Skip to main content

Advertisement

Log in

Steroidal Estrogens During Composting of Animal Manure: Persistence, Degradation, and Fate, a Review

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Different studies have shown that livestock manure has a high potential for fertilization in plant growth and crop yield. However, the main challenge of using animal manure as fertilizer is to increase the risk of endocrine-disrupting compounds (EDCs) pollution in soil and water. Because of their adverse effects, these compounds have gained more concern. Farmland applied with manure is considered the primary source of estrogens in the environment. To manage the pollution of EDCs, manure management approaches such as aerobic composting should be utilized to degrade and remove these pollutants. Composting has attracted attention because of its rapid reaction scale and strong degradation ability against the steroidal compounds. However, estrogen removal via traditional composting needs to be improved, as the steroidal compounds that remained in the composted manure could be quickly discharged to the environment because their biodegradation rate is lower than their discharge rate. For that reason, more advanced approaches, such as inoculation with microorganisms, should be involved. Also, applying adsorbent materials such as biochar (BC) and humic acid (HA) should be considered. In the light of the modern studies, affording an overall vision and perspectives about the fate of estrogens during composting is highly valuable. This review was designed to explore the sources, properties, occurrence, half-life, degradation, and transformation of estrogens during animal manure composting. Besides, the efficiency of estrogens degrading microorganisms and adsorbent additives was also reviewed. The eventual remarks were mentioned, and their prospects were discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdellah, Y. A., & Li, C. (2020). Livestock manure composting in cold regions: challenges and solutions. Agriculture (Pol'nohospodárstvo), 66(1), 1–14.

    Google Scholar 

  • Adeel, M., Song, X., Wang, Y., Francis, D., & Yang, Y. (2017). Environmental impact of estrogens on human, animal, and plant life: a critical review. Environment International, 99, 107–119.

    CAS  Google Scholar 

  • Akdeniz, N. (2019). A systematic review of biochar use in animal waste composting. Waste Management, 88, 291–300.

    CAS  Google Scholar 

  • Alizadeh, S., Prasher, S. O., Elsayed, E., Qi, Z., & Patel, & R. M. (2018). Effect of biochar on fate and transport of manure-borne estrogens in sandy soil. Journal of Environmental Sciences, 73, 162–176.

    Google Scholar 

  • An, X., Cheng, Y., Miao, L., Chen, X., Zang, H., & Li, C. (2020). Characterization and genome functional analysis of an efficient nitrile-degrading bacterium, Rhodococcus rhodochrous BX2, to lay the foundation for potential bioaugmentation for remediation of nitrile-contaminated environments. Journal of Hazardous Materials, 389, 121906.

    CAS  Google Scholar 

  • Andaluri, G., Suri, R. P. S., & Kumar, K. (2011). Occurrence of estrogen hormones in biosolids, animal manure, and mushroom compost. Environmental Monitoring & Assessment, 2, 1197–1205.

    Google Scholar 

  • Andersen, H. R., Hansen, M., Kjølholt, J., Stuer-Lauridsen, F., Ternes, T., & Halling-Sørensen, B. (2005). Assessment of the importance of sorption for steroid estrogens removal during activated sludge treatment. Chemosphere, 61, 139–146.

    CAS  Google Scholar 

  • Atkinson, C. F., Jones, D. D., & Gauthier, J. J. (1996). Putative anaerobic activity in aerated composts. Journal of Industrial Microbiology & Biotechnology, 3, 182–188.

    Google Scholar 

  • Auriol, M., Filali-Meknassi, Y., Adams, C. D., Tyagi, R. D., Noguerol, T.-N., & Piña, B. (2008). Removal of estrogenic activity of natural and synthetic hormones from municipal wastewater: efficiency of horseradish peroxidase and laccase from Trametes Versicolor. Chemosphere, 3, 445–452.

    Google Scholar 

  • Barnabe, S., Brar, S., Tyagi, R., Beauchesne, I., & Surampalli, R. (2009). Pre-treatment and bioconversion of wastewater sludge to value-added products, fate of endocrine-disrupting compounds. Science of the Total Environment, 5, 1471–1488.

  • Bartelt-Hunt, S. L., Snow, D. D., Kranz, W. L., Mader, T. L., Shapiro, C. A., Donk, S. J. V., & Zhang, T. C. (2012). Effect of growth Promotants on the occurrence of endogenous and synthetic steroid hormones on feedlot soils and in runoff from beef cattle feeding operations. Environmental Science & Technology, 3, 1352–1360.

