{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,13]],"date-time":"2026-01-13T05:35:37Z","timestamp":1768282537695,"version":"3.49.0"},"reference-count":53,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2023,4,20]],"date-time":"2023-04-20T00:00:00Z","timestamp":1681948800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000199","name":"USDA APHIS","doi-asserted-by":"publisher","award":["AP21WSHQ0000C004"],"award-info":[{"award-number":["AP21WSHQ0000C004"]}],"id":[{"id":"10.13039\/100000199","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Anthrax is a disease that affects livestock, wildlife, and humans worldwide; however, its relative impacts on these populations remain underappreciated. Feral swine (Sus scrofa) are relatively resistant to developing anthrax, and past serosurveys have alluded to their utility as sentinels, yet empirical data to support this are lacking. Moreover, whether feral swine may assist in the dissemination of infectious spores is unknown. To address these knowledge gaps, we intranasally inoculated 15 feral swine with varying quantities of Bacillus anthracis Sterne 34F2 spores and measured the seroconversion and bacterial shedding over time. The animals also were inoculated either one or three times. The sera were evaluated by enzyme-linked immunosorbent assay (ELISA) for antibodies against B. anthracis, and nasal swabs were cultured to detect bacterial shedding from the nasal passages. We report that the feral swine developed antibody responses to B. anthracis and that the strength of the response correlated with the inoculum dose and the number of exposure events experienced. Isolation of viable bacteria from the nasal passages of the animals throughout the study period suggests that feral swine may assist in the spread of infectious spores on the landscape and have implications for the identification of environments contaminated with B. anthracis as well as the exposure risk to more susceptible hosts.<\/jats:p>","DOI":"10.3390\/pathogens12040622","type":"journal-article","created":{"date-parts":[[2023,4,21]],"date-time":"2023-04-21T02:05:31Z","timestamp":1682042731000},"page":"622","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Feral Swine as Indirect Indicators of Environmental Anthrax Contamination and Potential Mechanical Vectors of Infectious Spores"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4003-2643","authenticated-orcid":false,"given":"Rachel M.","family":"Maison","sequence":"first","affiliation":[{"name":"Department of Biomedical Sciences, Colorado State University, Fort Collins, CO 80521, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maggie R.","family":"Priore","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO 80521, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Vienna R.","family":"Brown","sequence":"additional","affiliation":[{"name":"U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, National Wildlife Research Center, Fort Collins, CO 80521, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael J.","family":"Bodenchuk","sequence":"additional","affiliation":[{"name":"U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, San Antonio, TX 78269, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bradley R.","family":"Borlee","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO 80521, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Richard A.","family":"Bowen","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Colorado State University, Fort Collins, CO 80521, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Angela M.","family":"Bosco-Lauth","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Colorado State University, Fort Collins, CO 80521, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,20]]},"reference":[{"key":"ref_1","unstructured":"Miller, R.E., and Fowler, M.E. (2012). Fowler\u2019s Zoo and Wild Animal Medicine Current Therapy, Elsevier Health Sciences."},{"key":"ref_2","first-page":"99","article-title":"Anthrax epizo tics in Etosha National Park","volume":"1977","author":"Ebedes","year":"1977","journal-title":"Madoqua"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1017\/S0950268800049773","article-title":"Serology and anthrax in humans, livestock and Etosha National Park wildlife","volume":"108","author":"Turnbull","year":"1992","journal-title":"Epidemiol. Infect."