Microbial and chemical risks of organic fertilizers based on by-products of livestock farming
M.V. Kuznetsova1,2, D.O. Egorova1, D.A. Kochergina1, T.D. Kiryanova1, I.N. Zhdanova3, D.S. Fomin3, E.S. Gorovitz2
1Institute of Ecology and Genetics of Microorganisms of Ural Branch of Russian Academy of Sciences – affiliation of Perm Federal Research Centre of Ural Branch of RAS, 13 Goleva Str., Perm, 614081, Russian Federation
2Perm State Medical University named after Academician E.A. Wagner, 26 Petropavlovskaya Str., Perm, 614990, Russian Federation
3Perm Research Institute of Agriculture – branch of the Perm Federal Research Center of the Ural Branch of the Russian Academy of Sciences, 12 Kul’tury Str., Lobanovo village, Perm Krai, Russian Federation
Agro-industrial complexes are a major source of environmental pollution. Organic fertilizers based on by-products of livestock farming may contain pathogenic microorganisms, residual concentrations of antibiotics, vaccines, heavy metals, pesticides and, getting into the soil, cause their microbial and chemical pollution.
The aim of this study was to assess health risks based on analyzing microbial and chemical pollution due to by-products of livestock farming with different storage duration and conditions.
Our research objects were represented by samples of organic livestock wastes that differed per storage duration and conditions (non-composted and composted); they were taken at three large agro-industrial complexes in the Perm region. Strains of Escherichia coli were isolated from the wastes, in which the pathogenicity genes of diarrheagenic E. coli were detected. Concentrations of major pollutants posing health risks were determined in livestock farming by-products, including toxic substances (lead, cadmium, copper, manganese, magnesium, zinc, cobalt, iron), pesticides (gamma isomer of hexachlorocyclohexane – HCH, dichlorodiphenyltrichloroethane – DDT), and polychlorinated biphenyls (PCBs). Health risks were assessed.
Representatives of the Salmonella genus and opportunistic enterobacteria were shown to be able to survive in wastes for one month. In addition, levels of heavy metals in some samples were higher than the maximum allowable concentration (MAC) for soils. The sanitary indicators of fertilizers (by-products with a one-year storage period) did not exceed the safe standards; the samples did not contain diarrheagenic E. coli strains, organochlorine pesticides or polychlorinated biphenyls. The indicators characterizing the risk of prevalence of multiple antibiotic resistance and hazard indices of heavy metals were within permissible limits. By-products of livestock farming with a one-year storage period are safe in microbial and chemical terms and can be further used as a fertilizer.
- Milkereit J., Geisseler D., Lazicki P., Settles M.L., Durbin-Johnson B.P., Hodson A. Interactions between nitrogen availability, bacterial communities, and nematode indicators of soil food web function in response to organic amendments. Appl. Soil Ecol., 2021, vol. 157, no. 7, pp. 103767. DOI: 10.1016/j.apsoil.2020.103767
- Francioli D., Schulz E., Lentendu G., Wubet T., Buscot, F., Reitz T. Mineral vs. organic amendments: microbial community structure, activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies. Front. Microbiol., 2016, vol. 7, pp. 1446. DOI: 10.3389/fmicb.2016.01446
- Goss M.J., Tubeileh A., Goorahoo D. A review of the use of organic amendments and the risk to human health. Advances in Agronomy, 2013, vol. 120, pp. 275–379. DOI: 10.1016/B978-0-12-407686-0.00005-1
- Onishchenko G.G., Zaitseva N.V., Popova A.Yu., May I.V., Ustinova O.Yu., Trusov P.V., Hao L.T.H., Kleyn S.V. [et al.]. Analiz riska zdorov'yu v strategii gosudarstvennogo sotsial'no-ekonomicheskogo razvitiya [Health Risk Analysis in the Strategy of State Socio-Economic Development]: in 2 vol., 2nd ed., revised and enlarged. In: G.G. Onishchenko, N.V. Zaitseva eds. Moscow; Perm, PNRPU Publ., 2024 (in Russian).
