Seroprevalence of reproductive and infectious diseases in cattle: the case of Madre de Dios in the Peruvian southeastern tropics Silvia E. León Trinidad, MS1; Christian Barrantes Bravo, PhD2; Shefferson Feijoo Narvasta, ZE3; Ethel Huamán Fuertes, MS2; Gustavo Ampuero Trigoso, ZE4; Francys Canto Sáenz, MS3,4; Hurley A. Quispe-Ccasa, Dr3,4* 1Laboratorio de Biotecnología Reproductiva, PROMEG Nacional, Estación Experimental Agraria Donoso, Instituto Nacional de Innovación Agraria, Huaral, Lima, Peru 2Dirección General de Ganadería, Ministerio de Desarrollo Agrario y Riego, La Molina, Lima, Peru 3Estación Experimental Agraria San Bernardo, Instituto Nacional de Innovación Agraria, Puerto Maldonado, Madre de Dios, Peru 4PROMEG Tropical, Instituto Nacional de Innovación Agraria, La Molina, Lima, Peru *Corresponding author: Dr. Quispe-Ccasa (hurleyabelqc@gmail.com) OBJECTIVE The objective of this study was to determine the seroprevalence of reproductive and infectious diseases in tropical cattle in the Tambopata and Tahuamanu Provinces in the department of Madre de Dios, Peru. SAMPLE 156 bovines from 7 cattle farms were sampled. These farms used exclusive grazing for food and natural mating for reproduction and did not have sanitary or vaccination programs. METHODS The serum of blood samples was subjected to ELISA with commercial kits for the detection of antibodies against Neospora caninum, Mycobacterium avium subsp paratuberculosis (MAP), Leptospira interrogans, pestivirus bovine viral diarrhea virus-1, retrovirus bovine leukemia virus (BLV), orbivirus bluetongue virus (BTV), and herpesvirus bovine herpes virus-1 (BHV). The data were analyzed by means of association tests with χ2 (P < .05) and Spearman rank correlation (P < .05) in the SPSS v.15.0 software (IBM Corp). RESULTS A low prevalence of antibodies to L interrogans, N caninum, M avium subsp paratuberculosis, bovine viral diarrhea virus-1 was found, but it was high to BTV, BLV, and BHV (100%, 53.85%, and 72.44%, respectively). The presence of BLV and BHV was higher in the Las Piedras District, bovines less than 5 years old, and cattle with breed characteris- tics of zebu and crossbred (P < .01). In addition, there was a significant correlation between both infections, showing 83.3% of BLV positivity that were also BHV positive (P < .01). CLINICAL RELEVANCE The high prevalence of antibodies to BTV, BHV, and BLV could be due to livestock management practices, direct con- tact with infected animals, and variation of the presence of vectors and natural reservoirs in the context of climate change in the tropics. Keywords: bluetongue, natural mating, enzootic bovine leukosis, IBR, tropical livestock The presence of reproductive and infectious dis- RID’s transmission is multiple, due to the difficul-eases (RID) in livestock determines the produc- ties in implementing good management practices tive efficiency of bovine herds. The diversity of RID (dehorning, castration, gynecological examination, is quite wide and includes causative agents such as etc), contaminated pastures, direct contact with viruses, bacteria, protozoa, and fungi.1 The way of disease-carrying animals introduced into the herds, greater interaction with transmission vectors and wildlife, use of infected breeders in natural mating, Received August 3, 2023 or straws of semen and embryos without any guar- Accepted January 24, 2024 antee of sanitary control or even the transplacental doi.org/10.2460/ajvr.23.08.0177 route from mother to offspring.2–4 © 2024 THE AUTHORS. Published by the American Veterinary Medical Association as an Open Access article under Creative Commons CCBY-NC license. American Journal of Veterinary Research 1 Unauthenticated | Downloaded 02/12/24 07:48 PM UTC The greatest alterations due to RID can occur in bovine neosporosis (BN), bovine leptospirosis (BL), the reproductive process, such as failure during ser- bovine paratuberculosis (PTBC), bovine viral diar- vice and conception, embryo mortality, abortions, and rhea (BVD), bluetongue (BT), enzootic bovine leu- neonatal mortality. Typical clinical signs of infectious kosis (EBL), and infectious pustular vulvovaginitis diseases manifest as fever, emaciation and anorexia, (IPV) by detecting antibodies for the causal agents diarrhea, pneumonia, embryonic death or resorption, through ELISA, in cattle from the provinces of fetal malformations, early abortion and, at advanced Tambopata and Tahuamanu in Madre de Dios. ages, weak neonates, placental retention, genital lesions, and even temporary infertility.5–7 Some RIDs Methods cause death in severe cases because they do not have effective treatments, due to anorexia and neurologi- Location cal damage; however, the greatest economic impact The study was carried out in 7 cattle farms, 4 in occurs in subclinical and latent infections, since they the province of Tambopata and 3 in the province of affect the immune system and decrease milk produc- Tahuamanu in the department of Madre de Dios, in tion and weight gain and infected animals become 2021. The provinces are located on the Interoceanic reservoirs of infectious agents.8,9 The main control Highway and border to the north with the Republic strategy is strict