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"786","DOI":"10.7589\/2013-05-126","article-title":"Ante-and postmortem diagnostic techniques for anthrax: Rethinking pathogen exposure and the geographic extent of the disease in wildlife","volume":"49","author":"Bagamian","year":"2013","journal-title":"J. Wildl. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1526","DOI":"10.1017\/S0950268818001577","article-title":"A serological survey of anthrax in domestic dogs in Zimbabwe: A potential tool for anthrax surveillance","volume":"146","author":"Mukarati","year":"2018","journal-title":"Epidemiol. Infect."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1089\/vbz.2020.2747","article-title":"Anthrax surveillance and the limited overlap between obligate scavengers and endemic anthrax zones in the United States","volume":"21","author":"Walker","year":"2021","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"918","DOI":"10.7589\/0090-3558-46.3.918","article-title":"Confirmation of Bacillus anthracis from flesh-eating flies collected during a West Texas anthrax season","volume":"46","author":"Blackburn","year":"2010","journal-title":"J. Wildl. Dis."},{"key":"ref_8","first-page":"141","article-title":"Feeding habits and flight range of blow-flies (Chrysomyia spp.) in relation to anthrax transmission in the Kruger National Park, South Africa","volume":"57","author":"Braack","year":"1990","journal-title":"Onderstepoort J. Vet. Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"359","DOI":"10.20506\/rst.21.2.1336","article-title":"Anthrax and wildlife","volume":"21","year":"2002","journal-title":"Rev. Sci. Tech."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1046\/j.1365-2672.1999.00872.x","article-title":"A review of anthrax in Canada and implications for research on the disease in northern bison","volume":"87","author":"Dragon","year":"1999","journal-title":"J. Appl. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"34","DOI":"10.7589\/2017-04-069","article-title":"Dust-bathing behaviors of African herbivores and the potential risk of inhalational anthrax","volume":"54","author":"Barandongo","year":"2018","journal-title":"J. Wildl. Dis."},{"key":"ref_12","unstructured":"Turnbull, P.C.B. (2008). Anthrax in Humans and Animals, World Health Organization. [4th ed.]."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Glinert, I., Weiss, S., Sittner, A., Bar-David, E., Ben-Shmuel, A., Schlomovitz, J., Kobiler, D., and Levy, H. (2018). Infection with a nonencapsulated Bacillus anthracis strain in rabbits-the role of bacterial adhesion and the potential for a safe live attenuated vaccine. Toxins, 10.","DOI":"10.3390\/toxins10120506"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1016\/S0014-5793(02)03609-8","article-title":"Anthrax toxin: A tripartite lethal combination","volume":"531","author":"Ascenzi","year":"2002","journal-title":"FEBS Lett."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Friebe, S., Van der Goot, F.G., and B\u00fcrgi, J. (2016). The ins and outs of anthrax toxin. Toxins, 8.","DOI":"10.3390\/toxins8030069"},{"key":"ref_16","first-page":"295","article-title":"The ecology of anthrax spores: Tough but not invincible","volume":"36","author":"Dragon","year":"1995","journal-title":"Can. Vet. J."},{"key":"ref_17","unstructured":"Spickler, A.R. (2023, January 01). Anthrax. Available online: http:\/\/www.cfsph.iastate.edu\/DiseaseInfo\/factsheets.php."},{"key":"ref_18","first-page":"131","article-title":"Two generations of spore research: From father to son","volume":"13","author":"Halvorson","year":"1997","journal-title":"Microbiologia"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Norris, M.H., Zincke, D., Leiser, O.P., Kreuzer, H., Hadfied, T.L., and Blackburn, J.K. (2020). Laboratory strains of Bacillus anthracis lose their ability to rapidly grow and sporulate compared to wildlife outbreak strains. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0228270"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"3780","DOI":"10.1128\/JCM.38.10.3780-3784.2000","article-title":"Bacillus anthracis diversity in Kruger National Park","volume":"38","author":"Smith","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Childs, J.E., Mackenzie, J.S., and Richt, J.A. (2007). Wildlife and Emerging Zoonotic Diseases: The Biology, Circumstances and Consequences of Cross-Species Transmission, Springer.","DOI":"10.1007\/978-3-540-70962-6"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1111\/2041-210x.12021","article-title":"A hierarchical distance sampling approach to estimating mortality rates from opportunistic carcass surveillance data","volume":"4","author":"Bellan","year":"2013","journal-title":"Methods Ecol. Evol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"392","DOI":"10.4269\/ajtmh.19-0191","article-title":"Predicting the geographic distribution of the Bacillus anthracis A1. a\/Western North American sub-lineage for the continental United States: New outbreaks, new genotypes, and new climate data","volume":"102","author":"Yang","year":"2020","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1080\/00045608.2014.914834","article-title":"Spatial and temporal patterns of anthrax in white-tailed deer, Odocoileus virginianus, and hematophagous flies in west Texas during the summertime anthrax risk period","volume":"104","author":"Blackburn","year":"2014","journal-title":"Ann. Am. Assoc. Geogr."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.4269\/ajtmh.2007.77.1103","article-title":"Modeling the geographic distribution of Bacillus anthracis, the causative agent of anthrax disease, for the contiguous United States using predictive ecologic niche modeling","volume":"77","author":"Blackburn","year":"2007","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1046\/j.1365-2672.2001.01389.x","article-title":"Detection of anthrax spores in endemic regions of northern Canada","volume":"91","author":"Dragon","year":"2001","journal-title":"J. Appl. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"136","DOI":"10.7589\/0090-3558-43.1.136","article-title":"First detection of Bacillus anthracis in feces of free-ranging raptors from central Argentina","volume":"43","author":"Saggese","year":"2007","journal-title":"J. Wildl. Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1016\/j.mam.2009.07.005","article-title":"Animal models of human anthrax: The quest for the holy grail","volume":"30","author":"Goossens","year":"2009","journal-title":"Mol. Aspects Med."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3103","DOI":"10.3201\/eid2712.211482","article-title":"Potential use for serosurveillance of feral swine to map risk for anthrax exposure, Texas, USA","volume":"27","author":"Maison","year":"2021","journal-title":"J. Emerg. Infect. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1089\/vbz.2013.1521","article-title":"Serological anthrax surveillance in wild boar (Sus scrofa) in Ukraine","volume":"14","author":"Bagamian","year":"2014","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_31","unstructured":"USDA APHIS (2023, January 15). History of Feral Swine in the Americas, Available online: https:\/\/www.aphis.usda.gov\/aphis\/ourfocus\/wildlifedamage\/operational-activities\/feral-swine\/sa-fs-history."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"482","DOI":"10.2527\/jas1984.582482x","article-title":"Behavior and ecology of wild and feral swine (Sus scrofa)","volume":"58","author":"Graves","year":"1984","journal-title":"J. Anim. Sci."},{"key":"ref_33","unstructured":"USDA-WS (2020). Wildlife Services\u2019 Comprehensive Feral Swine Disease Surveillance Procedures Manual, Fiscal Year 2020, Procedure Manual for Comprehensive Feral Swine Disease Surveillance."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"4801","DOI":"10.1128\/IAI.72.8.4801-4809.2004","article-title":"Murine model of pulmonary anthrax: Kinetics of dissemination, histopathology, and mouse strain susceptibility","volume":"72","author":"Lyons","year":"2004","journal-title":"Infect. Immun."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"3189","DOI":"10.1016\/S0021-9258(18)62213-6","article-title":"The stability of messenger, ribonucleic acid during sporulation in Bacillus subtilis","volume":"246","author":"Leighton","year":"1971","journal-title":"J. Biol. Chem."},{"key":"ref_36","unstructured":"Janeway, C.A., Travers, P., Walport, M., and Shlomchik, M.J. (2001). Immunobiology: The Immune System in Health and Disease, Garland Science. [5th ed.]."},{"key":"ref_37","unstructured":"Snyder, J.W., Shapiro, D.S., Gilchrist, M.J., Wyant, R.S., Popovic, T., Ezzell, J.W., and Morse, S.A. (2002). Basic Diagnostic Testing Protocols for Level A Laboratories for the Presumptive Identification of Bacillus Anthracis, Centers for Disease Control and Prevention."