- Van Boeckel T.P., Pires J., Silvester R., Zhao C., Song J., Criscuolo N.G., Gilbert M., Bonhoeffer S., Laxminarayan R. Global Trends in Antimicrobial Resistance in Animals in Low- and Middle-Income Countries. Science, 2019, vol. 365, no. 6459, pp. eaaw1944. DOI: 10.1126/science.aaw1944
- Ardakani Z., Canali M., Aragrande M., Tomassone L., Simoes M., Balzani A., Beber C.L. Evaluating the contribution of antimicrobial use in farmed animals to global antimicrobial resistance in humans. One Health, 2023, vol. 17, pp. 100647. DOI: 10.1016/j.onehlt.2023.100647
- Salam A., Al-Amin Y., Salam M.T., Pawar J.S., Akhter N., Rabaan A.A., Alqumber M.A.A. Anti¬microbial Resistance: A Growing Serious Threat for Global Public Health. Healthcare (Basel), 2023, vol. 11, no. 13, pp. 1946. DOI: 10.3390/healthcare11131946
- Heredia N., García S. Animals as sources of food-borne pathogens: A review. Anim. Nutr., 2018, vol. 4, no. 3, pp. 250–255. DOI: 10.1016/j.aninu.2018.04.006
- Bentum K.E., Kuufire E., Nyarku R., Osei V., Price S., Bourassa D., Temesgen S., Jackson C.R., Woubit A. Salmonellosis in Cattle: Sources and Risk of Infection, Control, and Prevention. Zoonotic Dis., 2025, vol. 5, no. 1, pp. 4. DOI: 10.3390/zoonoticdis5010004
- Litt P.K., Omar A.N., Gartley S., Kelly A., Ramos T., Nyarko E., de Souza T.R., Jay-Russell M. [et al.]. Prevalence of Shiga-Toxigenic Escherichia coli in Bovine Manure in the Mid-Atlantic Region of the United States. Microorganisms, 2025, vol. 13, no. 2, pp. 419. DOI: 10.3390/microorganisms13020419
- Rashid A., Schutte B.J., Ulery A., Deyholos M.K., Sanogo S., Lehnhoff E.A., Beck L. Heavy Metal Contamination in Agricultural Soil: Environmental Pollutants Affecting Crop Health. Agronomy, 2023, vol. 13, no. 6, pp. 1521. DOI: 10.3390/agronomy13061521
- Ke X., Gui S., Huang H., Zhang H., Wang C., Guo W. Ecological risk assessment and source identification for heavy metals in surface sediment from the Liaohe River protected area, China. Chemosphere, 2017, vol. 175, pp. 473–481. DOI: 10.1016/j.chemosphere.2017.02.029
- More S., Dhakate R. Geogenic and anthropogenic sources of heavy metals in soil: An ecological and health risk assessment in the granitic terrain of South India. Catena, 2025, vol. 254, pp. 108960. DOI: 10.1016/j.catena.2025.108960
- Hao X., Liu K., Zhu L., Rong L., Jiang D., Bai L. Migration and risk assessment of heavy metals from swine manure in an organic fertilizer – soil – ryegrass – rex rabbit system: Based on field trials. Sci. Total Environ., 2025, vol. 959, pp. 178332. DOI: 10.1016/j.scitotenv.2024.178332
- Wei M., Pan A., Ma R., Wang H. Migration characteristics and human health risk assessment of selenium and heavy metals in rhizosphere soil-crop system in high geological background area of southern Qinling Mountains: A case study of Shiquan County, Shaanxi, China. Ecotoxicol. Environ. Saf., 2025, vol. 294, pp. 118013. DOI: 10.1016/j.ecoenv.2025.118013
- Ejaz U., Khan S.M., Shah S.F.A., Khalid N., Jehangir S., Rizvi Z.F., Svenning J.-C. Integrative data-driven analytics for assessing ecological and human health risks of soil heavy metal contamination. Journal of Hazardous Materials Advances, 2025, vol. 17, pp. 100596. DOI: 10.1016/j.hazadv.2025.100596
