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Revista mexicana de ciencias pecuarias

versión On-line ISSN 2448-6698versión impresa ISSN 2007-1124

Rev. mex. de cienc. pecuarias vol.12  supl.3 Mérida nov. 2021  Epub 24-Ene-2022

https://doi.org/10.22319/rmcp.v12s3.5848 

Reviews

Background and perspectives of certain priority diseases affecting cattle farming in Mexico

Carmen Rojas Martíneza 

Elizabeth Loza Rubiob 

Sergio Darío Rodríguez Camarilloa 

Julio Vicente Figueroa Millána 

Francisco Aguilar Romerob 

Rodolfo Esteban Lagunes Quintanillaa 

José Francisco Morales Álvarezb 

Marco Antonio Santillán Flores

Guadalupe Asunción Socci Escatellb 

Jesús Antonio Álvarez Martíneza  * 

a Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. CENID Salud Animal e Inocuidad, Carretera Cuernavaca-Cuautla 8534. Col. Progreso Jiutepec, 62574 Morelos. México.

b Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. CENID Salud Animal e Inocuidad. Ciudad de México. México.


Abstract

The review focused on concisely presenting the contributions that INIFAP researchers have developed, directly or in collaboration with researchers from other institutions, on different aspects of the diseases that affect cattle farming in Mexico. It describes the research on viral diseases such as rabies and bovine viral diarrhea; bacterial diseases such as anaplasmosis, brucellosis, tuberculosis, paratuberculosis, leptospirosis and bovine respiratory disease, and among parasitic diseases, tick infestation and babesiosis. It identifies potential lines of research that can help mitigate the impact of diseases on production. It considers contributions on the development or adaptation of serological and molecular diagnostic techniques and the diagnosis of resistance to ixodicides. In addition, it indicates epidemiological parameters of the diseases and makes reference to the biologics generated, which include vaccines against rabies, anaplasmosis and babesiosis; bacterin against leptospirosis, and a bacterin-toxoid against pneumonia. It also discusses the evaluations of the use of BCG against tuberculosis and a new generation vaccine against brucellosis. The review concludes that the research of INIFAP in animal health must necessarily have the omic sciences as a perspective. This is the only way to complement the understanding of disease mechanisms, the development of new diagnostic techniques and the design of effective and safe vaccines. Therefore, the great challenge will be the involvement of the animal health area in the concept of "One Health".

Key words Diseases; Vaccines; Prevention; Control

Resumen

La revisión se enfocó en presentar de manera concisa las aportaciones que investigadores del INIFAP, han desarrollado directamente o en colaboración con investigadores de otras instituciones sobre diferentes aspectos de las enfermedades que afectan a la ganadería bovina en México. Se describen investigaciones sobre enfermedades virales como la rabia y la diarrea viral bovina; bacterianas como la anaplasmosis, brucelosis, tuberculosis, paratuberculosis, leptospirosis y enfermedad respiratoria bovina; de las enfermedades parasitarias se incluye a la infestación por garrapatas y a la babesiosis. Se identifican posibles líneas de investigación que pueden coadyuvar a mitigar el impacto de las enfermedades en la producción. Se señalan aportes sobre el desarrollo o adaptación de técnicas diagnósticas de tipo serológico y molecular y se considera el diagnóstico de resistencia a los ixodicidas. Además, se indican parámetros epidemiológicos de las enfermedades y se refieren los biológicos generados que comprenden vacuna contra rabia, anaplasmosis y babesiosis; bacterina contra leptospirosis y una bacterina-toxoide contra neumonías. Asimismo, se comentan las evaluaciones del uso de BCG contra tuberculosis y una vacuna de nueva generación contra la brucelosis. En la revisión se concluye que la investigación del INIFAP en salud animal debe forzosamente tener como perspectiva las ciencias ómicas. Solo así se complementará el entendimiento de los mecanismos de las enfermedades, el desarrollo de nuevas técnicas diagnósticas y el diseño de vacunas efectivas y seguras. De modo que el gran reto será el involucramiento del área de salud animal al concepto de "Una Salud".

Palabras clave Enfermedades; Vacunas; Prevención; Control

Introduction

The purpose of livestock production is to produce quality food that is affordable for society and obtained in a sustainable environment, which is difficult in the face of a growing need for meat and milk. INIFAP researchers maintain a constant attention to the demands of producers, through the generation of scientific knowledge and technological innovation in animal health problems.

In Mexico, the inventory is slightly more than 34 million cattle1, which are exposed to viral, bacterial or parasitic pathogens, which often behave as co-infections or complexes. The distribution and frequency of diseases vary according to the interactions between the pathogen, the bovine host and the ecological conditions. Its occurrence causes different rates of morbidity, mortality and low productivity, with a detrimental effect on the use of the production potential, and inherently generates trade restrictions at both the national and international levels. It has been estimated that a disease outbreak can affect 20% of the commercial activities related to the herd2. Diseases involve a wide variability in the cost-benefit ratio of prevention and control programs, which results in underestimates of the impact on production, and, consequently, in inconsistency in the information on losses. It is also important to note that certain bovine diseases affect the human population3. Each disease has a different economic burden that is determined through direct costs, indirect costs of consumption or loss of resources; in general terms, it includes human, structural and economic resources. The objective of this review is to present in a concise manner the contributions that INIFAP researchers have made, directly or in collaboration with researchers from other institutions, on different aspects of the main diseases affecting cattle in Mexico. At the same time, the aim is to identify lines of research to mitigate the impact of diseases on production.