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1128\/jb.92.3.784-786.1966","article-title":"Selective medium for Bacillus anthracis","volume":"92","author":"Knisely","year":"1966","journal-title":"J. Bacteriol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Ogawa, H., Fujikura, D., Ohnuma, M., Ohnishi, N., Hang\u2019ombe, B.M., Mimuro, H., Ezaki, T., Mweene, A.S., and Higashi, H. (2015). A novel multiplex PCR discriminates Bacillus anthracis and its genetically related strains from other Bacillus cereus group species. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0122004"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"e00910-16","DOI":"10.1128\/genomeA.00910-16","article-title":"Draft genome sequence of biocontrol agent Bacillus cereus UW85","volume":"4","author":"Lozano","year":"2016","journal-title":"Genome Announc."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"4214","DOI":"10.1016\/S0264-410X(01)00159-1","article-title":"Detection of anthrax vaccine virulence factors by polymerase chain reaction","volume":"19","author":"Fasanella","year":"2001","journal-title":"Vaccine"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12866-019-1693-2","article-title":"Nucleotide polymorphism assay for the identification of west African group Bacillus anthracis: A lineage lacking anthrose","volume":"20","author":"Zincke","year":"2020","journal-title":"BMC Microbiol."},{"key":"ref_43","unstructured":"CDC (2023, January 20). Anthrax Sterne, General Information, Available online: https:\/\/www.cdc.gov\/nczved\/divisions\/dfbmd\/diseases\/anthrax_sterne\/."},{"key":"ref_44","unstructured":"Strom, B.L., Durch, J.S., Zwanziger, L.L., and Joellenbeck, L.M. (2002). The Anthrax Vaccine: Is It Safe? Does it Work?, National Academy Press."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"593","DOI":"10.20506\/rst.33.2.2309","article-title":"Anthrax as an example of the one health concept","volume":"33","author":"Bengis","year":"2014","journal-title":"Rev. Sci. Tech."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1016\/j.vetmic.2009.08.016","article-title":"Anthrax undervalued zoonosis","volume":"140","author":"Fasanella","year":"2010","journal-title":"Vet. Microbiol."},{"key":"ref_47","first-page":"135","article-title":"The environmental impact of wild boar","volume":"16","author":"Massei","year":"2004","journal-title":"Galemys"},{"key":"ref_48","first-page":"348","article-title":"Tabanus flies as transmitters of anthrax-a field experience","volume":"38","author":"Mohiyudekn","year":"1958","journal-title":"Indian Vet. J."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1859","DOI":"10.1128\/iai.55.8.1859-1861.1987","article-title":"Mechanical transmission of Bacillus anthracis by stable flies (Stomoxys calcitrans) and mosquitos (Aedes aegypti and Aedes taeniorhynchus)","volume":"55","author":"Turell","year":"1987","journal-title":"Infect. Immun."},{"key":"ref_50","unstructured":"Rollins, D. (1999, January 2\u20133). Impacts of Feral Swine on Wildlife. Proceedings of the First National Feral Swine Conference, Fort Worth, TX, USA."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"488","DOI":"10.7589\/2018-05-143","article-title":"Animal visitation to wild pig (Sus scrofa) wallow and implications for disease transmission","volume":"55","author":"Eckert","year":"2019","journal-title":"J. Wildl. Dis."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2841","DOI":"10.1128\/IAI.02029-06","article-title":"Identification of in vivo-expressed immunogenic proteins by serological proteome analysis of the Bacillus anthracis secretome","volume":"75","author":"Chitlaru","year":"2007","journal-title":"Infect. Immun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"67","DOI":"10.20506\/rst.21.1.1321","article-title":"Surveillance and monitoring of wildlife diseases","volume":"21","author":"Morner","year":"2002","journal-title":"Rev. Sci. Tech."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/12\/4\/622\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:19:58Z","timestamp":1760123998000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/12\/4\/622"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,20]]},"references-count":53,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["pathogens12040622"],"URL":"https:\/\/doi.org\/10.3390\/pathogens12040622","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,20]]}}}