnamoorthy P, Rahman H, Shome BR. 2018. Prevalence of Leptospira serogroup-specific antibodies in cattle associated with reproductive problems in endemic states of India. Trop Animal Health Prod, 50(5):1131-1138.).

Concerning the two viral infections (IBR/BVD) this epidemiological feature has a very important practical implication. Depending on the rate of previously infected and, consequently, seropositive animals, in the category of multiparous females the decision to vaccinate or not will depend on a cost-effective analysis of the vaccination. If the decision is vaccinating, a single vaccination dose in the animals of that category is enough, since it is likely that these animals have active immunological memory to these viral agents (Van Drunen Little-van den Hurk, 2006Van Drunen Little-van den Hurk S. 2006. Rationale and perspectives on the success of vaccination against bovine herpesvirus-1. Vet Microbiol, 113(3-4):275-82.). Additionally, also considering the immunological aspects related to a previous infection, the period between vaccination and artificial insemination may beshorter, and may even adapt to the management on day zero of the FTAI (Daly, 2006Daly R. 2006. Timing of reproductive vaccinations in beef cattle herds. In: Proceedings of Applied Reproductive Strategies in Beef Cattle, 2006, Rapid City, South Dakota, USA. p.190-195.; Vasconcelos et al., 2017Vasconcelos, JLM, Carvalho R, Peres RFG, Rodrigues ADP, Junior IC, Meneghetti M, Aono FH, Costa WM, Lopes CN, Cooke RF, Pohler KG. 2017. Reproductive programs for beef cattle: incorporating management and reproductive techniques for better fertility. In Proceedings of the 31st Annual Meeting of the Brazilian Embryo Technology Society (SBTE); Cabo de Santo Agostinho, PE, Brazil, 2017, Anim Reprod, 14(3):547-557.). However, in the categories of more susceptible females, such as nulliparous and primiparous, which have lower rates of seroconversion, the ideal is that before the mating season the animals receive two doses of vaccine with a minimum interval of 21 days between doses (Aono et al., 2013Aono FH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of beef cows submitted to fixed-timed AI in Brazilian cow-calf operations. Theriogenology, 79(2):242-248.; Pereira et al., 2013Pereira MH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of lactating dairy cows submitted to AI. Anim Reprod Sci, 37(3-4):156-162.). Also in this situation the second dose, for management reasons may coincide with the day of initiation of the FTAI protocol.

Vaccination vs. reproductive performance of cattle

Hundreds of scientific articles published in peer-reviewed and indexed journals that are available in relevant scientific databases, including Web of Science, PubMed, CAB Abstracts, and others analyzed different variables regarding the vaccination of beef and dairy cattle to control reproductive infections, such as IBR and BVD. These several articles were found by the authors of two meta-analysis based-studies aimed to evaluate the results of vaccination against BoHV-1 and BVDV on the reproductive performance of cattle herds (Newcomer et al., 2015Newcomer BW, Walz PH, Givens MD, Wilson AE. 2015. Efficacy of bovine viral diarrhea virus vaccination to prevent reproductive disease: a meta-analysis. Theriogenology, 83(3):360-365.; Newcomer et al., 2017Newcomer BW, Grady Cofield L, Walz PH, Givens MD. 2017. Prevention of abortion in cattle following vaccination against bovine herpesvirus 1: A meta-analysis. Prev Vet Med, 138:1-8.). In these studies, variables such as the type of reproductive management, body score, herd size, vaccination and/or revaccination program, infection epidemiology in the herds (rate of seropositive animals and antibody titers), type of vaccine (monovalent, polyvalent, inactivated, attenuated), among other less studied aspects were analized. Although the results considerably vary, most studies conclude that vaccination increases the reproductive performance of herds (Pospísil et al., 1996Pospísil Z, Krejcí J, Machatková M, Zendulková D, Lány P, Cíhal P. 1996. The efficacy of an inactivated IBR vaccine in the prevention of intra-uterine infection and its use in a disease-control programme. Zentralbl Veterinarmed B, 43(1):15-21.; Grooms, 2004Grooms DL. 2004. Reproductive consequences of infection with bovine viral diarrhea virus. Vet Clin North Am Food Anim Pract, 20(1):5-19.; Ficken et al., 2006Ficken MD, Ellsworth MA, Tucker CM. 2006. Evaluation of the efficacy of a modified-live combination vaccine against abortion caused by virulent bovine herpesvirus type 1 in a one-year duration-of-immunity study. Vet Ther, 7(3):275-282.; Zimmerman et al., 2007Zimmerman AD, Buterbaugh RE, Herbert JM, Hass JM, Frank NE, Luempert Iii LG, Chase CC. 2007. Efficacy of bovine herpesvirus-1 inactivated vaccine against abortion and stillbirth in pregnant heifers. J Am Vet Med Assoc, 231(9):1386-9.; Aono et al., 2013Aono FH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of beef cows submitted to fixed-timed AI in Brazilian cow-calf operations. Theriogenology, 79(2):242-248.; Pereira et al., 2013Pereira MH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of lactating dairy cows submitted to AI. Anim Reprod Sci, 37(3-4):156-162.; Ridpath, 2013Ridpath JF. 2013. Immunology of BVDV vaccines. Biologicals, 41(1):14-9.; Newcomer et al., 2015Newcomer BW, Walz PH, Givens MD, Wilson AE. 2015. Efficacy of bovine viral diarrhea virus vaccination to prevent reproductive disease: a meta-analysis. Theriogenology, 83(3):360-365.; Newcomer et al., 2017Newcomer BW, Grady Cofield L, Walz PH, Givens MD. 2017. Prevention of abortion in cattle following vaccination against bovine herpesvirus 1: A meta-analysis. Prev Vet Med, 138:1-8.).