monitoring of incoming animals, of Brazil, to the east with the Republic of Bolivia, to avoiding the entry of animals with unknown health the south with the province of Manu, and to the west status, a quarantine period, annual serological analy- with the department of Ucayali (Figure 1). The region sis, and early culling of infected animals.10 has an Amazonian geography, with a tropical, warm, In the department of Madre de Dios, Peru, a and humid climate, with annual rainfall that exceeds population of 28,197 bovines was reported in 1994,11 1,000 mm, an average annual temperature of 26 °C, and rose to 50,145 in 2012,12 denoting a substantial with maximums that reach 38 °C between August increase in livestock activity in recent years in the and September and minimums of 5 °C between May region. The cattle farms in the research area have and August.15 as their main purpose meat production by raising Bos indicus cattle, some crosses with Bos taurus, Sample and Creole cattle.13 However, the environmental and The study was cross-sectional and descrip- ecological characteristics of the tropical zone are tive of a single cohort. According to the IV National favorable for the development of natural reservoirs Agricultural Census,12 in the districts where the study of infectious agents (viruses, bacteria, and parasites) was carried out, the cattle populations was a total of and transmission vectors of RID.14 The objective of 35,520 heads in 3,303 herds (or agricultural units): this research was to determine seroprevalence of 5,439 in Iberia, 6,933 in Iñapari, 9,127 in Las Piedras, Figure 1—Location map of Iberia and Iñapari Districts (Tahuamanu Province) and the Las Piedras and Tambopata Districts (Tambopata Province) in the department of Madre de Dios, where the sampling was carried out. 2 AJVR Unauthenticated | Downloaded 02/12/24 07:48 PM UTC and 14,021 in the Tambopata District. Due to the high Parasitology and Bacteriology Laboratory of heterogeneity of the number of cattle in each herd, SENASA (National Agrarian Health Service of Peru). the sample was calculated based on the number of For detection and quantification of specific anti- cattle per district. The sample size formula for finite bodies for Neospora caninum (agent causal of BN) populations was used,16 with 95% confidence level, 7% trachizoites, a competition ELISA was used with error, and 50% probability of success; finally, a sample the cELISA VMRD Kit (DEX-UCDSA/par3). For the of 150 animals was obtained. The sampling was car- detection of Mycobacterium avium subsp paratu- ried out with the informed consent of the farmers, berculosis (MAP) antibodies (agent causal of PTBC), who were made aware of the pertinent information indirect ELISA was used with the DEX-UCDSA/ about the objectives of the study, the destination of Bac.77.PARACHECK 2-Prionics AG Kit. For diagnosis the collected samples, and confidentiality in all cases. of antibodies to Leptospira interrogans (agent causal The type of sampling was intentional, and the inclu- of BL), a microagglutination technique using the sion criteria were the acceptance of the farmers to DEX-UCDSA/Bac.11 Kit. For determination of anti- take the sample and the availability of handling cor- bodies to bovine leukemia virus (BLV; agent causal rals on their farms. The herds were selected at ran- of EBL), bluetongue virus (BTV; agent causal of BT), dom from the farms that had good vehicular access, bovine herpes virus (BHV; agent causal of IPV), and and then we determined if they met the proposed bovine viral diarrhea virus (vBVD; agent causal of inclusion criteria. One hundred fifty-six bovines BVD), the DEX-UCDSA/Vir-03, DEX-UCDSA/Vir-10, between males (8) and females (148) over 1 year old DEX-UCDSA/Vir-21, and DEX-UCDSA/Vir-07 BVD were sampled. The sample corresponded to subsets SERO-II kits were used, respectively. of the selected herds that met the age range and breed characteristics, as follows: 108 were from the Statistical analysis Tambopata District (from 3 herds), 22 from the Las The relative frequencies of positive cases of BN, Piedras District (from 1 herd), 19 were from the Iberia PTBC, BL, EBL, BT, IPV, and BVD by the presence District (from 2 herds), and 7 from the Iñapari District of antibodies to causative agents were determined (from 1 herd). The breed group included bovines according to province, district, sex, age, and breed with Nelore- and Brahman-breed characteristics group to evaluate the association degree with χ2 test (zebu cattle), Brown Swiss-breed characteristics, and (P < .05). In addition, the correlations between dis- undetermined characteristics (crossbred cattle). ease seropositivity in cattle were calculated using Spearman ordinal rank coefficients (P < .05) to Animal care and production system determine the cases of coinfection and the relative The study protocol was not submitted to an ethi- frequencies between paired variables. Analyzes were cal committee for animal experimentation, because carried out in the SPSS v.15.0 software (IBM Corp). the human-animal interaction was limited to the extraction of blood samples, taking a maximum time Results of 15 to 30 seconds for each animal. The study was nonexperimental