    Google Scholar 

  • Bartelt-Hunt, S. L., DeVivo, S., Johnson, L., Snow, D. D., Kranz, W. L., Mader, T. L., & Zhang, T. C. (2013). Effect of composting on the fate of steroids in beef cattle manure. Journal of Environmental Quality, 42, 1159.

    CAS  Google Scholar 

  • Bedard, M., Giffear, K. A., Ponton, L., Sienerth, K. D., & Moore, V. D. G. (2014). Characterization of binding between 17β-estradiol and estriol with humic acid via NMR and biochemical analysis. Biophysical Chemistry, 189, 1–7.

    CAS  Google Scholar 

  • Bernet, N., & Béline, F. (2009). Challenges and innovations on biological treatment of livestock effluents. Bioresource Technology, 22, 5431–5436.

    Google Scholar 

  • Bhandari, R. K., Deem, S. L., Holliday, D. K., Jandegian, C. M., Kassotis, C. D., & Nagel, &S. C., Rosenfeld, C. S. (2015). Effects of the environmental estrogenic contaminants bisphenol a and 17α-Ethinyl estradiol on sexual development and adult behaviors in aquatic wildlife species. General & Comparative Endocrinology, 214, 195–219.

    CAS  Google Scholar 

  • Bilal, M., & Iqbal, H. M. (2019). Persistence and impact of steroidal estrogens on the environment and their laccase-assisted removal. Science of the Total Environment, 690, 447–459.

    CAS  Google Scholar 

  • Biswas, S., Kranz, W. L., Shapiro, C. A., Snow, D. D., Bartelt-Hunt, S. L., Mamo, M., & Tarkalson, D. D. (2017). Effect of rainfall timing and tillage on the transport of steroid hormones in runoff from manure amended row crop fields. Journal of Hazardous Materials, 324, 436–447.

    CAS  Google Scholar 

  • Blunt, S. M., Benotti, M. J., Rosen, M. R., Hedlund, B. P., & Moser, D. P. (2017). Reversible reduction of estrone to 17β-estradiol by Rhizobium, Sphingopyxis, and Pseudomonas isolates from the Las Vegas wash. Journal of Environmental Quality, 2, 281–287.

    Google Scholar 

  • Brion, F., Tyler, C., Palazzi, X., Laillet, B., Porcher, J., Garric, J., & Flammarion, P. (2004). Impacts of 17β-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult life stages in zebrafish (Danio rerio). Aquatic Toxicology, 3, 193–217.

    Google Scholar 

  • Burkhardt-Holm, P. (2010). Endocrine disruptors and water quality: a state-of-the-art review. International Journal of Water Resources Development, 3, 477–493.

    Google Scholar 

  • Cajthaml, T., Křesinová, Z., Svobodová, K., Sigler, K., & Řezanka, T. (2009). Microbial transformation of synthetic estrogen 17α-ethinylestradiol. Environmental Pollution, 12, 3325–3335.

    Google Scholar 

  • Caliman, F. A., & Gavrilescu, M. (2009). Pharmaceuticals, personal care products and endocrine disrupting agents in the environment - a review. Clean-Soil Air Water, 5, 277–303.

    Google Scholar 

  • Card, M. L., Schnoor, J. L., & Chin, Y. (2012). Uptake of natural and synthetic estrogens by maize seedlings. Journal of Agricultural & Food Chemistry, 60(34), 8264–8271.

    CAS  Google Scholar 

  • Casey, F. X. M., Larsen, G. L., Hakk, H., & Simunek, J. (2003). Fate and transport of 17β-estradiol in soil-water systems. Environmental Science & Technology, 37, 2400–2409.

    CAS  Google Scholar 

  • Casey, F. X., Hakk, H., & Desutter, T. M. (2020). Free and conjugated estrogens detections in drainage tiles and wells beneath fields receiving swine manure slurry. Environmental Pollution, 256, 113384.

    CAS  Google Scholar 

  • Chen, M., Waigi, M. G., Li, S., Sun, K., & Si, Y. (2019). Fungal laccase-mediated humification of estrogens in aquatic ecosystems. Water Research, 166, 115040.

    CAS  Google Scholar 

  • Colucci, M. S., Bork, H., & Topp, E. (2001). Persistence of estrogenic hormones in agriculture: I. 17β-estradiol and estrone. Journal of Environmental Quality, 30, 2070–2076.

    CAS  Google Scholar 

  • Combalbert, S., & Hernandez-Raquet, G. (2010). Occurrence, fate, and biodegradation of estrogens in sewage and manure. Journal of Industrial Microbiology & Biotechnology, 86, 1671–1692.

