{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,28]],"date-time":"2026-08-28T08:22:50Z","timestamp":1787905370394,"version":"build-2784847793"},"reference-count":60,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2020,11,11]],"date-time":"2020-11-11T00:00:00Z","timestamp":1605052800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004681","name":"Higher Education Commission, Pakistan","doi-asserted-by":"publisher","award":["7173\/Punjab\/NRPU\/R&D\/HEC\/2017 and 8570\/Punjab\/NRPU\/R&D\/HEC\/2017"],"award-info":[{"award-number":["7173\/Punjab\/NRPU\/R&D\/HEC\/2017 and 8570\/Punjab\/NRPU\/R&D\/HEC\/2017"]}],"id":[{"id":"10.13039\/501100004681","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>The current vaccines to control bovine Babesia bigemina (B. bigemina) infection are not fully protective and vaccination failures incur heavy losses to the cattle industry around the world. Using modified micro-aerophilous stationary phase, we developed a culture-derived attenuated live vaccine against B. bigemina and tested a single subcutaneous inoculation of 2 \u00d7 108 infected erythrocytes in calves. The protection was measured after a lethal intravenous challenge with 5 \u00d7 108 virulent calf-derived B. bigemina. Our results demonstrated that a single shot of attenuated vaccine was capable of inducing robust humoral and cell-mediated immune responses in calves. We found a significant increase in the IgG antibody titers post-challenge and a strong proliferation of both CD4+ and CD8+ T cells contributing towards the protection. Our vaccine provided complete protection and parasitic clearance, which was followed for more than 100 days post-challenge. This immunity against babesiosis was directly linked to strong humoral responses; however, the parasitic clearance was attributed to significant T cells effector responses in vaccinated calves as compared to the infected control calves. We anticipate that these results will be helpful in the development of more efficient culture-derived vaccines against Babesia infections, thus reducing significant global economic losses to farmers and the cattle industry.<\/jats:p>","DOI":"10.3390\/pathogens9110936","type":"journal-article","created":{"date-parts":[[2020,11,11]],"date-time":"2020-11-11T19:08:28Z","timestamp":1605121708000},"page":"936","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Humoral and Cell-Mediated Immune Response Validation in Calves after a Live Attenuated Vaccine of Babesia bigemina"],"prefix":"10.3390","volume":"9","author":[{"given":"Umber","family":"Rauf","sequence":"first","affiliation":[{"name":"Department of Parasitology, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"},{"name":"Veterinary Research Institute (VRI), Lahore 54810, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8076-2440","authenticated-orcid":false,"given":"Muhammad","family":"Suleman","sequence":"additional","affiliation":[{"name":"University Diagnostic Laboratory, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"},{"name":"Institute of Microbiology, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8833-1530","authenticated-orcid":false,"given":"Asadullah","family":"Abid","sequence":"additional","affiliation":[{"name":"Department of Parasitology, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7159-3673","authenticated-orcid":false,"given":"Hamna","family":"Jamil","sequence":"additional","affiliation":[{"name":"Department of Parasitology, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6773-8304","authenticated-orcid":false,"given":"Harish","family":"Menghwar","sequence":"additional","affiliation":[{"name":"Vaccine and Infectious Disease Organization, International Vaccine Center (VIDO-InterVac), Saskatoon, SK S7N 5E3, Canada"},{"name":"Molecular Immunology &amp; Vaccine Development of Infectious Diseases, University of Saskatchewan, Saskatoon, SK S7N 5A2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aneela Zameer","family":"Durrani","sequence":"additional","affiliation":[{"name":"Department of Clinical Medicine and Surgery, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0280-9335","authenticated-orcid":false,"given":"Muhammad Imran","family":"Rashid","sequence":"additional","affiliation":[{"name":"Department of Parasitology, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8294-5862","authenticated-orcid":false,"given":"Haroon","family":"Akbar","sequence":"additional","affiliation":[{"name":"Department