Bovine paralytic rabies

Bovine paralytic rabies (BPR), also known in Spanish as derriengue, is an encephalitis caused by a negative-strand RNA virus of the Rhabdoviridae family and of the genus Lyssavirus. In Mexico, the main transmitter is the chiropteran Desmodus rotundus, a hematophagous bat, distributed in Latin America from the coasts of Mexico to the north of Argentina4. In Mexico, BPR is a frequent disease: 284 positive cases were diagnosed in 20195.

Contributions by INIFAP

Diagnosis. In endemic countries such as Mexico, diagnosis is critical for the prevention and control of rabies. The reference test is direct immunofluorescence (DIF); however, in tropical climates, the brain tissue frequently exhibits decomposition when handled, which makes it impossible to perform the diagnosis or leads to false negative results. Therefore, a real-time polymerase chain reaction test (RT-PCR) was developed based on the sequences of 40 virus isolates from different reservoirs and geographical areas of the country. For this purpose, primers were designed for the N gene, which is the most conserved gene of the virus. With the application of the test, sensitivity, specificity and predictive value rates of 86, 91 and 96 %, respectively, were obtained6. The virus was also detected in samples stored at 27 °C for 23 days. Thus, RT-PCR is currently accepted as an excellent alternative for virus diagnosis7.

Molecular Epidemiology. INIFAP researchers have pioneered the antigenic and molecular characterization of the rabies virus. They performed the detection of antigenic variants using a panel of monoclonal antibodies obtained from the Pasteur Institute in Paris, France8. Subsequently, using monoclonal antibodies from the U.S. Center for Disease Control, they achieved molecular characterization of samples from humans and domestic and wild animals collected from 1990 to 1995. Thus, they recognized a new cycle, called "hypervariables", circulating in skunks in Baja California Sur. At the same time, antigenic and molecular variants circulating in vampires and other wildlife were identified9,10. In a collaborative study with researchers from the Pasteur Institute, the main epidemiological cycles of rabies in Mexico were determined using the Restriction Fragment Length Polymorphism (RFLP) technique8. In other research, using a portion of the P gene, it was discovered that a variant of the virus that circulates in cats also circulates in the bat Tadarida brasiliensis11,12.

Vaccination. The use of gamma radiation with a Cobalt-60 source made it possible to maintain the potency, safety, stability, and shelf life of traditional vaccines13-16. In the application of a gene vaccine in dogs, it was possible to successfully replace the gene gun with an insulin syringe17.

Edible rabies vaccines were generated using the N gene expressed in the tomato; however, a low level of immunogenicity was obtained18. In contrast to the G protein expressed in carrot embryogenic callus, it provided a 60% protection in mice19. Subsequently, an anti-rabies vaccine was produced in corn, whereby the protection was increased to 80% in sheep in the face of a challenge with a lethal virus4.

Recent collaborative research has uncovered differences in Toll-like receptors (TLR) between chiropterans and terrestrial mammals20. The Nature series has published the hologenome of the vampire, and it has been inferred that the hematophagous bat has adapted to blood through a close relationship between its genome and the gut microbiome21.

Perspectives. In tropical conditions, the maintenance of the cold chain is a serious inconvenience; therefore, a thermostable vaccine must be generated for massive use. Also, mass testing for neutralizing antibodies associated with protection must be carried out in order to evaluate the effectiveness of vaccines. In addition, it is essential to produce a good quality conjugate that will allow high sensitivity, specificity and lower cost of the test.

Bovine viral diarrhea

Bovine viral diarrhea (BVD) is a globally distributed disease that causes significant losses to livestock. The causal agent is a Pestivirus of the Flaviviridae family, which has an immunosuppressive effect that facilitates secondary or concomitant infections. It affects the digestive, respiratory and reproductive systems, and is a component of the bovine respiratory complex22. The virus has high genetic variability and is classified into two genotypes and several subgenotypes.

Contributions by INIFAP

Epidemiology. In Mexico, the first description of BVD was made in 1975, specifically in cattle with reproductive problems in which circulating antibodies were detected23. INIFAP studies have been limited to understanding the epidemiology and measurement of risk factors. However, the presence of subgenotypes 1a, 1b, 1c and 2a has been demonstrated in Mexico24.

A report describes a sampling of dairy cattle in different states of the country, in which a seroprevalence of 78.8% was determined. In the same study, the significant risk factors were herd size, pens, intensive production, and long inter-calving periods25.

Perspectives. The high prevalence of BVD suggests the opportunity to create lines of basic and applied research for the prevention and control. The ideal challenge would be the elimination of BVD, for which a vaccine should be developed with Mexican isolates representing the subgenotypes present. It would be desirable to develop new generation vaccines, as well as diagnostic techniques with high sensitivity and specificity for recognizing concomitant infections.