Newcomer et al. (2015)Newcomer BW, Walz PH, Givens MD, Wilson AE. 2015. Efficacy of bovine viral diarrhea virus vaccination to prevent reproductive disease: a meta-analysis. Theriogenology, 83(3):360-365. evaluated the impact of BVDV vaccination on three outcomes in cows: risk of fetal infection, abortion risk, and pregnancy risk. Forty-six studies in 41 separate papers matched the inclusion criteria. The analysis revealed a decrease in abortions of nearly 45% and a nearly 85% decrease in fetal infection rate in cattle vaccinated for BVDV compared with unvaccinated cohorts. Additionally, pregnancy risk was increased by approximately 5% in field trials of BVDV vaccinations. This meta-analysis provided quantitative support for the benefit of vaccination in the prevention of BVDV-associated reproductive disease.

The meta-analysis study developed by Newcomer et al. (2017)Newcomer BW, Grady Cofield L, Walz PH, Givens MD. 2017. Prevention of abortion in cattle following vaccination against bovine herpesvirus 1: A meta-analysis. Prev Vet Med, 138:1-8. comprised the analysis of 15 experiments in 10 manuscripts involving more than 7,500 animals. The aim of this meta-analysis was to determine the cumulative efficacy of BoHV-1 vaccination to prevent abortion in pregnant cattle. Risk ratio effect sizes were used in random effects, weighted meta-analyses to assess the impact of vaccination. A 60% decrease in abortion risk in vaccinated cattle was demonstrated. This meta-analysis provided quantitative support for the benefit of BoHV-1vaccination in the prevention of abortion.

Brazilian vaccination based-studies

In the central-western region of Brazil, Aono et al. (2013)Aono FH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of beef cows submitted to fixed-timed AI in Brazilian cow-calf operations. Theriogenology, 79(2):242-248. evaluated the reproductive efficiency of 16 herds of beef cattle, of which 13 herds did not vaccinate and three herds were regularly vaccinated for IBR, BVD, and leptospirosis. All animals were submitted to the same FTAI protocol and the pregnancy rate was determined by transrectal ultrasonography at 30 and 120 days post-FTAI. The mean rate of pregnancy loss was significantly lower in the animals of the vaccinated herds when compared with the mean rate of embryonic loss observed in animals from unvaccinated herds. Concerning the category of cows, authors also observed a reduction in the embryonic mortality at 30 and 120 days post-FTAI in vaccinated and non-vaccinated primiparous cows.

Also in the Midwest Brazilian region, the effect of vaccination against IBR, BVD, and leptospirosis was evaluated from six commercial herds of beef cattle. From a total of 1,968 cows, 953 were vaccinated and 1,015 were not-vaccinated. The body score was similar for both groups. The reproductive management and diagnosis of gestation were performed as in the previous experiment. The pregnancy rate was significantly higher in the vaccinated group at both 30 and 120 days of gestation. In the group of primiparous cows there was a significant reduction in embryonic mortality. However, vaccination had no effect in the multiparous cow group (Aono et al., 2013Aono FH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of beef cows submitted to fixed-timed AI in Brazilian cow-calf operations. Theriogenology, 79(2):242-248.).

Alternative vaccination schemes for IBR, BVD, and leptospirosis were also compared. In this experiment, the influence of the day of the first vaccination in relation to the initiation of the FTAI protocol on the pregnancy and pregnancy loss rates in primiparous Nelore cows was analyzed. Two groups of vaccinated animals were constituted. In the first group (pre-vaccinated) the first dose of vaccine was administered 30 days before the initiation of the FTAI protocol and the second dose coincided with the initiation of the protocol. The second group of cows received the first dose on the day of initiation of the FTAI protocol and the second dose 30 days after the end of the protocol. There was an effect of the vaccination scheme used on the pregnancy rate at 30 and at 120 days, being higher in the pre-vaccinated group. However, the vaccination protocol had no effect on the rate of pregnancy loss or embryo mortality (Aono et al., 2013Aono FH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of beef cows submitted to fixed-timed AI in Brazilian cow-calf operations. Theriogenology, 79(2):242-248.).