of Parasitology, University of Veterinary and Animal Sciences, Lahore 54000, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,11,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"151","DOI":"10.14202\/vetworld.2018.151-160","article-title":"Projected economic losses due to vector and vector-borne parasitic diseases in livestock of india and its significance in implementing the concept of integrated practices for vector management","volume":"11","author":"Narladkar","year":"2018","journal-title":"Vet. World"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1128\/CVI.00388-10","article-title":"Spherical body protein 4 is a new serological antigen for global detection of Babesia bovis infection in cattle","volume":"18","author":"Terkawi","year":"2011","journal-title":"Clin. Vaccine Immunol."},{"key":"ref_3","unstructured":"Pegram, R.G., Tatchell, R.J., de Castro, J.J., Chizyuka, H.G.B., Creek, M.J., McCosker, P.J., Moran, M.C., and Nigarura, G. (2020, August 27). Ticks in a Changing World\u2014Les Tiques dans un Monde en \u00c9volution\u2014Las Garrapatas en un Mundo en Evoluci\u00f3n. Available online: http:\/\/www.fao.org\/3\/u9550T04.htm."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/j.ttbdis.2015.12.012","article-title":"A review of reverse vaccinology approaches for the development of vaccines against ticks and tick borne diseases","volume":"7","year":"2016","journal-title":"Ticks Tick. Borne. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1007\/s12639-012-0119-y","article-title":"Prevalence of parasitic infections in cattle of Ludhiana district, Punjab","volume":"36","author":"Singh","year":"2012","journal-title":"J. Parasit. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1504","DOI":"10.2174\/092986712799828355","article-title":"Current Advances in Detection and Treatment of Babesiosis","volume":"19","author":"Mosqueda","year":"2012","journal-title":"Curr. Med. Chem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-016-1859-9","article-title":"Identification of interchangeable cross-species function of elongation factor-1 alpha promoters in Babesia bigemina and Babesia bovis","volume":"9","author":"Silva","year":"2016","journal-title":"Parasites Vectors"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.ttbdis.2016.09.019","article-title":"Multiple resistance to acaricides in field populations of Rhipicephalus microplus from Rio Grande do Sul state, Southern Brazil","volume":"8","author":"Klafke","year":"2017","journal-title":"Ticks Tick. Borne. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1071\/AN17157","article-title":"Resistance to the tick Rhipicephalus microplus and Babesia bovis infection levels in beef heifers raised in an endemic area of Sao Paulo state, Brazil","volume":"59","author":"Maiorano","year":"2019","journal-title":"Anim. Prod. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.vetpar.2011.05.032","article-title":"Emerging perspectives in the research of bovine babesiosis and anaplasmosis","volume":"180","author":"Suarez","year":"2011","journal-title":"Vet. Parasitol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/j.parint.2010.06.004","article-title":"Artesunate, a potential drug for treatment of Babesia infection","volume":"59","author":"Goo","year":"2010","journal-title":"Parasitol. Int."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.ijpddr.2019.02.001","article-title":"Development of unstable resistance to diminazene aceturate in Babesia bovis","volume":"9","author":"Tuvshintulga","year":"2019","journal-title":"Int. J. Parasitol. Drugs Drug Resist."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Yoshida, M., Reyes, S.G., Tsuda, S., Horinouchi, T., Furusawa, C., and Cronin, L. (2017). Time-programmable drug dosing allows the manipulation, suppression and reversal of antibiotic drug resistance in vitro. Nat. Commun., 8.","DOI":"10.1038\/ncomms15589"},{"key":"ref_14","first-page":"239","article-title":"Molecular characterization and expression of the apical membrane antigen-1 from in vivo and in vitro isolates of Babesia bigemina Kayseri\/Turkey strain","volume":"3","author":"Yildirim","year":"2018","journal-title":"Ankara \u00dcniv. Vet. Fak\u00fcltesi Derg."