Bovine Anaplasmosis

Bovine anaplasmosis is a disease caused by the Gram-negative bacterium Anaplasma marginale, which affects mostly grazing cattle in tropical areas where the largest livestock populations are concentrated in extensive farms in Mexico. The disease can cause up to 25% of the total death losses of animals moved to the tropics for breeding programs26. The clinical form is manifested by anemia, jaundice, lack of appetite, loss of weight and milk production, miscarriage in the third third, and death. At INIFAP, the Anaplasmosis Unit was founded by Dr. Ramón Aboytes Torres in 1994, where research on diagnosis, epidemiology, bovine immune response, in vitro culture of the bacteria, and the generation of vaccines is carried out.

Contributions by INIFAP

Diagnosis and epidemiology. Serological and molecular studies have been performed, and prevalence rates of 50% have been estimated in northern Veracruz27. Serological diagnosis was improved with the development of an indirect enzyme-linked immunosorbent assay (ELISAi), which has been adopted by SENASICA28. In molecular epidemiology studies using the msp1 α and msp4 genes as markers, Mexican strains have been observed to have a distribution that allows to assume their migration. Several strains of A. marginale present in Mexico were also found to be more similar to those characterized in Brazil than to U.S. strains29. More than 20 strains are stored in the laboratory, having been collected in different states of the Republic and used for testing conserved antigens30,31.

Immunity and vaccines against anaplasmosis. A. marginale infects mature erythrocytes; this makes it behave as an extracellular bacterium, since it does not infect nucleated cells and, therefore, does not induce a typical Tc response with CD8+ cells, but prompts a Th1 response. This Th1-type immune response model had been previously postulated32; at INIFAP, it was tested in calves that normally establish infection but resist the clinical occurrence of the disease. The model was also corroborated in adult cattle, in which a Th1-type response was observed, associated with the presence of IgG2, Interferon- γ and CD4+ T-helper (Th) lymphocytes, which is essential for resistance to the clinical occurrence of anaplasmosis33.

An inactivated immunogen was developed to induce protective immunity to a homologous challenge28,34,35. In the search for broad-spectrum alternatives, a strain of A. marginale from the state of Yucatan was identified, which was named "Tizimín" and characterized as a strain of low natural virulence36. This strain was used as a vaccine and was shown to protect against a heterologous challenge in cattle vaccinated with doses of 1x104-1x1010(37. The inactivated immunogen has been used to vaccinate both local and imported animals in Veracruz and Tamaulipas, thus contributing to reduce the morbidity and mortality due to anaplasmosis. On the other hand, the use of live immunogen has been limited due to the difficulty to maintain it in liquid nitrogen. In Mexico, the most important biological vector of A. marginale is known to be the Rhipicephalus microplus tick38,39. Trans-ovarian transmission was demonstrated in the laboratory this was done with R. microplus larvae that were fed on infected cattle and which subsequently transmitted the infection to susceptible cattle40.

Genome studies. The first complete genome of A. marginale was published in 200541, revolutionizing the study of potential vaccine candidates against this bacterium. Today, there are 23 complete sequences, including seven Mexican strains42,43. Membrane proteins with vaccine potential have been analyzed for the development of immunogens44, and trials have been conducted with recombinant proteins or synthetic peptides31. However, there is still no immunogen capable of fully protecting experimentally or naturally challenged cattle against this bacterium. Currently, in the Anaplasmosis Unit, studies focus on these sequences in order to include proteins associated with transport, signaling or metabolic pathways in the design of vaccines30.

Perspectives. After the publication of the 23 genomes of A. marginale, the sequences are to be analyzed by bioinformatics procedures in order to establish criteria for the identification of vaccine candidates linked to vital or virulence functions. Currently, there are examples of multi-epitope vaccines and reverse vaccinology strategies; thus, INIFAP research group according is making use of these tools to design new vaccines against A. marginale30. It is very likely that proteins other than those already studied will be identified for inclusion in a vaccine. This may take place within a period of five years, at which time an immunogen will be widely and safely used.

Brucellosis

Brucellosis is an infectious disease caused by bacteria of the genus Brucella that affects different domestic species such as cattle, sheep and goats. The most important species that affects cattle is Brucella abortus45. In Mexico, brucellosis is the main zoonosis of bacterial origin. In cattle, the most notorious clinical signs are reproductive, including miscarriage and reduction of milk production, which have a high impact on cattle farming. For the purpose of controlling the disease in the country, there is a National Campaign against Brucellosis in animals, which applies the NOM-041-ZOO-1995 standard based on diagnosis and vaccination.

Nationally, B. abortus strains S19 and RB51 are used for immunization of cattle. S19 induces the presence of antibodies in serum and milk, but interferes with official diagnostic tests; therefore, the alternative is RB5146-49. For diagnosis, the most commonly used serological methods are the 8% card test and the rivanol test50; these tests detect antibodies against the components of the outer membrane of Brucella, directed against the O-chain of the lipopolysaccharide (LPS), which is the most antigenic structure of the smooth strains51.

Despite the efforts made in the campaign, brucellosis in Mexico continues to have an unfavorable effect on animal and human health. Prevalence in production units is higher than 20%; in humans, an average of 3,000 new cases are reported each year according to Ministry of Health of Mexico (Secretaría de Salud), CENAPRECE 2013-2018).