- Wang X., Li X., Yan X., Tu C., Yu Z. Environmental risks for application of iron and steel slags in soils in China: A review. Pedosphere, 2021, vol. 31, no. 1, pp. 28–42. DOI: 10.1016/S1002-0160(20)60058-3
- Zhang L., Xue W., Sun H., Sun Q., Hu Y., Wu R., Du Y., Liu S., Zou G. Heavy metal(loid)s accumulation and human health risk assessment in wheat after long-term application of various urban and rural organic fertilizers. Sci. Total Environ., 2025, vol. 961, pp. 178389. DOI: 10.1016/j.scitotenv.2025.178389
- Wu S., Li K., Diao T., Sun Y., Sun T., Wang C. Influence of continuous fertilization on heavy metals accumulation and microorganism communities in greenhouse soils under 22 years of long-term manure organic fertilizer experiment. Sci. Total Environ., 2025, vol. 959, pp. 178294. DOI: 10.1016/j.scitotenv.2024.178294
- Ma Y., Yun X., Ruan Z., Lu C., Shi Y., Qin Q., Men Z., Zou D. [et al.]. Review of hexachlorocyclohexane (HCH) and dichlorodiphenyltrichloroethane (DDT) contamination in Chinese soils. Sci. Total Environ., 2020, vol. 749, pp. 141212. DOI: 10.1016/j.scitotenv.2020.141212
- Seo S.-H., Xia T., Islam M.K., Batterman S. Polychlorinated naphthalenes (PCNs) and polychlorinated biphenyls (PCBs) in surface soils and street dusts in Detroit, Michigan. Sci. Total Environ., 2025, vol. 964, pp. 178582. DOI: 10.1016/j.scitotenv.2025.178582
- Fang S., Cui Q., Dai X. Understanding urbanization development process and the associated PCBs concentration in urban soils – A genetic algorithm-based urbanization index approach. J. Hazard. Mater., 2025, vol. 489, pp. 137725. DOI: 10.1016/j.jhazmat.2025.137725
- Lacomba I., Palomares-Bolaños J., Juan-García A., López A., Olivero-Verbel J., Caballero-Gallardo K., Coscollà C., Juan C. Levels and risk assessment of dl-PCBs and dioxins in soils surrounded by cement plants from industrial areas of Colombia and Spain. Emerging Contaminants, 2025, vol. 11, no. 1, pp. 100427. DOI: 10.1016/j.emcon.2024.100427
- Shen H., Starr J., Han J., Zhang L., Lu D., Guan R., Xu X., Wang X. [et al.]. The bioaccessibility of polychlorinated biphenyls (PCBs) and polychlorinated dibenzo-p-dioxins/furans (PCDD/Fs) in cooked plant and animal origin foods. Environ. Int., 2016, vol. 94, pp. 33–42. DOI: 10.1016/j.envint.2016.05.003
- Lallas P.L. The Stockholm Convention on Persistent Organic Pollutants. American Journal of International Law, 2001, vol. 95, no. 3, pp. 692–708. DOI: 10.2307/2668517
- Warenik-Bany M., Strucinski P., Piskorska-Pliszczynska J. Dioxins and PCBs in game animals: Interspecies comparison and related consumer exposure. Environ. Int., 2016, vol. 89–90, pp. 21–29. DOI: 10.1016/j.envint.2016.01.007
- Pietron W.J., Warenik-Bany M. Terrestrial animal livers as a source of PCDD/Fs, PCBs and PBDEs in the diet. Sci. Total Environ., 2023, vol. 867, pp. 161508. DOI: 10.1016/j.scitotenv.2023.161508
- Trukhin A.M., Boyarova M.D. Organochlorine pesticides (HCH and DDT) in blubber of spotted seals (Phoca largha) from the western Sea of Japan. Mar. Pollut. Bull., 2020, vol. 150, pp. 110738. DOI: 10.1016/j.marpolbul.2019.110738
