{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T06:20:51Z","timestamp":1781072451822,"version":"3.54.1"},"reference-count":51,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2025,5,21]],"date-time":"2025-05-21T00:00:00Z","timestamp":1747785600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"MSCA4Ukraine project","award":["1233283"],"award-info":[{"award-number":["1233283"]}]},{"name":"MSCA4Ukraine project","award":["101003575"],"award-info":[{"award-number":["101003575"]}]},{"name":"MSCA4Ukraine project","award":["TH79020003"],"award-info":[{"award-number":["TH79020003"]}]},{"name":"MSCA4Ukraine project","award":["0125U000500"],"award-info":[{"award-number":["0125U000500"]}]},{"name":"Horizon 2020 Program","award":["1233283"],"award-info":[{"award-number":["1233283"]}]},{"name":"Horizon 2020 Program","award":["101003575"],"award-info":[{"award-number":["101003575"]}]},{"name":"Horizon 2020 Program","award":["TH79020003"],"award-info":[{"award-number":["TH79020003"]}]},{"name":"Horizon 2020 Program","award":["0125U000500"],"award-info":[{"award-number":["0125U000500"]}]},{"name":"Technology Agency of the Czech Republic","award":["1233283"],"award-info":[{"award-number":["1233283"]}]},{"name":"Technology Agency of the Czech Republic","award":["101003575"],"award-info":[{"award-number":["101003575"]}]},{"name":"Technology Agency of the Czech Republic","award":["TH79020003"],"award-info":[{"award-number":["TH79020003"]}]},{"name":"Technology Agency of the Czech Republic","award":["0125U000500"],"award-info":[{"award-number":["0125U000500"]}]},{"name":"Ministry of Education and Science of Ukraine","award":["1233283"],"award-info":[{"award-number":["1233283"]}]},{"name":"Ministry of Education and Science of Ukraine","award":["101003575"],"award-info":[{"award-number":["101003575"]}]},{"name":"Ministry of Education and Science of Ukraine","award":["TH79020003"],"award-info":[{"award-number":["TH79020003"]}]},{"name":"Ministry of Education and Science of Ukraine","award":["0125U000500"],"award-info":[{"award-number":["0125U000500"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Waste from livestock farms contains various pathogens, including eggs and larvae of helminths\u2014pathogens of parasitic diseases harmful to animals and humans. One of the methods for their effective processing to obtain biofertilizer and biofuel is anaerobic digestion, which requires further improvement to completely suppress the viability of pathogenic microorganisms in mesophilic conditions. To this end, the use of anaerobic digestion under sulfate reduction conditions to suppress pathogens using biogenic hydrogen sulfide is promising. Consequently, this study aims to study the effect of a sulfur-containing additive such as phosphogypsum on the disinfection of pig manure during anaerobic digestion. Egg mortality was already found to increase significantly compared to the control (80% and more), even at a minimum concentration of phosphogypsum (5%), on the fifth day of the experiment. At the same time, the maximum effect (100% mortality of Trichuris suis eggs) was recorded at a 10% concentration of phosphogypsum, starting from the 10th day of the study. Our experiment showed that changes in anaerobic digestion conditions using phosphogypsum could positively affect digestate disinfection. However, further research is needed to optimize the conditions of the process for an effective combination of disinfection with the production of environmentally safe organic fertilizers and high-quality biogas with a high level of methane.<\/jats:p>","DOI":"10.3390\/microorganisms13051165","type":"journal-article","created":{"date-parts":[[2025,5,21]],"date-time":"2025-05-21T04:05:17Z","timestamp":1747800317000},"page":"1165","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Impact of Phosphogypsum on Viability of Trichuris suis Eggs in Anaerobic Digestion of Swine Manure"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7299-9920","authenticated-orcid":false,"given":"Olexandra","family":"Boyko","sequence":"first","affiliation":[{"name":"Department of Parasitology and Veterinary and Sanitary Expertise, Dnipro State Agrarian and Economic University, Serhii Efremov St., 25, 49000 Dnipro, Ukraine"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9448-8232","authenticated-orcid":false,"given":"Viktor","family":"Brygadyrenko","sequence":"additional","affiliation":[{"name":"Department of Biodiversity and Ecology, Oles Honchar Dnipro National University, Nauky Av., 72, 49010 Dnipro, Ukraine"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4103-4306","authenticated-orcid":false,"given":"Yelizaveta","family":"Chernysh","sequence":"additional","affiliation":[{"name":"Department of Sustainable Technologies, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Kam\u00fdck\u00e1 129, 16500 Prague, Czech Republic"},{"name":"Department of Ecology and Environmental Protection Technologies, Sumy State University, Kharkivska St., 116, 40007 Sumy, Ukraine"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Viktoriia","family":"Chubur","sequence":"additional","affiliation":[{"name":"Department of Sustainable