Contributions by INIFAP

At INIFAP, researchers have made relevant contributions to the campaign in multiple aspects. The diagnostic tests that are applied directly or indirectly have been the result of its research, and are endorsed by the Mexican Official Standard. The tests utilized are Rose Bengal, rivanol, complement fixation and ring in milk. However, with the use of these tests, it is difficult to differentiate between vaccinated and infected animals, especially in those that are revaccinated; this issue has been solved with the radial immunodiffusion (RID) test52. In turn, this test facilitated the development of other tests with greater sensitivity and specificity, such as ELISA and polarized fluorescence, in which the polysaccharide known as native hapten (NH) is used as antigen49,53.

In relation to the pathogenesis of brucellosis, it was studied the survival and intracellular trafficking of the vaccine strain RB51 vs. field strains in phagocytic cells. Thus, a shorter survival time of the vaccine strain was observed, and a lower probability of causing disease was inferred54.

The effect of revaccination and the management of infected herds were evaluated in order to demonstrate the effectiveness of the vaccines used in the campaign. Trials have also been carried out with new generation vaccines such as rfbK mutants47,55,56. The RB51 vaccine exposed the potential risk to public health, as it was shown to be eliminated in the milk and vaginal secretions of cows57. Although the RB51 vaccine strain displaced Strain 19, its real protective potential is still unknown, although its efficacy in eliminating reagent animals to conventional tests has been demonstrated. Vaccination per se has not been sufficient to reduce the high incidence of the bacterium in infected herds46,47. Vaccination with the RB51 strain has been described as not interfering with official diagnostic tests because it lacks the "O" chain. While some positive "outlier" responses have been observed, these have been attributed to contact with field strains that occurred during the studies58,59. The use of the rough mutants RB51 and rfbK as vaccines has been described as inducing adequate protection in a herd under medium prevalence conditions56.

Perspectives. Despite the existence of the national campaign for the control of brucellosis, the prevalence and incidence of the disease remain at a level that has economic and social repercussions. Therefore, the prevention and control of brucellosis could be approached under the concept of "One Health"; this would involve producers and authorities in charge of animal and human health. Technically, projects should be continued to improve the efficacy and safety of existing vaccines and to develop new types of vaccines.

Tuberculosis

Bovine tuberculosis is a chronic disease caused by the mycobacterium Mycobacterium bovis, which belongs to the Mycobacterium tuberculosis complex. M. bovis affects a wide variety of species, including humans. In Mexico, tuberculosis is the second most important zoonosis of bacterial origin after brucellosis60. Control depends on the application of the Mexican Official Standard NOM-031-ZOO-1995 of the National Campaign Against Bovine Tuberculosis (Mycobacterium bovis)61, whose strategy is based on the diagnosis and elimination of reagents. The diagnosis is performed with the tuberculin test, using as antigen the bovine purified protein derivative (PPD) made with M. bovis strain AN5. Bovine PPD is applied in the caudal fold or at par with avian PPD made with M. avium strain D4, in a comparative cervical test62. Animals positive to this test are sent to the slaughterhouse; the diagnosis is confirmed by specific bacteriological analysis and by histopathology of granulomatous lesions, which is established in NOM-031-ZOO-199561. In Mexico, the prevalence is usually above 2.5 % in milk production units; it is lower in beef cattle, but in both systems it affects the commercialization of cattle. More than 15,000 new cases of tuberculosis are reported in humans each year (Secretaría de Salud, CENAPRECE 2017).

Contributions by INIFAP

INIFAP, through its researchers, has contributed to the development and application of the different diagnostic techniques applied in the campaign, which are endorsed by the Mexican Official Standard. An outstanding contribution is a study that proved that the tuberculin test does not identify animals in the terminal stages of tuberculosis. Therefore, complementary tests such as ELISA, Interferon-γ and spoligotyping were implemented to improve the reliability of the diagnosis and identify these anergic animals62.

The use of sodium tetraborate in the isolation of mycobacteria was established as a routine procedure for the optimal preservation of samples for up to 90 days; this is also a contribution made by INIFAP researchers. Another contribution was the use of PCR and histopathological analysis with Ziehl-Neelsen staining, which improved the sensitivity and specificity of bacteriological culture63. A major achievement was the development of end-point PCR and Multiplex PCR tests, with which it is possible to differentiate between animals vaccinated with BCG and those infected with field strains64,65.

In Mexico, there is no authorized vaccine to prevent tuberculosis in animals; however, INIFAP has conducted studies of the BCG vaccine used in humans to evaluate its protective capacity in animals. Laboratory animals have been used as models and preliminary tests have been carried out in cattle. In a study of calves vaccinated with BCG and challenged with a pathogenic strain of M. bovis, a marked reduction in granulomatous lesions was demonstrated. Therefore, its use has been suggested for the control of tuberculosis in high prevalence areas66.

Perspectives. The scientific information that has been generated, in association with with the existence of a campaign for the control of tuberculosis with an Official Standard, suggests that an efficient control of bovine tuberculosis is feasible. However, the suitability of the use of BCG vaccine, which is currently the only vaccine in existence to prevent tuberculosis in cattle, must be solidly demonstrated. At the same time, an alternative line of research should be established for another vaccine that will not interfere with discrimination between vaccinated and infected animals, which would reduce the prevalence and allow efficient control of bovine tuberculosis.