and descriptive of a single cohort Sampling of 156 bovines was carried out, where in which the animals were carefully restrained in a 16.67% (26) were in the Tahuamanu Province and restraint box inside the cattle stable to avoid sud- 83.33% (130) were in the Tambopata Province. den movements according to Animal Research: There were 63.23% (108) of cattle in the Tambopata Reporting of In Vivo Experiments 2.0 guidelines. District, 14.10% (22) in the Las Piedras District, The farms had an extensive production system, with 12.18% (19) in the Iberia District, and 4.48% (7) in the exclusive grazing and no provision of any nutritional Iñapari District; 94.87% (148) were female, and 5.13% supplements, although mineral salt blocks are occa- (8) were male. Regarding the classification by age sionally provided. Cows arrive at their first calving at group, 51.28% (80) were between 2 and 5 years old, 3.5 years old and have a productive life of approxi- and 48.72% (76) were over 5 years old. Regarding mately 8 years. The reproduction system is by nat- breed characteristics, 73.72% (115) were crossbred ural mating, using permanent bulls in the female cattle, 6.41% (10) were Zebuino, and 19.87% (31) had herds. The productive purpose is mixed since eco- Brown Swiss characteristics. nomic income is received from the sale of milk and From the analysis of blood samples, a high cattle for meat. Regarding the sanitary management prevalence of BTV antibodies was found in the study system, farmers carry out deworming programs and area, reaching 100% positive diagnosis. No positive vitamin supplementation once a year; however, vac- case of L interrogans antibodies was found (0% prev- cination programs are not carried out. alence). There is a high presence of antibodies to BHV (72.44%), which is associated with the district Blood extraction and (P < .01), reaching 100% prevalence in Las Piedras serological analysis and Iñapari. The presence of antibodies to BLV is also Blood samples were drawn by direct puncture high (53.85%), and it is higher in the Iberia and Las of the middle coccygeal artery, using sterile 10-mL Piedras Districts than the others (P < .01). The preva- Vacutainer tubes without anticoagulant. After a lence of antibodies to N caninum and MAP was lower period of centrifugation of the samples, the serum (6 cases and 2 cases, respectively), but a significant was stored in 5-mL vials and frozen at −20 °C until association was found by district (P < .01), which analysis. The serum vials were sent to the Virology, was higher in Las Piedras and Iñapari. Only 1 positive AJVR 3 Unauthenticated | Downloaded 02/12/24 07:48 PM UTC case of antibodies to vBVD (0.64%) was found in the Table 3—Correlation coefficient and significance of Las Piedras District (Table 1). antibodies for reproductive and infectious diseases in An association analysis of the positive diagnosis cattle. of antibodies to causal agents of diseases with the BN PTBC BVD EBL IPV sex, age, and breed group of the sampled animals was performed (Table 2). No significant association BN 1.000 −0.023 −0.016 −0.015 0.049 of any disease with sex was found, but it was found 0.778 0.842 0.848 0.545 according to age group. There was a higher presence PTBC 1.000 −0.009 0.106 0.0700.910 0.190 0.383 of antibodies to N caninum (P < .05) and antibod- BVD 1.000 0.074 0.050 ies to BHV (P < .01) in cattle from 2 to 5 years old 0.356 0.539 (7.50% and 87.50%, respectively). According to the EBL 1.000 0.263a breed group, crossbred cattle had a higher presence 0.001 of antibodies to BLV (64.35%) and BHV (87.83%), and IPV 1.000 in Zebu cattle (Nelore and Brahman), 100% were pos- itive for BHV (P < .01). BN = Bovine neosporosis. BVD = Bovine viral diarrhea. The correlation between positive cases of anti- EBL = Enzootic bovine leukosis. IPV = Infectious pustular bodies to N caninum, MAP, vBVD, BLV, and BHV was vulvovaginitis. PTBC = Bovine paratuberculosis. evaluated (Table 3), and no relationship was found aSignificant correlation at the P < .01 level with Spearman’s between N caninum, MAP, or vBVD; however, a sig- rank coefficients. nificant correlation was found between the presence of antibodies to BLV and BHV (P < .01). Table 1—Seroprevalence rate of reproductive and infectious diseases according to province and district in the department of Madre de Dios. Variable/level BN BL PTBC BVD BT EBL IPV Province Tambopata 3.08 (4) 0 (0) 3.85 (1) 0.77 (1) 100 (130) 51.54 (67) 73.85 (96) Tahuamanu 7.69 (2) 0 (0) 0.77 (1) 0 (0) 100 (26) 65.38 (17) 65.38 (17) P value .26 – .20 .65 – .20 .38 District Tambopata 0 (0) 0 (0) 0 (0) 0 (0) 100 (108) 44.44 (48) 68.52 (74) Las Piedras 18.18 (4) 0 (0) 4.55 (1) 4.55 (1) 100 (22) 86.36 (19) 100 (22) Iberia 5.26 (1) 0 (0) 0 (0) 0 (0) 100 (19) 73.68 (14) 52.63 (10) Iñapari 14.29 (1) 0 (0) 14.29 (1) 0 (0) 100 (7) 42.86 (3) 100 (7) P value < .01a – < .01a .11 – < .01a < .01a Total 3.85 (6) 0 (0) 1.28 (2) 0.64 (1) 100 (156) 53.85 (84) 72.44 (113) The numbers in parentheses represent the count of positive cases. BL = Bovine leptospirosis. BN = Bovine neosporosis. BVD = Bovine viral diarrhea. BT = Bluetongue. EBL = Enzootic bovine leukosis. IPV = Infectious pustular vulvovaginitis. PTBC = Bovine paratuberculosis. – = Not applicable. aSignificant association at the P < .01 level. Table 2—Seroprevalence rate of reproductive and infectious diseases according to sex, age, and breed group. Variable/level BN PTBC BVD EBL IPV Sex Female 4.05 (6) 1.35 (2) 0.68 (1) 54.73 (81) 70.95 (105) Male 0 (0) 0 (0) 0 (0) 37.50 (3) 100 (8) P value .56 .74 .82 .34 .07 Age 2–5 y 7.50 (6) 1.25 (1) 1.25 (1) 52.50 (42) 87.50 (70) > 5 y 0 (0) 1.32 (1) 0 (0) 55.26 (42) 56.58 (43) P value .01a .97 .33 .73 < .01b Breed group Crossbred 4.35 (5) 0.87 (1) 0.87 (1) 64.35 (74) 87.83 (101) Zebuino 10.00 (1) 10.00 (1) 0 (0) 30.00 (3) 100 (10) Brown Swiss 0 (0) 0 (0) 0 (0) 22.58 (7) 6.45 (2) P value .31 .04a .84 < .01b < .01b Total 3.85 (6) 1.28 (2) 0.64 (1) 53.85 (84) 72.44 (113) The numbers in parentheses represent the count of positive cases. BN = Bovine neosporosis. BVD = Bovine viral diarrhea. EBL = Enzootic bovine leukosis. IPV = Infectious pustular vulvovaginitis. PTBC = Bovine paratuberculosis. aSignificant association at the P < .05 level. bSignificant association at the P < .01 level. 4 AJVR Unauthenticated | Downloaded 02/12/24 07:48 PM UTC No cases of possible coinfection between BN significant association with district (higher preva- and PTBC, BN and BVD, or PTBC and BVD were lence in Las Piedras) and age group (higher preva- found (Table 4). All positive cases of antibodies to lence in cattle from 2 to 5 years old). Other studies18 MAP and vBVD were positive for BLV and BHV. In have already analyzed the presence of these dis- addition, 83.3% of positive cases of antibodies to eases in other areas of the Peruvian Amazon, such BHV and 50.0% of BLV were also positive for N cani- as in the department of Ucayali, with 1.5% antibod- num, although not significantly (P > .05). A possible ies against N caninum but no antibodies against the coinfection between EBL and IPV was found, where vBVD; in Colombia, the seroprevalence of 12.5% for 83.3% of cases were positive for antibodies to BLV N caninum,7 76.4% for vBVD, and 10.7% for N caninum were also positive for BHV (P < .05). was reported.6 On the other hand, in the state of Rio Grande do Sul, Brazil, a seroprevalence of 30.0% Table 4 to 42.5% for BVD and 21.8% to 35.0% for BN were —Relative frequency (%) of simultaneous 20 negative and positive cases of reproductive and found. It is likely that the higher frequency in the infectious diseases in cattle. Las Piedras District is due to the introduction of an infected individual, where the congenital transmis- BN PTBC BVD EBL sion route maintains the prevalence of N caninum at (−) (+) (−) (+) (−) (+) (−) (+) a local level and horizontal transmission would be PTBC less frequent. Bovine neosporosis causes abortions, (−) 98.7 100 newborn death, or the birth of weak calves with (+) 1.3 0 nervous signs and no apparent infection, which are BVD spreaders of the disease in the herd. The fetus can (−) 99.3 100 99.4 100 die in utero to be reabsorbed, mummified, or auto- (+) 0.7 0 0.6 0 lyzed; to be born alive and die immediately; or to be EBL born clinically normal but congenitally infected.21,22 (−) 46.0 50.0 46.8 0 46.5 0 This disease is characterized to be generally asymp- (+) 54.0 50.0 53.2 100 53.5 100 tomatic and congenitally transmitted; there is no IPV (−) 28.0 16.7 27.9 0 27.7 0 40.3 16.7 effective treatment, so the control is based on the (+) 72.0 83.3 72.1 100 72.3 100 59.7 83.3 prevention of transmission and culling of infected animals.23,24 Regarding the lower frequency of BN in BN = Bovine neosporosis. BVD = Bovine viral diarrhea. cattle over 5 years old, it may be due to the fact that EBL = Enzootic bovine leukosis. IPV = Infectious pustular the reproductive problems caused by N caninum vulvovaginitis. PTBC = Bovine paratuberculosis. could motivate the early culling of these animals from the herd. The PTBC results of this study are lower than the reports from Nariño, Colombia, with Discussion an 8% prevalence in milking cows, which was associ- ated with the body condition of the animals.25 Bovine This is the first report about the simultane- paratuberculosis is a disease caused by MAP, which ous analysis of various RIDs that affect cattle in affects sheep and cattle (mainly dairy cattle), and the department of Madre de Dios, such as BN, BL, feces, colostrum, and milk are an important source of PTBC, BVD, BT, EBL, and IPV. In the tropical region, transmission. It is characterized by chronic enteritis, diagnostic studies of other infectious and reproduc- progressive emaciation, and diarrhea and leads to a tive diseases in cattle have been reported, such as state of malnutrition, weakness, and death.26–28 In Babesiosis,17 and Brucellosis in the departments of the study areas, the breeding of crossed Bos taurus Ucayali and18 Huánuco19 and in Colombia.7 The sero- X Bos indicus cattle oriented toward meat produc- prevalence of antibodies indicates that the subjects tion predominates, and there are very few herds have been previously exposed to infectious agents. dedicated to milk production, which would explain In this study, no presence of BL was found (0% of anti- the low prevalence of PTBC. bodies to L interrogans), despite that L interrogans A 100% presence