Technologies, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Kam\u00fdck\u00e1 129, 16500 Prague, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7498-4140","authenticated-orcid":false,"given":"Hynek","family":"Roub\u00edk","sequence":"additional","affiliation":[{"name":"Department of Sustainable Technologies, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Kam\u00fdck\u00e1 129, 16500 Prague, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Kiyasudeen, K.S., Ibrahim, M.H., Quaik, S., and Ismail, S.A. (2015). Introduction to organic wastes and its management. Prospects of Organic Waste Management and the Significance of Earthworms, Springer.","DOI":"10.1007\/978-3-319-24708-3"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e18208","DOI":"10.1016\/j.heliyon.2023.e18208","article-title":"Trends in the management of organic swine farm waste by composting: A systematic review","volume":"9","year":"2023","journal-title":"Heliyon"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"306","DOI":"10.54846\/jshap\/662","article-title":"Trichuris suis in finishing pigs: Case report and review","volume":"18","author":"Pittman","year":"2010","journal-title":"J. Swine Health Prod."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"B\u00fcnger, M., Renzhammer, R., Joachim, A., Hinney, B., Brunthaler, R., Al Hossan, M., Matt, J., Nedorost, N., Weissenbacher-Lang, C., and Schwarz, L. (2022). Trichurosis on a conventional swine fattening farm with extensive husbandry\u2014A case report. Pathogens, 11.","DOI":"10.3390\/pathogens11070775"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"105","DOI":"10.5152\/actavet.2023.22119","article-title":"Effect of temperature on the survival rates of the embryonic states of development of Trichuris skrjabini nematodes parasitizing sheep","volume":"49","author":"Yevstafieva","year":"2023","journal-title":"Acta Vet. Eurasia"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"70","DOI":"10.15421\/022311","article-title":"Effect of disinfectants on viability of Trichuris skrjabini eggs","volume":"14","author":"Yevstafieva","year":"2023","journal-title":"Regul. Mech. Biosyst."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Rusanowska, P., Zieli\u0144ski, M., Kisielewska, M., Dudek, M., Paukszto, \u0141., and D\u0119bowski, M. (2025). Methane production, microbial community, and volatile fatty acids profiling during anaerobic digestion under different organic loading. Energies, 18.","DOI":"10.20944\/preprints202501.1245.v1"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Kabaivanova, L., Hubenov, V., Dimitrova, L., Simeonov, I., Wang, H., and Petrova, P. (2022). Archaeal and bacterial content in a two-stage anaerobic system for efficient energy production from agricultural wastes. Molecules, 27.","DOI":"10.3390\/molecules27051512"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Lee, H., Fitamo, T.M., Nesb\u00f8, C.L., Guilford, N.G.H., Kanger, K., Yang, M.I., and Edwards, E.A. (2022). Microbial community dynamics of a sequentially fed anaerobic digester treating solid organic waste. bioRxiv, 99.","DOI":"10.1101\/2022.04.10.487789"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"260","DOI":"10.15421\/012428","article-title":"Recycling and decontamination of organic waste in Ukraine: Current state, technologies and prospects for the biogas industry","volume":"32","author":"Boyko","year":"2024","journal-title":"Biosyst. Divers."},{"key":"ref_11","first-page":"58","article-title":"Viability of exogenous stages of development of the causative agent of trichuriasis of dogs under the influence of temperature","volume":"107","author":"Yevstafieva","year":"2022","journal-title":"Sci. Messenger LNU Vet. Med. Biotechnol. Ser. Vet. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1515\/vzoo-2016-0020","article-title":"An investigation of embryo and eggshell development in Trichuris suis (Nematoda, Trichuridae) under laboratory conditions","volume":"50","author":"Yevstafieva","year":"2016","journal-title":"Vestn. Zool."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"5527","DOI":"10.1016\/j.biortech.2009.02.038","article-title":"Livestock waste treatment systems for environmental quality, food safety, and sustainability","volume":"100","author":"Martinez","year":"2009","journal-title":"Bioresour. Technol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"321","DOI":"10.22271\/j.ento.2022.v10.i5d.9075","article-title":"Livestock waste management practices to strengthen the farm profitability","volume":"10","author":"Shakya","year":"2022","journal-title":"J. Entomol. Zool. Stud."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Boyko, O., and Brygadyrenko, V. (2022). Nematicidal activity of inorganic food additives. Diversity, 14.","DOI":"10.3390\/d14080663"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Boyko, O., and Brygadyrenko, V. (2023). Survival of nematode larvae Strongyloides papillosus and Haemonchus contortus under the influence of various groups of organic compounds. Diversity, 15.","DOI":"10.3390\/d15020254"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3128","DOI":"10.1021\/es505807a","article-title":"Assessing the fate of Ascaris suum ova during mesophilic anaerobic digestion","volume":"49","author":"Manser","year":"2015","journal-title":"Environ. Sci. Technol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"93","DOI":"10.12688\/gatesopenres.14573.2","article-title":"Study of helminth eggs (Ascaris suum) inactivation by anaerobic digestion and electrochemical treatment","volume":"7","author":"Patil","year":"2024","journal-title":"Gates Open Res."