Paratuberculosis

Paratuberculosis is a chronic infectious disease affecting cattle, sheep and goats. It is caused by Mycobacterium avium subspecies paratuberculosis (Map); it is characterized by granulomatous lesions in the small intestine. This disease causes nutrient malabsorption syndrome, loss of physical condition in infected animals, and a reduction of productive capacity. The etiological agent is eliminated in feces; therefore, the animals become infected by ingesting contaminated colostrum, milk, feed, or water. The slow spread of the disease and its chronic course cause periodic economic losses67.

Contributions by INIFAP

Researchers at former CENID-Microbiología obtained a protoplasmic antigen from a strain called Map 3065, derived from a clinical case of a sheep. This antigen was used to standardize agar immunodiffusion techniques (IDGA) and enzyme-linked immunosorbent assay (ELISA)68.

In Mexico, epidemiological indicators have been determined in production units (PU) in the states of Chihuahua, Coahuila, Sinaloa, Durango, San Luis Potosí, Jalisco, Aguascalientes, Guanajuato, Querétaro, Hidalgo, Puebla, Chiapas, and Veracruz. Prevalences ranged from 1.0 to 32.37 % in the different states; in each individual PU, prevalences ranged from 1.0 to 88.87 %. In another epidemiological study, the presence of paratuberculosis was associated with the sanitary conditions of each PU, which allowed the issuance of sanitary management recommendations for the control of the disease67,69,70,71.

Another technique that was implemented was the fluorescence polarization assay (FPA), which improved the epidemiological sensitivity and specificity rates72. A PCR was also implemented, in which DNA is extracted from feces, milk, cheese, or tissues with lesions. Using this technique, cases of serology-negative animals are confirmed, which, if they remain in the herd, would be the main source of infection. Thus, PCR is useful as a confirmatory test for the disease.

In addition, a nested PCR (nPCR) has been standardized, for which primers were designed to amplify a region of the IS900 insertion sequence gene specific for Map. With nPCR, results are obtained in a shorter time, and high sensitivity and specificity are attained. It should be contrasted with bacteriological isolation, which regularly requires 16 weeks73.

Perspectives. In order to understand the processes of humoral and cellular immunity of cattle to M. avium subspecies paratuberculosis, it is necessary to generate a line of research, and the challenge will be to develop an effective immunogen for the prevention of the disease.

Bovine respiratory disease

This is a multifactorial disease involving exposure to viral, bacterial, environmental and physiological stressors affecting the cattle. It has been described as the most common and costly disease afflicting cattle worldwide. Clinical manifestations include fever (>40°C), nasal and ocular discharge, dyspnea, poor appetite, depression, prostration, and death. The economic impact due to morbidity, mortality, treatment costs, and lower production is substantial.

Bovine respiratory disease (BRD) involves infectious bovine rhinotracheitis (IBR), bovine respiratory syncytial virus (BRSV), bovine viral diarrhea virus (BVDV), parainfluenza-3(PI3), and bovine herpes virus type 1 (BHV1). Viruses create conditions conducive to the colonization and replication of bacteria, facilitating their adhesion to infected cells. Thus, in cattle with viral infections and subjected to stressful conditions, severe respiratory infections associated with bacteria are present. The most frequent are Mannheimia haemolytica, Pasteurella multocida, and Histophilus somni; these are normally part of the microbiota of the upper respiratory tract. They possess various virulence factors, M. haemolytica produces a leukotoxin that affects ruminant leukocytes; P. multocida has an antiphagocytic capsule and lipopolysaccharides; H. somni can survive intracellularly and is capable of producing biofilm74. The complex is capable of altering the functions of alveolar macrophages, suppressing lymphocyte proliferation, inducing apoptosis, modifying cytokine expression, and triggering an inflammatory process75.

Contributions by INIFAP

A collaborative project called "Pneumonic Complex in Ruminants”, with the aim of determining the bacterial genera involved in BRD, their serotypes and resistance to chemotherapeutics, was developed between INIFAP former CENID-Microbiología and UNAM. This project allowed the isolation of H. somnus (H. somni)76, P. haemolytica (M. haemolytica), and P. multocida. These bacteria were also serotyped and characterized for resistance to chemotherapeutics. Likewise, it was found that most of the M. haemolytica serotypes belonged to type A1, and those of P. multocida, to type A77,78,79; specifically, resistance to penicillin, ampicillin, and streptomycin was detected80,81. Subsequently, virulence factors such as leucotoxin were detected in M. haemolytica82, and biofilm formation was evidenced in P. multocida, M. haemolytica, and H. somni83. In addition, P. multocida was observed to produce vesicles on the outer membrane84.

From the isolates, strains were generated with which it was possible to formulate a bacterin-toxoid vaccine for the prevention of BRD, which was evaluated in ovine models85,86,87. The biologic generated is currently produced at INIFAP and is used in some ovine health programs.

Perspectives. The priority will be to develop biologics with domestic strains of IBR, BRSV and PI3 viruses, and combine them with live attenuated strains or subunits of M. haemolytica, P. multocida, and H. somni to confer effective protection against BRD. In order to improve diagnosis, it will be necessary to initiate metabolomics studies to monitor metabolites during the course of the disease. It would also be desirable to create a line of research on the genetic resistance of cattle to BRD. Collaterally, transcriptomics would be a very useful tool to try to make a genetic selection and form BRD-resistant herds.