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1111\/j.1751-0813.2001.tb10931.x","article-title":"Immunity following use of Australian tick fever vaccine: A review of the evidence","volume":"79","author":"Bock","year":"2001","journal-title":"Aust. Vet. J."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/S0020-7519(97)00034-9","article-title":"Development of effective living vaccines against bovine babesiosis\u2014The longest field trial?","volume":"27","author":"Callow","year":"1997","journal-title":"Int. J. Parasitol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/0304-4017(93)90193-Q","article-title":"Live and soluble antigens for cattle protection to Babesia bigemina","volume":"51","author":"Echaide","year":"1993","journal-title":"Vet. Parasitol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1111\/j.1751-0813.1989.tb09738.x","article-title":"Comparison of immunogenicity and virulence between Babesia bigemina parasites from continuous culture and from a splenectomised calf","volume":"66","author":"Jorgensen","year":"1989","journal-title":"Aust. Vet. J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/0304-4017(95)00839-X","article-title":"Viability after thawing and dilution of simultaneously cryopreserved vaccinal Babesia bovis and Babesia bigemina strains cultured in vitro","volume":"61","author":"Mangold","year":"1996","journal-title":"Vet. Parasitol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.vetpar.2005.01.013","article-title":"Vaccination of older Bos taurus bulls against bovine babesiosis","volume":"129","author":"Shkap","year":"2005","journal-title":"Vet. Parasitol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.meegid.2012.12.005","article-title":"Multi-locus typing scheme for Babesia bovis and Babesia bigemina reveals high levels of genetic variability in strains from Northern Argentina","volume":"14","author":"Guillemi","year":"2013","journal-title":"Infect. Genet. Evol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Allred, D.R. (2019). Variable and Variant Protein Multigene Families in Babesia bovis Persistence. Pathogens, 8.","DOI":"10.3390\/pathogens8020076"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1111\/j.1751-0813.1981.tb07075.x","article-title":"Development of a highly infective Babesia bigemina vaccine of reduced virulance","volume":"57","author":"Dalgliesh","year":"1981","journal-title":"Aust. Vet. J."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1046\/j.1365-3024.1998.00169.x","article-title":"Amelioration of virulent Babesia bovis infection in calves by administration of the nitric oxide synthase inhibitor aminoguanidine","volume":"20","author":"Gale","year":"1998","journal-title":"Parasite Immunol."},{"key":"ref_25","first-page":"416","article-title":"In vitro cultivation of Babesia bigemina","volume":"46","author":"Vega","year":"1985","journal-title":"Am. J. Vet. Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1111\/j.1749-6632.2000.tb05286.x","article-title":"Culture-Derived Parasites in Vaccination of Cattle against Tick-Borne Diseases","volume":"916","author":"Shkap","year":"2006","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1535","DOI":"10.2741\/4659","article-title":"Immunological control of ticks and tick-borne diseases that impact cattle health and production","volume":"23","author":"Almazan","year":"2018","journal-title":"Front. Biosci.-Landmark"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1007\/BF02243499","article-title":"Australian frozen vaccines for the control of babesiosis and anaplasmosis in cattle\u2014A review","volume":"22","author":"Dalgliesh","year":"1990","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.parint.2017.11.004","article-title":"Bovine babesiosis: Cattle protected in the field with a frozen vaccine containing Babesia bovis and Babesia bigemina cultured in vitro with a serum-free medium","volume":"67","author":"Carrasco","year":"2018","journal-title":"Parasitol. Int."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/j.parint.2015.04.005","article-title":"Co-immunization of cattle with a vaccine against babesiosis and Lactobacillus casei increases specific IgG1 levels to Babesia bovis and B. bigemina","volume":"64","author":"Lozano","year":"2015","journal-title":"Parasitol. Int."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"364","DOI":"10.3389\/fvets.2020.00364","article-title":"An Overview of Current Knowledge on in vitro Babesia Cultivation for Production of Live Attenuated Vaccines for Bovine Babesiosis in Mexico","volume":"7","author":"Alvarez","year":"2020","journal-title":"Front. Vet. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.pt.2005.02.006","article-title":"Vaccination against canine babesiosis","volume":"21","author":"Schetters","year":"2005","journal-title":"Trends Parasitol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.vetpar.2012.01.008","article-title":"Genetic detection of Babesia bigemina from Mongolian cattle using apical membrane antigen-1 gene-based PCR assay","volume":"187","author":"Sivakumar","year":"2012","journal-title":"Vet. Parasitol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1218","DOI":"10.1126\/science.7355284","article-title":"Babesia bovis: Continuous cultivation in a microaerophilous stationary phase culture","volume":"207","author":"Levy","year":"1980","journal-title":"Science (80-.)"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.vetpar.2007.02.018","article-title":"Babesia bigemina: Attenuation of an Uzbek isolate for immunization of cattle with live calf- or culture-derived parasites","volume":"146","author":"Shkap","year":"2007","journal-title":"Vet. Parasitol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1590\/S0074-02762001000200017","article-title":"Development of an Enzyme-linked Immunosorbent Assay for Detection of IgM Antibodies to Babesia bigemina in Cattle","volume":"96","author":"Passos","year":"2001","journal-title":"Mem. Inst. Oswaldo Cruz"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1080\/21691401.2018.1478421","article-title":"Induction of Th1 type-oriented humoral response through intranasal immunization of mice with SAG1- Toxoplasma gondii polymeric nanospheres","volume":"46","author":"Naeem","year":"2018","journal-title":"Artif. Cells Nanomed. Biotechnol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Suleman, M., Prysliak, T., Clarke, K., Burrage, P., Windeyer, C., and Perez-Casal, J. (2016). Mycoplasma bovis isolates recovered from cattle and bison (Bison bison) show differential in vitro effects on PBMC proliferation, alveolar macrophage apoptosis and invasion of epithelial and immune cells. Vet. Microbiol., 186.","DOI":"10.1016\/j.vetmic.2016.02.016"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Bock, R., Jackson, L., De Vos, A., and Jorgensen, W. (2004). Babesiosis of cattle. Parasitology, 129.","DOI":"10.1017\/S0031182004005190"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"109136","DOI":"10.1016\/j.vetpar.2020.109136","article-title":"Bovine babesiosis: An insight into the global perspective on the disease distribution by systematic review and meta-analysis","volume":"283","author":"Jacob","year":"2020","journal-title":"Vet. Parasitol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.ijpara.2018.11.002","article-title":"Unravelling the cellular and molecular pathogenesis of bovine babesiosis: Is the sky the limit?","volume":"49","author":"Suarez","year":"2019","journal-title":"Int. J. Parasitol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/s13567-018-0543-9","article-title":"Cooperation of PD-1 and LAG-3 in the exhaustion of CD4+ and CD8+ T cells during bovine leukemia virus infection","volume":"49","author":"Okagawa","year":"2018","journal-title":"Vet. Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1186\/1297-9716-42-103","article-title":"Increase of cells expressing PD-L1 in bovine leukemia virus infection and enhancement of anti-viral immune responses in vitro via PD-L1 blockade","volume":"42","author":"Ikebuchi","year":"2011","journal-title":"Vet. Res."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Suleman, M., Cyprian, F.S., Jimbo, S., Maina, T., Prysliak, T., Windeyer, C., and Perez-Casal, J. (2018). Mycoplasma bovis-induced inhibition of bovine peripheral blood mononuclear cell proliferation is ameliorated after blocking the immune-inhibitory programmed death 1 receptor. Infect. Immun., 86.","DOI":"10.1128\/IAI.00921-17"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1881","DOI":"10.1128\/CVI.00257-10","article-title":"Anaplasma marginale infection with persistent high-load bacteremia induces a dysfunctional memory CD4+ T lymphocyte response but sustained high IgG titers","volume":"17","author":"Han","year":"2010","journal-title":"Clin. Vaccine Immunol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2418","DOI":"10.1128\/iai.59.7.2418-2426.1991","article-title":"Cell-mediated immune responses to Babesia bovis merozoite antigens in cattle following infection with tick-derived or cultured parasites","volume":"59","author":"Brown","year":"1991","journal-title":"Infect. Immun."