of antibodies to BTV was found is zoonotic and wild animals (rats, weasels, reptiles, in the samples analyzed. BT is an infection caused etc) are its natural reservoirs. Rivera et al18 found by a virus of the Orbivirus genus of the Reoviridae 52.2% of samples with antibodies to L interrogans family, which causes cyanosis of the tongue, fever, in the Amazonian department of Ucayali, but in inflammation, and hemorrhage in the oral and nasal Colombia, lower levels of these antibodies were mucosa and throughout the digestive tract, loss of reported: 28.0% and 23.1%.6,7 The department of body condition, inflammation in the coronary bands Madre de Dios is abundant in wildlife biodiversity, and sensitive hoof plates, and fetal malformations which could suggest a high presence of transmit- in infections during the first third of gestation; in ting vectors and natural reservoirs of pathogens for domestic and wild ruminants.29,30 In the depart- extensive livestock farming; however, in this study, ment of Madre de Dios, the presence of antibodies no cases of BL were found. Therefore, it is suggested to BTV in Huanganas (Tayassu pecari) was already more investigation is necessary. reported in 7.5% and to other antibodies of the A low seroprevalence of BN (3.85%), PTBC same serogroup in 29.2% of sample.31 The virus is (1.28%), and BVD (0.64%) was found, where the transmitted by arthropods of the genus Culicoides frequency of antibodies to N caninum showed a (Culicoides insignis) infected by biting animals with AJVR 5 Unauthenticated | Downloaded 02/12/24 07:48 PM UTC viremia, which makes its prevalence higher in areas tremors, ataxia, and blindness, leading to death.44 For with a favorable climate for the development of the its control, it is recommended to monitor the move- vector.29 Vertical transmission of BT from pregnant ment of cattle, quarantine period, frequent sero- cows to their offspring and from infected males to logical analysis, and culling of positive animals upon females through semen has also been verified. The diagnosis. EBL is caused by the BLV, which infects BTV has a predilection for the reproductive tract, so B lymphocytes. The majority of individuals infected its disorders generated include embryonic death, with BLV never develop clinical disease, although abortions, fetal malformations, temporary infertility subclinical infection can cause immunosuppression, in males, and virus elimination in semen.32,33 BT has where T cells infected with BLV increase the expres- been studied mainly in sheep, with variable levels of sion of immunoinhibitory receptors, which increase prevalence in the tropical zone of Peru. A 56.1% BT their ability to evade the immune response to other prevalence in Blackbelly sheep from the department infections. Only a small percentage of infected ani- of Junín was found,34 96.0% in sheep from the depart- mals develop a tumor (lymphosarcomas), which ment of Ucayali,35 and 99.0% in cattle from Ecuador.36 causes early slaughter and consequent direct eco- In a recent study,37 BT prevalence in sheep is not nomic loss.45 The main mechanism of transmission uniformly distributed in Brazil, and there is a higher of BLV is through livestock equipment contaminated concentration of cases in the state of Rio Grande do with blood from infected animals (dehorner, hypo- Sul30 and the state of Amazonas. In 2004, no anti- dermic needles, surgical instruments, or infested bodies against the BTV and BHV were detected in equipment), blood-sucking insects, or vertical trans- deer (Mazama gouazoubira) in Bolivia38; however, mission from mother to fetus or by ingestion of colos- the recent increase in BT cases in cattle could be trum from infected cows to suckling calves.45,46 The due to variations in environmental conditions, tem- immunosuppressive effect of EBL could explain the perature patterns, precipitation, and wind, as well as high seropositivity of BHV antibodies for IPV, which management practices, which would affect the dis- coincides with Mionetto and Rodríguez,8 who also tribution of vectors and hosts in tropical zones.30,39 In found a significant association between seropositiv- this regard, Clavijo et al40 argue that BTV serotypes ity between BLV and BHV-1, since BLV would facili- may be continuously changing as a function of cli- tate the entry of other pathogens or would diminish mate change, and changes in land use in recent years the immunological protection mechanisms such as could affect the geographic distribution of domes- lower production of IgM and IgG2 against BHV-1. tic and wild ruminants and influence areas where Furthermore, the high seroprevalence of antibodies new BTV serotypes may emerge and persist, which to BHV may be due to direct contact with respira- could explain the high prevalence of BT in the pres- tory, ocular, or genital secretions of infected cattle, ent study. In addition, the increase in the dynamics or indirectly through equipment contaminated with of circulation of live cattle in border areas of Peru, the virus, and the transmission through the semen Brazil, and Bolivia could contribute to the spread of of infected bulls is not ruled out. In other reports, infected animals as BTV