- Heijnen L., Medema G. Quantitative detection of E. coli, E. coli O157 and other Shiga toxin producing E. coli in water samples using a culture method combined with real-time PCR. J. Water Health, 2006, vol. 4, no. 4, pp. 487–498. DOI: 10.2166/wh.2006.0032
- Christopher A.F., Hora S., Ali Z. Investigation of plasmid profile antibiotic susceptibility pattern multiple antibiotic resistance index calculation of Escherichia coli isolates obtained from different human clinical specimens at tertiary care hospital in Bareilly‐India. ATMPH, 2013, vol. 6, pp. 285–289. DOI: 10.4103/1755-6783.120985
- Chapman T.A., Wu X.-Y., Barchia I., Bettelheim K.A., Driesen S., Trott D., Wilson M., Chin J.J.-C. Comparison of virulence gene profiles of Escherichia coli strains isolated from healthy and diarheic swine. Appl. Environ. Microbiol., 2006, vol. 72, no. 7, pp. 4782–4795. DOI: 10.1128/AEM.02885-05
- Caine L.-A., Nwodo U.U., Okoh A.I., Ndip R.N., Green E. Occurrence of virulence genes associated with diarrheagenic Escherichia coli isolated from raw cow's milk from two commercial dairy farms in the Eastern Cape Province, South Africa. Int. J. Environ. Res. Public Health, 2014, vol. 11, no. 11, pp. 11950–11963. DOI: 10.3390/ijerph111111950
- Gorbunova T.I., Egorova D.O., Pervova M.G., Kyrianova T.D., Demakov V.A., Saloutin V.I., Chupakhin O.N. Biodegradation of trichlorobiphenyls and their hydroxylated derivatives by Rhodococcus-strains. J. Hazard. Mater., 2021, vol. 409, pp. 124471. DOI: 10.1016/j.jhazmat.2020.124471
- Egorova D.O., Buzmakov S.A., Nazarova E.A., Andreev D.N., Demakov V.A., Plotnikova E.G. Bioremediation of hexachlorocyclohexane-contaminated soil by the new Rhodococcus wratislaviensis strain Ch628. Water Air Soil Pollut., 2017, vol. 228, pp. 183–199. DOI: 10.1007/s11270-017-3344-2
- Tyurin V.G., Biryukov K.N., Mysova G.A., Potemkina N.N., Kochish O.I., Sakharov A.Yu., Kovalenko P.S. Comparative assessment of organic fertilizers based on animal by-products using various methods of their processing. Problemy veterinarnoi sanitarii, gigieny i ekologii, 2025, no. 1 (53), pp. 117–124. DOI: 10.36871/vet.san.hyg.ecol.202501015 (in Russian).
- Mthembu T.P., Zishiri O.T., El Zowalaty M.E. Molecular detection of multidrug-resistant Salmonella isolated from livestock production systems in South Africa. Infect. Drug Re-sist., 2019, vol. 12, pp. 3537–3548. DOI: 10.2147/IDR.S211618
- Vogeleer P., Tremblay Y.D., Mafu A.A., Jacques M., Harel J. Life on the outside: Role of biofilms in environmental persistence of Shiga-toxin producing Escherichia coli. Front. Microbiol., 2014, vol. 5, pp. 317. DOI: 10.3389/fmicb.2014.00317
- Makarova M.A. A modern view of diarrheagenic Escherichia coli – a causative agent of acute intestinal infections. Journal of Microbiology, Epidemiology and Immunobiology, 2023, vol. 100, no. 4, pp. 333–344. DOI: 10.36233/0372-9311-410
- Zaitseva N.V., Onishchenko G.G., May I.V., Shur P.Z. Development of methodology for health risk assessment within the public administration of population sanitary and epidemiological welfare. Health Risk Analysis, 2022, no. 3, pp. 4–20. DOI: 10.21668/health.risk/2022.3.01.eng

fcrisk.ru