Leptospirosis

Leptospirosis is a zoonosis of worldwide distribution; it is caused by bacteria of the genus Leptospira. According to the DNA analysis, this genus includes 10 pathogenic, 5 intermediate, and 7 saprophytic species88. Serology recognizes more than 300 serovars89. Worldwide, hardjo is the most commonly detected serovar in cattle90. Small mammals are the main reservoirs of the bacterium, large herbivores are a source of infection, and humans can be accidental hosts91.

Cattle are renal carriers of Leptospira spp. and therefore eliminate the bacteria through urine, contaminating the environment92. Leptospirosis causes reproductive disorders such as miscarriages, stillbirths, weak premature calves, and reduced milk production, resulting in considerable economic losses93. In Mexico, the first descriptions of leptospirosis in humans and cattle were made in 1928 and 1930, respectively94.

Contributions by INIFAP

A collaborative work between INIFAP, UAM and UAEM reported the situation of bovine leptospirosis in Mexico. Prevalence rates were determined in different ecological zones of the country; in the arid and semi-arid zones, the prevalence was 37.8%; in the dry tropics, 45.9%; in the humid tropics, 63.8%, and in the temperate zone, 39.4%. The presence of the hardjo, wolffi, and tarassovi serovars was demonstrated in all regions. In the temperate region, the icterohaemorrhagiae, portland-Vere, bratislava, pyrogenes, canicola, and pomona serovars were detected95. The grippotyphosa, mini, and tarassovi serovars were isolated; this had not been done in Mexico96,97. In other epidemiological studies, the same serovars were identified, but prevalences varied widely from 31 to 91 %98-103.

For diagnosis, INIFAP implemented the PCR technique, which allowed the detection of bacteria in urine collected from cattle with a history of reproductive problems100.

Bacterins were generated to prevent the disease: one was added with adjuvant using liposoluble vitamins, which yielded satisfactory results104. Another bacterin was made with serovars isolated in the state of Chiapas that were not contained in commercial bacterins; an excellent level of protection was observed in susceptible cattle with this homologous biologic. INIFAP currently has a bacterin that has been validated in dairy herds105.

Perspectives. The endemicity and high prevalence of leptospirosis in Mexico is evident; therefore, it is a real challenge to massify the use of microagglutination, which is the reference test for determining the Leptospira serovars present in the different regions, and then produce homologous bacterins that will effectively prevent leptospirosis. A line of research should be generated to develop molecular vaccines that can be used in any ecological region. It would also be advisable to implement an accurate methodology with high sensitivity and specificity, fast execution, and low cost. This can result in a better diagnosis that will increase the reproductive and productive parameters of cattle.

Ticks

Ticks are hematophagous ectoparasites capable of injecting toxins and transmitting to livestock different pathogens such as A. marginale and Babesia spp. with high morbidity and mortality rates. Of the various ticks identified in Mexico, the most important is Rhipicephalus microplus. Today they constitute a global problem due to their great adaptability to different ecological niches, it is considered that 65% of the national territory is infested with this tick.

Contributions by INIFAP

Epidemiology. An epidemiological study involving different states of the country corroborated that the distribution of R. microplus was essentially associated with environmental temperature, rainfall and water vapor106. In another research, greater efficiency and reproductive fitness was observed in ticks of a native strain collected in the field in Sinaloa, compared to a reference strain from CENID-SAI107.

Biological control. For tick control, this strategy has been well documented in studies conducted at INIFAP. Among the evaluation of techniques for the collection of R. microplus tick larvae, the double-traveled flag technique was selected for various studies. The effect of the recovery of R. microplus larvae using tropical legumes in the state of Morelos was evaluated108. Another study evaluated the anti-larvae effect using Stylosanthes humilis, S. hamata, Cenchurus ciliaris, and Andropogon gayanus grasses in artificially infested plots. A favorable effect was observed in S. humilis plots where only 3% of live larvae were recovered109. Other research using mature plants of S. humilis and S. hamata observed no anti-tick effect110. On the other hand, when evaluating crops of the legumes Leucaena leucocephala and Macroptilium artropurpureum, S. humilis, and S. hamata, a significant reduction in the number of larvae of R. microplus was observed111. Based on these findings, certain chemical compounds in S. humilis and S. hamata were identified as possible causes of the repellent effect112. Similarly, another study using M. minutiflora grass also showed a reduction in larval recovery 113.

Other strategies have involved the use of fungi or bacteria for tick control; thus, the use of the entomopathogenic fungus Metarhizium anisopliae demonstrated its ability to infect ticks and induce up to 100 % mortality, which allowed inferring that it could be a potential acaricide for the biological control of R. microplus114. On the other hand, in engorged adult ticks that were experimentally infected with Staphylococcus saprophyticus bacteria, it was able to induce tick mortality115. It was reported for the first time that the fungus Aspergillus flavus is capable of infecting 80 % of engorged adult ticks, the ovigerous masses and the larvae that emerge after hatching, under controlled conditions116.

Resistance. This is one of the most studied topics at INIFAP; in one of the first studies it was demonstrated that in R. microplus tick populations resistant to organophosphates, there is an elevated expression of carboxylesterase enzymes117. Subsequently, some genes coding for esterases were characterized to provide molecular markers for discriminating ixodicide-susceptible and ixodicide-resistant tick strains118. Genes coding for carboxylesterases B were analyzed by PCR assays in individual R. microplus larvae, detecting polymorphisms upon protein translation119,120; an esterase was also identified in the "Coatzacoalcos" strain (Cz EST9)121.