In a series of four experiments, Pereira et al. (2013)Pereira MH, Cooke RF, Alfieri AA, Vasconcelos JL. 2013. Effects of vaccination against reproductive diseases on reproductive performance of lactating dairy cows submitted to AI. Anim Reprod Sci, 37(3-4):156-162. also evaluated the effect of different vaccination schemes against IBR, BVD, and leptospirosis in dairy herds of Minas Gerais and Paraná states. The four studies involved the total of 3,640 Holstein or Gir x Holstein lactating cows. All the animals of each study received two doses of vaccines, which were administered in different periods based on the beginning of the FTAI protocol. The results showed that pregnant rates were higher in the groups that received the two doses of vaccine before the time of the FTAI in relation to the control group. As well, pregnancy rates were higher in comparison with the group that received thefirst dose of the vaccine at the moment of FTAI. Therefore, it was concluded that when both doses of vaccines are administered prior to AI there is improve of the reproductive efficiency in dairy production systems.

Biosecurity

Currently in Brazil, the concept of biosecurity is easily associated with animal health involving the pork and poultry production chains, particularly due to the higher animal density in these both production systems. In Brazilian cattle breeding, the concepts of biosecurity are still very little used. However, we have recently observed in dairy cattle the beginning, albeit timid, of the application of some standards of biosecurity, particularly in herds with high genetics and production. Nevertheless, in the vast majority of Brazilian beef cattle, this important action for the control and prophylaxis of infectious diseases is still neglected.

Important actions must be implemented and regularly monitored in order to increase the biosecurity of the herds. Some are easier to be implemented, while others are more complex. Even at reduced percentages, some of these actions can change production costs, while in others there is practically no additional cost.

Biosecurity can be divided into two types, external and internal. External biosecurity is related to measures aimed at preventing the entry of pathogens into the cattle herd. Measures related to this type of biosecurity include quarantine before the introduction of newly acquired animals, and transit restriction of vehicle, person, and animals. Meanwhile, internal biosecurity is related to the decrease in the chance of transmission of pathogens present within the same cattle herd. Measures should be taken to clean and disinfect the installation, to provide adequate facilities according to the different age groups, to separate diseased animals (isolated facilities), to control rodent and other synanthropic animals, to perform correct disposal of dead animals avoiding the transmission of infectious agents, and to promoted the animal welfare (Sarrazin et al., 2014Sarrazin S, Cay AB, Laureyns J, Dewulf J. 2014. A survey on biosecurity and management practices in selected Belgian cattle farms. Prev Vet Med, 117(1):129-139.; Sahlström et al., 2014Sahlström L, Virtanen T, Kyyrö J, Lyytikäinen T. 2014. Biosecurity on Finnish cattle, pig and sheep farms - results from a questionnaire. Prev Vet Med, 117(1):59-67.; Pegoraro et al., 2018Pegoraro LMC, Nunes e Souza G, Pradieé J, Weissheimer CF, Dereti RM, Viegas DP, Saalfed MH, Zanela MB, Almeida LL. 2018. Biosecurity measures - internal and external. [In Portuguese]. In Pegoraro, LMC (Ed.). Biosecurity in dairy cattle. Pelotas, BR: Embrapa. pp.28-41.).

Conclusion

Depending on the epidemiology of BoHV-1, BVDV and Leptospira spp. infection in a cattle herd, especially in certain categories of females of the herd, as well as the vaccination scheme used for the control and prophylaxis of these reproductive diseases the use of vaccines can contribute considerably to the increase the pregnancy rates and reduce embryonic mortality rates in both the Brazilian beef and dairy cattle herds.

Acknowledgments

The authors thank the following Brazilian Institutes for financial support: the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES), the National Council of Technological and Scientific Development (CNPq), Financing of Studies and Projects (FINEP), and the Araucaria Foundation (FAP/PR). AA Alfieri and AF Alfieri are recipients of CNPq fellowships. RA Leme is a recipient of the CAPES fellowship. AM Dall Agnol Leme is a recipient of the FAP/PR fellowship.

  • FundingThis work was supported by the INCT-Leite under Grant (Number 465725/2014-7).

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Publication Dates

  • Publication in this collection
    28 Nov 2019
  • Date of issue
    Jul-Sep 2019

History

  • Received
    29 May 2019
  • Accepted
    30 July 2019
Colégio Brasileiro de Reprodução Animal Coronel José dias Bicalho, 1224, CEP: , 31275-050, Belo Horizonte, MG - Brasil, Tel.: 55-31-3491 7122 - Belo Horizonte - MG - Brazil
E-mail: animreprod@cbra.org.br