reservoirs.29 Rivera et al18 registered the presence of antibod- A high presence of antibodies to BHV (72.44%) ies to BHV-1 in 46.3% of cattle in the department of and BLV (53.85%) was found. In addition, both fre- Ucayali, and Souza et al41 found a seroprevalence of quencies were significantly correlated (P < .01), 54.5% to 60.3% in Rio Grande do Sul20 and 43.3% to finding a possible coinfection in 83.3%, where IPV- 86.2% in Acre, Brazil. The scarce control of the tran- positive diagnoses were also EBL positive. Infectious sit of animals in border areas could have contributed bovine rhinotracheitis is produced by BHV-1 that to the high prevalence of IPV and EBL, especially affects the respiratory, reproductive, and nervous in the districts of Iñapari, Iberia, and Las Piedras. systems, which can be transmitted by direct contact There are reports about the significant association with bodily secretions and semen during natural mat- of age, breed, and number of births with the EBL ing, artificial insemination, or embryo transfer.41,42 In and IPV seroprevalence.47–49 In this study, the degree the respiratory form, infected animals present fever, of breed purity of the animals was not certain, and serous nasal discharge, conjunctivitis, salivation, 73.72% corresponded to crossbred cattle, where a cough, loss of appetite, depression, necrotic lesions higher seroprevalence of antibodies to BHV and BLV in the nose that can progress to pustules, and ulcers was found in zebu breeds (100% and 30.0%, respec- covered by a pseudomembrane that obstructs the tively) and in crossbred cattle (87.8% and 64.4%, upper airways.43 A frequent complication is abor- respectively); cattle with Brown Swiss character- tion, between the third and sixth week after infec- istics had the lowest prevalence of both infections tion, mainly in cows from 5 to 8 months of gestation. (6.45% and 22.58%, respectively). However, cattle In the genital form, females develop IPV and males with Brown Swiss characteristics were present in show infectious pustular balanoposthitis.20,42 The only 1 herd, so the prevalence could be increased if infection acute phase lasts from 2 to 4 days and all herds had these types of cattle. Further studies recovery from 10 to 14 days after the onset of signs, are required to determine genetic resistance to BLV and the animals remain virus carriers. In this study, a as a control strategy.50 lower prevalence of IPV was found in cattle > 5 years, In cattle from the Tambopata and Tahuamanu which could be due to the death or culling of adult Provinces in the department of Madre de Dios, Peru, cattle. In the nervous form, young animals present a seroprevalence of antibodies to BTV and L inter- meningoencephalitis, lack of coordination, muscle rogans was found in 100% and 0% of the sample, 6 AJVR Unauthenticated | Downloaded 02/12/24 07:48 PM UTC respectively. The seroprevalence of antibodies to N sp. and Neospora caninum in cattle, buffaloes and mixed caninum, MAP, and vBVD (3.85%, 1.28%, and 0.64%, farms, in the Department of Caqueta, Colombia. Rev respectively) in the study area was lower than Salud Anim. 2014;36(2):80–89. BLV and BHV (53.85% and 72.44%, respectively). 8. Mionetto M, Rodríguez AF. Asociación entre leucosis bovina enzoótica y la respuesta inmune humoral natu- Antibodies to BLV and BHV were more frequent in ral contra enfermedades infecciosas de interés repro- the Las Piedras District, BHV in cattle from 2 to 5 ductivo. Universidad de La República. 2018. Accessed years old, BHV in cattle with breed characteristics of May 15, 2023. https://www.colibri.udelar.edu.uy/jspui/ zebu, and BLV in crossbred cattle. In addition, a posi- handle/20.500.12008/25172 tive correlation was found in cases positive for both 9. Palomares G, Aguilar F, Flores C, et al. Important infectious diseases in goat production in Mexico: history, challenges infections, where 83.3% of individuals were positive and outlook. Rev Mex Cienc Pecu. 2021;12:205–223. for EBL and positive for IPV. doi:10.22319/rmcp.v12s3.5801 10. Brennan ML, Christley RM. Biosecurity on cattle Acknowledgments farms: a study in North-West England. PLoS One. 2012;7(2):e28139. doi:10.1371/journal.pone.0028139 1 1. III. Censo Nacional Agropecuario. National Institute of We express our gratitude to Dr. Manuel Antonio Canto Statistics and Informatics (INEI). 1994. Accessed May Saenz for his kind support in copyediting and language of 15, 2023. https://censos.inei.gob.pe/bcoCuadros/ the manuscript. IIIcenagro.htm 1 2. IV. Censo Nacional Agropecuario. National Institute of Disclosures Statistics and Informatics (INEI). 2012. Accessed May 15, 2023. http://censos.inei.gob.pe/cenagro/tabulados/ 13. Quispe-Ccasa HA, Canto-Saenz FM, Ampuero G, Feijoo S, The authors have nothing to disclose. Hauman-Fuertes E. Characterization of livestock systems The Google translator tool was used on some occasions on farms in the Tambopata and Tahuamanu Provinces, during the writing of the text to review some terms in the Madre de Dios, Peru. Rev Cient Fac Cienc Vet Univ Zulia. English language. 