Another study sought to identify the association of gene mutations with pyrethroid resistance. Noting that the presence of the mutation is not associated with resistance in the dose-response form122. Studies on pyrethroid resistance attempted to correlate different diagnostic tests, and it was concluded that resistance is mediated by a mutation in the target gene Kdr123. The participation of cytochrome P450 has also been studied, and it has been observed to be expressed at high levels in pyrethroid-resistant strains124. However, a multifactorial process has been evidenced in the resistance of R. microplus to organophosphates and pyrethroids125. The first case of amitraz resistance was reported126, and selection pressure with amitraz was described as increasing the level of resistance in field populations127. In addition, RT-PCR methodology was used to measure the expression of cholinesterase and carboxylesterase in acaricide-resistant ticks128.

Immunological control. For tick control, immunogenic proteins derived from extracts of R. microplus ovaries obtained from cattle after immunization have been identified 129. Other studies have characterized and evaluated homology to vitellogenin proteins130 and ATAQ, both as potential vaccine candidates against R. microplus131,132. Certain immunization experiments against R. microplus and R. annulatus ticks have shown inconclusive results. However, similar studies have continued, such as the use of the protein subolesin, which was described as a potential target for developing a tick vaccine133,134.

Perspectives. There is an undeniable need to place greater emphasis on research into the epidemiology of ticks; especially climate change is a factor that is favoring their greater spatial distribution and, therefore, the infestation of livestock not previously exposed to ticks. It is also imperative to develop molecular techniques for the rapid diagnosis of resistance to the different chemical principles of ixodicides. Collaterally, a line of research on biological control should be maintained, involving the identification and characterization of plants. A line of research on the development of immunogens from conserved proteins associated with vital tick functions should be a priority. The major challenge will be to implement an integrated program for the control of R. microplus.

Babesiosis

Bovine babesiosis or piroplasmosis is a parasitic disease caused by protozoa of the genus Babesia that invade the erythrocytes of the bovine host. In Mexico, the recognized species are Babesia bovis and B. bigemina, both transmitted by the R. microplus and R. annulatus ticks135. Approximately 70% of the country's 35,224 960 head of cattle136 are permanently exposed to tick infestation. Thus, the prevalence of Babesia spp. varies between 50 and 96 %, which in turn explains the high risk of outbreaks occurring137.

Babesiosis has been identified as the most important arthropod-borne disease of cattle138. In Mexico territory, losses are estimated at 573.61 million dollars per year due to ticks and the diseases they transmit139. However, there is no commercial vaccine, and no national production of diagnostic reagents. In addition to the above, the wide distribution of resistance to ixodicides and climate change are major factors contributing to the abundance of vectors and the facilitation of pathogen transmission140.

Contributions by INIFAP

Diagnosis and epidemiology. INIFAP has implemented direct methods for the confirmatory diagnosis of babesiosis. Techniques for the identification of intraerythrocytic stages are routinely available. The most common is the peripheral blood smear with which B. bovis and B. bigemina are identified by means of microscopic observation; brain tissue imprints are also made, particularly for the detection of B. bovis141,142. Histopathological analysis of tissues collected at necropsy can also be performed143,144,145. Immunologically based indirect methods have been developed to detect circulating anti-B. bovis or anti-B. bigemina antibodies143,146,147. Defined and characterized parasitic antigens have been obtained for these procedures148,149. Advantages have been observed when compared to crude antigens with which a low specificity is regularly obtained in diagnostic tests; this occurs due to the similarity of epitopes present between different species of Babesia146,150,151, and it can also generate cross-reactions with other species148,151,152.

INIFAP research group has also improved the specificity of serological tests. For this purpose, genes coding for immunodominant, species-specific peptides have been cloned, and monoclonal antibodies have been used148,149,153.

Other studies have identified the most conserved antigens for B. bovis154-158, utilized for developing indirect ELISA tests for both species159,160, which in turn were tools for serological monitoring of experimentally immunized animals 161,162,163. These tests were also incorporated in seroepidemiological studies of cattle herds located in different cattle-raising areas of the country160,164.

On the other hand, there was a notorious advance in direct diagnosis; molecular procedures that detect genetic material of the parasites were reported. These have included the use of nucleic acid probes or nucleic acid amplification techniques165,166, which have been used in epidemiological studies in different cattle-raising regions of the country167. Using B. bigemina genomic DNA, a PCR with high analytical sensitivity was developed, for which the amplified product was hybridized with a non-radioactive DNA probe168,169. A multiple format was also implemented for the simultaneous detection of B. bovis and B. bigemina, to which the diagnosis of A. marginale was added166,170,171. DNA probes were used in epidemiological studies in Yucatán, Tabasco and Campeche172,173. They were also used for the monitoring of cattle inoculated with vaccine strains of B. bovis and B. bigemina149,174; as well as in the monitoring of susceptible animals introduced to endemic areas175,176. This same methodology proved useful for the detection of pathogen DNA in ticks177, as well as for the specific identification of B. bovis and B. bigemina in the tick R. microplus178,179.