    CAS  Google Scholar 

  • Combalbert, S., Bellet, V., Dabert, P., Bernet, N., Balaguer, P., & Hernandez-Raquet, G. (2012). Fate of steroid hormones and endocrine activities in swine manure disposal and treatment facilities. Water Research, 3, 895–906.

    Google Scholar 

  • Cromwell, G. L., Stahly, T. S., Coffey, R. D., Monegue, H. J., & Randolph, J. H. (1993). Efficacy of phytase in improving the bioavailability of phosphorus in soybean meal and corn-soybean meal diets for pigs. Journal of Animal Science, 7, 1831–1840.

    Google Scholar 

  • Derby, N. E., Hakk, H., Casey, F. X., & Desutter, T. M. (2011). Effects of composting swine manure on nutrients and estrogens. Soil Science, 2, 91–98.

    Google Scholar 

  • Ermawati, R., Morimura, S., Tang, Y., Liu, K., & Kida, K. (2007). Degradation and behavior of natural steroid hormones in cow manure waste during biological treatments and ozone oxidation. Journal of Bioscience and Bioengineering, 1, 27–31.

    Google Scholar 

  • Fahrbach, M. (2006). Denitratisoma oestradiolicum gen. Nov., sp. nov., a 17β-estradiol-degrading, denitrifying beta proteobacterium. International Journal of Systematic & Evolutionary Microbiology, 7, 1547–1552.

    Google Scholar 

  • Fahrbach, M., Kuever, J., Remesch, M., Huber, B. E., Kampfer, P., Dott, W., & Hollender, J. (2008). Steroidobacter denitrificans gen. Nov., sp. nov., a steroidal hormone-degrading gammaproteobacterium. International Journal of Systematic & Evolutionary Microbiology, 9, 2215–2223.

    Google Scholar 

  • Fels, L. E., Ouaqoudi, F.-Z. E., Lemee, L., Geffroy, C., Ambles, A., & Hafidi, M. (2016). Occurrence of plant and fecal steroids and their evolution during co-composting of sewage sludge and lignocellulosic waste. Biochemical Engineering, 105, 497–504.

    Google Scholar 

  • Fine, D. D., Breidenbach, G., Price, T. L., & Hutchins, S. R. (2003). Quantitation of estrogens in groundwater and swine lagoon samples using solid-phase extraction, pentafluorobenzyl/trimethylsilyl derivatizations and gas chromatography–negative ion chemical ionization tandem mass spectrometry. Journal of Chromatography A, 1017, 167–185.

    CAS  Google Scholar 

  • Fujii, K., Kikuchi, S., Satomi, M., Ushio-Sata, N., & Morita, N. (2002). Degradation of 17β -estradiol by a gram-negative bacterium isolated from activated sludge in a sewage treatment Plant in Tokyo, Japan. Applied & Environmental Microbiology, 68, 2057–2060.

    CAS  Google Scholar 

  • G. Füleky, & S. Benedek. (2010). Composting to recycle biowaste E. Lichtfouse (Ed.), sociology, organic farming, climate change, and soil science, springer, Netherlands.

  • Gadd, J. B., Tremblay, L. A., & Northcott, G. L. (2010). Steroid estrogens, conjugated estrogens and estrogenic activity in farm dairy shed effluents. Environmental Pollution, 3, 730–736.

    Google Scholar 

  • Gao, X., Tan, W., Zhao, Y., Wu, J., Sun, Q., Qi, H., & Wei, Z. (2019). Diversity in the mechanisms of Humin formation during composting with different materials. Environmental Science & Technology, 53, 3653–3662.

    CAS  Google Scholar 

  • Ghirardini, A., Grillini, V., & Verlicchi, P. (2020). A review of the occurrence of selected micropollutants and microorganisms in different raw and treated manure – Environmental risk due to antibiotics after application to soil. Science of the Total Environment, 707, 136118.

    CAS  Google Scholar 

  • Goeppert, N., Dror, I., & Berkowitz, B. (2015). Fate and transport of free and conjugated estrogens during soil passage. Environmental Pollution, 206, 80–87.

    CAS  Google Scholar 

  • Guardian, M. G. E., & Aga, D. S. (2019). Mineralization and biotransformation of estrone in simulated poultry litter and cow manure runoff water. Journal of Environmental Quality, 48(4), 1120.

    CAS  Google Scholar 

  • Guo, X.-X., Liu, H.-T., & Zhang, J. (2020). The role of biochar in organic waste composting and soil improvement: a review. Waste Management, 102, 884–899.

    CAS  Google Scholar 

  • Hakk, H., & Sikora, L. (2011). Dissipation of 17β-estradiol in composted poultry litter. Journal of Environmental Quality, 40, 1560–1566.