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Shao, Z., Guo, X., Qu, Q., Kang, K., Su, Q., Wang, C., and Qiu, L. (2021). Effects of chlorine disinfectants on the microbial community structure and the performance of anaerobic digestion of swine manure. Bioresour. Technol., 339.","DOI":"10.1016\/j.biortech.2021.125576"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/j.wasman.2005.02.010","article-title":"Factors controlling pathogen destruction during anaerobic digestion of biowastes","volume":"25","author":"Smith","year":"2005","journal-title":"Waste Manag."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/j.jes.2015.11.013","article-title":"Anaerobic digestion in mesophilic and room temperature conditions: Digestion performance and soil-borne pathogen survival","volume":"43","author":"Chen","year":"2016","journal-title":"J. Environ. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Boyko, O., Brygadyrenko, V., Chernysh, Y., Chubur, V., and Roub\u00edk, H. (2024). Possibilities of decontaminating organic waste from swine-farming complexes using anaerobic digestion. Biomass Convers. Biorefin., in press.","DOI":"10.1007\/s13399-024-05914-6"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"120787","DOI":"10.1016\/j.watres.2023.120787","article-title":"Disinfectant sodium dichloroisocyanurate synergistically strengthened sludge acidogenic process and pathogens inactivation: Targeted upregulation of functional microorganisms and metabolic traits via self-adaptation","volume":"247","author":"Huang","year":"2023","journal-title":"Water Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.psep.2022.11.089","article-title":"Insights into the phenol disinfectant on the methane performance from wastewater by mesophilic anaerobic digestion: Single and two stages analysis","volume":"170","author":"Xu","year":"2023","journal-title":"Process Saf. Environ. Prot."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"866","DOI":"10.3390\/microorganisms3040866","article-title":"Hydrogen sulfide in physiology and diseases of the digestive tract","volume":"3","author":"Singh","year":"2015","journal-title":"Microorganisms"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1089\/ars.2021.0004","article-title":"Effects of hydrogen sulfide on the microbiome: From toxicity to therapy","volume":"36","author":"Buret","year":"2022","journal-title":"Antioxid. Redox Signal."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1134\/S0026893322050120","article-title":"Enhancement of the bactericidal effect of antibiotics by inhibition of enzymes involved in production of hydrogen sulfide in bacteria","volume":"56","author":"Seregina","year":"2022","journal-title":"Mol. Biol."},{"key":"ref_28","first-page":"1105","article-title":"Composition, structure and physical-chemical properties of phosphogypsum","volume":"10","author":"Jovliyev","year":"2022","journal-title":"Galaxy Int. Interdiscip. Res. J."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Plyatsuk, L., Balintova, M., Chernysh, Y., Demcak, S., Holub, M., and Yakhnenko, E. (2019). Influence of phosphogypsum dump on the soil ecosystem in the Sumy Region (Ukraine). Appl. Sci., 9.","DOI":"10.3390\/app9245559"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Chernysh, Y., Yakhnenko, O., Chubur, V., and Roub\u00edk, H. (2021). Phosphogypsum recycling: A review of environmental issues, current trends, and prospects. Appl. Sci., 11.","DOI":"10.3390\/app11041575"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Onopriienko, D., Makarova, T., Hapich, H., Chernysh, Y., and Roub\u00edk, H. (2024). Agroecological transformation in the salt composition of soil under the phosphogypsum influence on irrigated lands in Ukraine. Agriculture, 14.","DOI":"10.3390\/agriculture14030408"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.1080\/10426507.2022.2052881","article-title":"Reduction of phosphogypsum to calcium sulfide (CaS) using metallic iron in a hydrochloric acid medium","volume":"197","author":"Alla","year":"2022","journal-title":"Phosphorus Sulfur Silicon Relat. Elem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"166296","DOI":"10.1016\/j.scitotenv.2023.166296","article-title":"Effect of alkaline leaching of phosphogypsum on sulfate reduction activity and bacterial community composition using different sources of anaerobic microbial inoculum","volume":"904","author":"Bounaga","year":"2023","journal-title":"Sci. Total Environ."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1016\/j.ibiod.2005.09.003","article-title":"Sulfate reduction from phosphogypsum using a mixed culture of sulfate-reducing bacteria","volume":"56","author":"Azabou","year":"2005","journal-title":"Int. Biodeterior. Biodegrad."