},{"key":"ref_47","first-page":"736","article-title":"Role of T cells and cytokines in fatal and resolving experimental babesiosis: Protection in tnfrp55\u2212\/\u2212 mice infected with the human babesia wa1 parasite","volume":"86","author":"Hemmer","year":"2000","journal-title":"J. Parasitol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1128\/iai.60.2.644-652.1992","article-title":"Induction of proliferative responses of T cells from Babesia bovis-immune cattle with a recombinant 77-kilodalton merozoite protein (Bb-1)","volume":"60","author":"Tetzlaff","year":"1992","journal-title":"Infect. Immun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1016\/j.cyto.2012.06.090","article-title":"P007 IL-21, B cells and CD4-CD8- T cells are key for resistance to Babesia microti infection in immunosuppressed hosts","volume":"59","author":"Wilson","year":"2012","journal-title":"Cytokine"},{"key":"ref_50","first-page":"65","article-title":"T-cell antigens and epitopes in malaria vaccine design","volume":"155","author":"Good","year":"1990","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"271","DOI":"10.4049\/jimmunol.144.1.271","article-title":"Recognition of soluble Theileria parva antigen by bovine helper T cell clones: Characterization and partial purification of the antigen","volume":"144","author":"Brown","year":"1990","journal-title":"J. Immunol."},{"key":"ref_52","unstructured":"Siegrist, C.-A. (2018). Plotkin\u2019s Vaccines, Elsevier."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1084\/jem.20011174","article-title":"The mechanism and significance of deletion of parasite-specific CD4+ T cells in malaria infection","volume":"195","author":"Xu","year":"2002","journal-title":"J. Exp. Med."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1016\/j.exppara.2010.05.008","article-title":"Regulation of CD8+ T cell responses to infection with parasitic protozoa","volume":"126","author":"Jordan","year":"2010","journal-title":"Exp. Parasitol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"169","DOI":"10.2174\/1573395509666131126232327","article-title":"CD8+ T Cell Responses to Plasmodium and Intracellular Parasites","volume":"9","author":"Villarino","year":"2014","journal-title":"Curr. Immunol. Rev."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"136","DOI":"10.3389\/fcimb.2019.00136","article-title":"Toxoplasma gondii: CD8 T Cells Cry for CD4 Help","volume":"9","author":"Khan","year":"2019","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"4625","DOI":"10.1016\/j.vaccine.2014.06.075","article-title":"Vaccine strategies against Babesia bovis based on prime-boost immunizations in mice with modified vaccinia Ankara vector and recombinant proteins","volume":"32","author":"Zanetti","year":"2014","journal-title":"Vaccine"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1963","DOI":"10.3389\/fimmu.2018.01963","article-title":"New vaccine technologies to combat outbreak situations","volume":"9","author":"Rauch","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.vetpar.2006.01.041","article-title":"Immune control of Babesia bovis infection","volume":"138","author":"Brown","year":"2006","journal-title":"Vet. Parasitol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3913","DOI":"10.1016\/j.vaccine.2016.05.053","article-title":"Evaluation of different heterologous prime\u2013boost immunization strategies against Babesia bovis using viral vectored and protein-adjuvant vaccines based on a chimeric multi-antigen","volume":"34","author":"Molinari","year":"2016","journal-title":"Vaccine"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/11\/936\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:32:07Z","timestamp":1760178727000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/11\/936"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,11,11]]},"references-count":60,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11]]}},"alternative-id":["pathogens9110936"],"URL":"https:\/\/doi.org\/10.3390\/pathogens9110936","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,11,11]]}}}