2022;33:1–11. doi:10.52973/rcfcv-e33193 14. Villegas G, Bolaños A, Olguín L. La Ganadería en México. Funding 1st ed. Universidad Nacional Autónoma de México; 2001.1 5. Caracterización del Departamento de Madre de Dios. Departamento de Estudios Económicos de la Sucursal This work was supported by the Dirección General Cusco. BCRP (Banco Central de Reserva del Perú). 2022. de Ganadería (DGGA) of MIDAGRI and by the project Accessed May 15, 2023. https://www.bcrp.gob.pe/docs/ “Mejoramiento de la disponibilidad y acceso del material Sucursales/Cusco/madre-de-dios-caracterizacion.pdf genético mediante el uso de técnicas de biotecnología repro- 16. Murray RS, Larry JS. Análisis de varianza. In: Estadística. ductiva en ganado bovino tropical en las regiones de San 4th Ed. McGraw-Hill; 2009. Martín, Loreto y Ucayali” with CUI 2338934–PROMEG Tropical. 17. Ore AH. Determinación de la prevalencia de Babesiosis en bovinos de la raza Brown Swiss en el sector Castañal References del distrito de Tambopata – Madre de Dios – 2019. Universidad Nacional Amazónica de Madre de Dios. 2022. Accessed May 20, 2023. https://repositorio.unamad.edu. 1. Da Silva C. Enfermedades infecciosas que causan abor- pe/handle/20.500.14070/884 tos en bovinos con enfoque en rodeos lecheros en 1 8. Rivera H, Benito A, Ramos O, Manchego A. Prevalencia Uruguay. Universidad de la República. 2019. Accessed de enfermedades de impacto reproductivo en bovi- May 15, 2023. https://bibliotecadigital.fvet.edu.uy/ nos de la Estación Experimental de Trópico del Centro handle/123456789/2693 de Investigaciones IVITA. Rev Investig Vet Perú. 2. Abad-Zavaleta J, Ríos-Utrera A, Rosete-Fernández JV. 2004;15(2):120–126. Prevalence of infectious bovine rhinotracheitis and bovine 19. Meza A, Morales S, Ara M, Manchego A, Calle ES, viral diarrhea in females in three seasons in the down- Angulo JC. Seroprevalence of bovine brucellosis in town area of Veracruz. Nova Sci. 2016;8(16):213–227. Puerto Inca district, Huánuco. Rev Investig Vet Perú. doi:10.21640/ns.v8i16.433 2010;21(2):223–226. 3. De la Sota MD. Manual de Procedimientos: Lengua Azul. 20. Souza GN, Pegoraro LM, Weissheimer CF, et al. Servicio Nacional de Sanidad y Calidad Agroalimentaria Epidemiological situation and risk factors to infectious SENASA; 2005. diseases in dairy cattle located in different mesoregions 4. Solano MJ, Ramónez X. Aplicación de P4 intravaginal en of the state of Rio Grande do Sul, Brazil, 2016/2017. Vet protocolos de IATF en vacas y aprovisionamiento de un Sci Med. 2019;2(2):1–6. equipo de inseminación artificial en el Centro de Apoyo 21. Boas RV, Pacheco TDA, Melo ALT, de Oliveira AC, “Juan Lunardi.” Universidad Politécnica Salesiana. 2013. de Aguiar DM, Pacheco Rde C. Infection by Neospora cani- Accessed May 26, 2023. https://dspace.ups.edu.ec/ num in dairy cattle belonging to family farmers in the north- handle/123456789/5107 ern region of Brazil. Rev Bras Parasitol Vet. 2015;24(2): 5. Girata JG. Estudio zootécnico de la neosporosis bovina: 204–208. doi:10.1590/S1984-29612015035 análisis teórico de orientación para los Ganaderos de 22. Softic A, Asmare K, Granquist EG, Godfroid J, Fejzic N, Santander y Boyacá, Colombia. Universidad Nacional Skjerve E. The serostatus of Brucella spp., Chlamydia Abierta y a Distancia. 2016. Accesed May 15, 2023. abortus, Coxiella burnetii and Neospora caninum in cattle https://repository.unad.edu.co/handle/10596/6861 in three cantons in Bosnia and Herzegovina. BMC Vet Res. 6. Moreno-Figueredo G, Benavides-Ortiz E, Guerrero B, 2018;14(1):40. doi:10.1186/s12917-018-1361-z Cruz-Carrillo A. Association between seropositivity to BVD 2 3. Baquero-Tapia F, Díaz-Monroy B, Vinueza-Veloz P. virus, Leptospira interrogans and Neospora caninum and Estudio de la neosporosis en bovinos de la provincia de abortions in small holder farms in the dairy belt of Boyacá, Chimborazo, Ecuador. Revista Alfa. 2022;6(17):224–238. Colombia. Rev Investig Vet Perú. 2017;28(4):1002–1009. doi:10.33996/revistaalfa.v6i17.163 doi:10.15381/rivep.v28i4.12850 2 4. Sánchez-Sánchez R, Vázquez P, Ferre I, Ortega-Mora LM. 7. Motta-Giraldo JL, Clavijo-Hoyos JA, Waltero-García I, Treatment of toxoplasmosis and neosporosis in farm Abeledo M. Seroprevalence of Brucella abortus, Leptospira ruminants: state of knowledge and future trends. Curr Top AJVR 7 Unauthenticated | Downloaded 02/12/24 07:48 PM UTC Med Chem. 2018;18(15):1304–1323. doi:10.2174/15680 gouazoubira) in the Gran Chaco, Bolivia. J Wildl Dis. 26618666181002113617 2004;40(2):92–98. doi:10.7589/0090-3558-40.1.92 25. Benavides-Benavides B, Arteaga-Cadena AV, Montezuma- 39. Mayo C, Gardnerb I, Mullensc B, et al. Anthropogenic Misnaza CA. Epidemiological study of bovine paratuber- and meteorological factors influence vector abundance culosis in dairy herds in Southern Nariño, Colombia. Rev and prevalence of bluetongue virus infection of dairy Med Vet. 2016;31:57–66. cattle in California. Vet Microbiol. 2012;155(2-4)158–164. 26. Palmer MV, Kanipe C, Cox R, Robbe-Austerman S, doi:10.1016/j.vetmic.2011.08.029 Thacker TC. Characteristics of subclinical Mycobacterium 40. Clavijo A, Sepulveda L, Riva J, Pessoa-Silva M, Tailor- avium ssp. paratuberculosis infection in a captive white- Ruthes A, Lopez JW. Isolation of bluetongue virus tailed deer herd. J Vet Diagn Invest. 