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1021\/acsestengg.4c00563","article-title":"Sulfate leached from phosphogypsum is transformed in a hydrogen-based membrane biofilm reactor","volume":"5","author":"Alsanea","year":"2024","journal-title":"ACS ES&T Eng."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Medennikov, O.A., Egorova, M.A., Shabelskaya, N.P., Rajabov, A., Sulima, S.I., Sulima, E.V., Khliyan, Z.D., and Monastyrskiy, D.I. (2024). Studying the process of phosphogypsum recycling into a calcium sulphide-based luminophor. Nanomaterials, 14.","DOI":"10.3390\/nano14110904"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Verma, S., Malik, Y.S., Singh, G., Dhar, P., and Singla, A.K. (2024). Aseptic collection, preservation, and dispatch of samples for disease diagnosis. Core Competencies of a Veterinary Graduate, Springer.","DOI":"10.1007\/978-981-97-0433-0"},{"key":"ref_38","unstructured":"Zajac, A.M., and Conboy, G.A. (2011). Veterinary Clinical Parasitology, John Wiley and Sons. [8th ed.]."},{"key":"ref_39","unstructured":"Zhuravel, S.V., Kravchuk, M.M., Kropyvnytskyi, R.B., Klymenko, T.V., Trembitska, O.I., Radko, V.H., Nihorodova, S.A., Dyachenko, M.O., Zhuravel, S.S., and Polishchuk, V.O. (2020). Orhanichni dobryva [Organic fertilizers], Polisskyi University Press. (In Ukrainian)."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.biortech.2016.02.077","article-title":"Biogas production and microbial community shift through neutral pH control during the anaerobic digestion of pig manure","volume":"217","author":"Zhou","year":"2016","journal-title":"Bioresour. Technol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1186\/s13568-022-01486-8","article-title":"Effect of the initial pH on the anaerobic digestion process of dairy cattle manure","volume":"12","year":"2022","journal-title":"AMB Express"},{"key":"ref_42","first-page":"H11","article-title":"Effect of phosphogypsum addition on methane yield in biogas and digestate properties during anaerobic digestion","volume":"9","author":"Chubur","year":"2022","journal-title":"J. Eng. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1128\/aem.35.6.1027-1034.1978","article-title":"Effect of sulfur-containing compounds on anaerobic degradation of cellulose to methane by mixed cultures obtained from sewage sludge","volume":"35","author":"Khan","year":"1978","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Maslova, O., Senko, O., Stepanov, N., Gladchenko, M., Gaydamaka, S., Akopyan, A., Eseva, E., Anisimov, A., and Efremenko, E. (2022). Sulfur containing mixed wastes in anaerobic processing by new immobilized synthetic consortia. Bioresour. Technol., 362.","DOI":"10.1016\/j.biortech.2022.127794"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e19768","DOI":"10.1016\/j.heliyon.2023.e19768","article-title":"Approaches to mitigation of hydrogen sulfide during anaerobic digestion process\u2014A review","volume":"9","author":"Mutegoa","year":"2023","journal-title":"Heliyon"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"120013","DOI":"10.1016\/j.watres.2023.120013","article-title":"Thiosulfate pretreatment enhancing short-chain fatty acids production from anaerobic fermentation of waste activated sludge: Performance, metabolic activity and microbial community","volume":"238","author":"Cheng","year":"2023","journal-title":"Water Res."},{"key":"ref_47","first-page":"774","article-title":"Advancing circular bioeconomy: Trends, clusters, and roadmaps in biofuel production and waste valorisation","volume":"22","author":"Chernysh","year":"2024","journal-title":"Agron. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1016\/0020-7519(82)90077-7","article-title":"Reversible inhibition of hatching of infective eggs of Ascaris suum (Nematoda)","volume":"12","author":"Hurley","year":"1982","journal-title":"Int. J. Parasitol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.hydromet.2018.06.020","article-title":"Continuous biological sulfate reduction from phosphogypsum waste leachate","volume":"180","author":"Salo","year":"2018","journal-title":"Hydrometallurgy"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"146072","DOI":"10.1016\/j.cej.2023.146072","article-title":"Optimization of sulfate leaching from phosphogypsum for efficient bioreduction in a batch bioreactor using a sulfate-reducing microbial consortium","volume":"475","author":"Danouche","year":"2023","journal-title":"Chem. Eng. J."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"2705","DOI":"10.1007\/s00436-015-4476-1","article-title":"In vitro hatching of Trichuris suis eggs","volume":"114","author":"Thamsborg","year":"2015","journal-title":"Parasitol. Res."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/5\/1165\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:36:09Z","timestamp":1760031369000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/5\/1165"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,21]]},"references-count":51,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["microorganisms13051165"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13051165","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,21]]}}}