Prevention. So far the best babesiosis prevention strategy in endemic regions is immunization with live attenuated vaccines, which can be derived from subinoculation into splenectomized calves, or from in vitro culture of B. bovis and B. bigemina180. The application of attenuated vaccines in susceptible cattle has been shown to induce a robust immune response in the face of attacks by highly virulent parasites181,182.

INIFAP researchers have participated in the development and adaptation of in vitro culture of B. bovis and B. bigemina, and today attenuated strains of these protozoans are available in Mexico183,184. A review of the development in Mexico of the attenuated vaccine from in vitro culture can be carried out based on various studies. These include the demonstration of low virulence of in vitro-culture derived parasite clones that were inoculated into susceptible cattle185. When using the material as fresh immunogen, the appropriate dose was determined to be 1 x 107 erythrocytes infected with B. bovis or B. bigemina186,187. Another study showed the need to include both Babesia species to induce successful protection against the disease188. Similar results were obtained with the vaccination of cattle against a natural challenge in the tropics189. Subsequently, it was determined that material derived from in vitro culture that was removed from cryopreservation in liquid nitrogen (-196 °C) required increasing the dose to 1 x 108 infected erythrocytes of each species in order to protect cattle from challenge with virulent parasites190. The use of the vaccine was also evaluated in native cattle kept in farms with high endemicity and enzootic instability, where an excellent level of protection against babesiosis was also demonstrated191. In another study, the vaccine was spiked with Lactobacillus casei and evaluated against a natural challenge; increased levels of specific IgG1 against B. bovis and B. bigemina; however, the level of protection was analogous to that of the vaccine without the bacteria192.

In vitro culture of B. bovis and B. bigemina is apparently a simple methodology; however, few laboratories in the world do it successfully. After more than 30 years of being established in Mexico, there was a low efficiency in the production of biomass. In recent years, INIFAP has positioned itself as a leading institution at the international level for innovations that have been integrated into the in vitro cultivation of B. bovis and B. bigemina. Bovine serum has been successfully removed from the culture medium and replaced by vital components such as insulin, transferrin, selenite, and putrescine. For the first time, the process was transferred to a perfusion bioreagent, thereby increasing the number of infected erythrocytes by 300%. This implied obtaining a high number of vaccine doses, compared to the traditional procedure193,194,195. The bioreagent-derived material evaluated as an immunogen conferred to cattle a level of protection above 80% in a field challenge196. That immunogen without the presence of serum proteins has been proposed to induce a response with greater immunological specificity197. At the same time, the incorporation of the bioreagent has generated a line of research on the use of soluble antigens derived from the culture supernatant. Recently, in INIFAP laboratory have achieved for the first time the proliferation of B. bigemina in a culture medium free of animal components, and also successfully transferred it to the bioreagent -a procedure that represents a scale-up of the process for vaccine production-198. These changes will facilitate the continued development of subunit vaccines199. Due to their degree of invention, the innovations described above have caused two patents to be granted in favor of INIFAP, and a third one is pending. One of the granted patents is entitled "Serum-free in vitro culture composition for obtaining erythrocytes parasitized with Babesia spp." (Patent No. 347729), and the other is called "Process for the elaboration of vaccinal reagent of erythrocytes parasitized with Babesia spp. Babesia bovis or Babesia bigemina" (Patent No. 337161).

Perspectives. There is a need to generate highly sensitive diagnostic tests with the ability to identify Babesia strains resistant or susceptible to antibabesial compounds. It would also be relevant to implement a procedure to discriminate attenuated (vaccine, conventional, genetically modified) or virulent field strains. Dynamic mapping of distribution and frequency is essential for the timely application of babesiosis prevention or control procedures. Live vaccines are now the only way to prevent the disease, but it is imperative to maintain the omics sciences in order to generate more knowledge of the interactions between parasites and cattle. This knowledge will facilitate the development of subunit vaccines that may be safer and more easily scalable.

Conclusions

INIFAP has developed and adapted serological and molecular diagnostic tools that have contributed to programs for the prevention and control of cattle diseases. Techniques for the detection of resistance to ixodicides have also been implemented. The distribution and frequency of some of the most important diseases affecting cattle farming in Mexico have been determined. The biologics developed include vaccines against rabies, anaplasmosis and babesiosis, as well as a bacterin against leptospirosis and a bacterin-toxoid against pneumonia. In addition, a BCG vaccine against tuberculosis and a new generation vaccine against brucellosis have been studied. The animal health perspective on zoonotic diseases such as tuberculosis and brucellosis suggests directing scientific and technical efforts toward those diseases elimination. Research on the effect of climate change, especially on vector-borne diseases, should be developed through the protocols and methods of omics sciences, such as genomics, epigenomics, transcriptomics, proteomics, metabolomics and other omics derivatives. It is currently the most appropriate way to understand the mechanisms of disease, and, therefore, it generates more effective vaccines and allows designing more precise diagnostic tools, which will be essential to integral control programs. Probably the biggest challenge will be to incorporate animal health research at INIFAP into the "One Health" concept. This has been defined as a multi-sectoral and transdisciplinary collaborative process at local, regional, national and global levels, based on the interconnections between humans, animals, plants and the environment200.

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Received: November 11, 2020; Accepted: March 08, 2021

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