2019;31(6):844–851. serotype 12 from an outbreak of the disease in South doi:10.1177/1040638719873028 America. Vet Rec. 2002;151(11):301–302. doi:10.1136/ 2 7. Osuna-Chávez R, López-Robles G, Celaya-Michel H, vr.151.10.301 Sosa-Castañeda J, Nieblas-López M, Ibarra-Zazueta C. 41. De Arruda EF, da Silva TIB, Aragão BB, Soares de Seroprevalencia de Mycobacterium avium subespecie Castro R. Soroprevalence of bovine alphaherpesvirus paratuberculosis en bovinos sospechosos sacrificados type 1 (BoHV-1) and risk factors associated with dairy en rastro de Sonora, México. Abanico Vet. 2021;11:e403. properties of the municipality of Senador Guiomard, doi:10.21929/abavet2021.21 Acre, Brazil. Arqu Inst Biol. 2019;86:1–6. doi:10.1590/ 28. Artigot P, Magreñán J, Ríos M, Rodriguz M, Ruiz H, 1808-1657001362018 Grasa L. Paratuberculosis y adenocarcinoma intestinal: 42. Tadeg WM, Lemma A, Yilma T, Asgedom H, Reda AA. diagnóstico diferencial. Badajoz Vet. 2023;29:6–13. Seroprevalence of infectious bovine rhinotracheitis and 2 9. Gong QL, Wang Q, Yang XY, et al. Seroprevalence and risk brucellosis and their effect on reproductive performance factors of the bluetongue virus in cattle in China from 1988 of dairy cattle. J Vet Med Anim Health. 2021;13:106–113. to 2019: a comprehensive literature review and meta- doi:10.5897/JVMAH2020.0889 analysis. Front Vet Sci. 2021;7:550381. doi:10.3389/ 43. Riaz A, Javid B, Shah MAA, et al. First report on the detec- fvets.2020.550381 tion and molecular characterization of bovine herpesvirus 30. Souza EJ, Silva FA, da Silva TG, et al. Biogeography of 1 from a clinical case of infectious bovine rhinotracheitis in the spread of bluetongue disease in sheep in Brazil. Pakistan. Pak Vet J. 2021;41(10):160–162. doi:10.29261/ Small Rumin Res. 2023;222:106964. doi:10.1016/ pakvetj/2020.084 j.smallrumres.2023.106964 4 4. Campos FS, Dezen D, Antunes DA, et al. Efficacy of an 3 1. Rivera H, Cárdenas L, Ramírez M, Manchego A. Orbivirus inactivated, recombinant bovine herpesvirus type 5 infection in white-lipped peccaries (Tayassu pecari) (BoHV-5) vaccine. Vet Microbiol. 2011;148(1):18–26. from Madre de Dios region, Peru. Rev Investig Vet Perú. doi:10.1016/j.vetmic.2010.08.004 2013;24(4):544–550. 4 5. González ET, Oliva GA, Valera AR, Bonzo E, Licursi M, 32. Reis JN, Varaschin MS, Dorneles EMS, et al. Blue tongue Etcheverrigaray ME. Enzootic bovine leukosis: evalua- virus in dairy cattle in the southern region of minas gerais, tion of diagnostic techniques (AGID, I-ELISA, WB and Brazil – serological survey. Acta Sci Vet. 2022;50:1898. PCR) in experimentally inoculated bovines. Anal Vet. doi:10.22456/1679-9216.127535 2001;21(2):12–20. 3 3. Saminathan M, Singh KP, Vineetha S, et al. Virological, 4 6. Vásconez-Hernández A, Sandoval-Valencia P, Puga-Torres B, immunological and pathological findings of transplacen- De La Cueva-Jácome F. Seroprevalence of bovine enzootic tally transmitted bluetongue virus serotype 1 in IFNAR1- leucosis in 6 to 24 months animals, in Manabí, Pichincha blocked mice during early and mid gestation. Sci Rep. and Chimborazo, Ecuador. La Granja Revist Cien Vida. 2020;10:1–19. doi.10.1038/s41598-020-58268-0 2017;26(2):131–141. doi:10.17163/lgr.n26.2017.11 34. Jurado J, Navarro D, Ramírez M, Santiago MA, Rivera HA. 4 7. Nava Z, Obando C, Molina M, Bracamonte M, Tkachuk O. Detection of antibodies against bluetongue virus in sheep Seroprevalence of enzootic bovine leukosis and its asso- from two locations in Junín, Peru. Rev Investig Vet Perú. ciation with clinical signs and risk factors in dairy herds 2020;31(2):e17850. doi:10.15381/rivep.v31i2.17850 from Barinas State, Venezuela. Rev Fac Cienc Vet. 35. Navarro MD, Rojas MM, Jurado PJ, et al. Molecular detec- 2011;52(1):13–23. tion of bluetongue virus in Culicoides insignis and sheep 48. Jiménez-Sánchez JA, Bulla-Castañeda DM, Díaz-Anaya AM, of Pucallapa, Peru. Rev Investig Vet Perú. 2019;30(1): José Garcia-Corredor D, Orlando Pulido-Medellin M. 465–476. doi:10.15381/rivep.v30i1.15690 Determinación serológica del virus de leucosis enzoótica 3 6. De la Torre E, Moreira N, Saegerman C, et al. Bluetongue bovina (VLEB) en el municipio de Paipa, Boyacá (Colombia). virus infections in cattle herds of Manabí province of Rev Mex Cienc Pecu. 2022;13(1):200–210. doi:10.22319/ Ecuador. Pathogens. 2021;10(11):1445. doi:10.3390/ rmcp.v13i1.5675 pathogens10111445 4 9. Vilchez-Tineo C, Morales-Cauti S. Seroprevalence of anti- 37. Ferreira Neto JV, Menezes Silva AP, Carvalho Mesquita D, bodies against the infectious bovine rinotracheitis virus in Soares de Araujo JA, Pereira Silva JW, Costa Pessoa FA. extensive cattle herds in three districts of Ayacucho, Peru. First record of antibodies to the bluetongue vírus in ewe Rev Invest Vet Perú. 2022;33(2):e22577. doi:10.15381/ (Ovis aries) in the state of Amazonas, Brazil. R Bras Ci Vet. rivep.v33i2.22577 2022;29(2):81–84. doi:10.4322/rbcv.2022.015x 50. Gutiérrez SE, Lützelschwab CM, Barrios CN, et al. 3 8. Deem SL, Noss AJ, Villarroel R, Uhart MM, Karesh WB. Bovine leukosis: an updated review. Rev Invest Vet Perú. Disease survey of free-ranging grey brocket deer (Mazama 2020;31(3):e16913. doi:10.15381/rivep.v31i3.16913 8 AJVR Unauthenticated | Downloaded 02/12/24 07:48 PM UTC