    CAS  Google Scholar 

  • Hakk, H., Millner, P., & Larsen, G. (2005). Decrease in water-soluble 17β-estradiol and testosterone in composted poultry manure with time. Journal of Environmental Quality, 34(3), 943.

    CAS  Google Scholar 

  • Hamid, H., & Eskicioglu, C. (2012). Fate of estrogenic hormones in wastewater and sludge treatment: a review of properties and analytical detection techniques in the sludge matrix. Water Research, 18, 5813–5833.

    Google Scholar 

  • Hanselman, T. A., Graetz, D. A., & Wilkie, A. C. (2003). Manure-borne estrogens as potential environmental contaminants: a review. Environmental Science & Technology, 24, 5471–5478.

    Google Scholar 

  • Ho, Y. B., Zakaria, M. P., Latif, P. A., & Saari, N. (2013). Degradation of veterinary antibiotics and hormones during broiler manure composting. Bioresource Technology, 131, 476–484.

    CAS  Google Scholar 

  • Hou, N., Wen, L., Cao, H., Liu, K., An, X., Li, D., & Li, C. (2017). Role of psychrotrophic bacteria in organic domestic waste composting in cold regions of China. Bioresource Technology, 236, 20–28.

    CAS  Google Scholar 

  • Hu, Y., Cheng, H., & Tao, S. (2017). Environmental and human health challenges of industrial livestock and poultry farming in China and their mitigation. Environment International, 107, 111–130.

    CAS  Google Scholar 

  • Huang, B., Lai, C., Dai, H., Mu, K., Xu, Z., Gu, L., & Pan, X. (2019). Microbially reduced humic acid promotes the anaerobic photodegradation of 17α-ethinylestradiol. Ecotoxicology & Environmental Safety, 171, 313–320.

    CAS  Google Scholar 

  • Ivanov, V., Lim, J. J.-W., Stabnikova, O., Gin, K., & Y.-H. (2010). Biodegradation of estrogens by facultative anaerobic iron-reducing bacteria. Process Biochemistry, 2, 284–287.

    Google Scholar 

  • Jiang, C., Cheng, Y., Zang, H., Chen, X., Wang, Y., & Zhang, & Y., Li, C. (2019). Biodegradation of lignin and the associated degradation pathway by psychrotrophic Arthrobacter sp. C2 from the cold region of China. Cellulose, 27(3), 1423–1440.

    Google Scholar 

  • Johnson, A., Williams, R., & Matthiessen, P. (2006). The potential steroid hormone contribution of farm animals to freshwaters, the United Kingdom as a case study. Science of the Total Environment, 362, 166–178.

    CAS  Google Scholar 

  • Jung, C., Park, J., Lim, K. H., Park, S., Heo, J., Her, N., & Yoon, Y. (2013). Adsorption of selected endocrine disrupting compounds and pharmaceuticals on activated biochars. Journal of Hazardous Materials, 263, 702–710.

    CAS  Google Scholar 

  • Ke, J., Zhuang, W., Gin, K. Y.-H., Reinhard, M., Hoon, L. T., & Tay, J.-H. (2007). Characterization of estrogen-degrading bacteria isolated from an artificial sandy aquifer with ultrafiltered secondary effluent as the medium. Applied Microbiology & Biotechnology, 7, 1163–1171.

    Google Scholar 

  • Kidd, K. A., Blanchfield, P. J., Mills, K. H., Palace, V. P., Evans, R. E., Lazorchak, J. M., & Flick, R. W. (2007). Collapse of a fish population after exposure to synthetic estrogen. PNAS, 21, 8897–8901.

    Google Scholar 

  • Kurisu, F., Ogura, M., Saitoh, S., Yamazoe, A., & Yagi, O. (2010). Degradation of natural estrogen and identification of the metabolites produced by soil isolates of Rhodococcus sp. and Sphingomonas sp. Journal of Bioscience and Bioengineering, 109, 576–582.

    CAS  Google Scholar 

  • Lange, I. G., Daxenberger, A., Schiffer, B., Witters, H., Ibarreta, D., & Meyer, H. H. (2002). Sex hormones originating from different livestock production systems: fate and potential disrupting activity in the environment. Analytica Chimica Acta, 473, 27–37.

    CAS  Google Scholar 

  • Larsson, D., Adolfsson-Erici, M., Parkkonen, J., Pettersson, M., Berg, A., Olsson, P.-E., & Förlin, L. (1999). Ethinyloestradiol - an undesired fish contraceptive? Aquatic Toxicology, 45, 91–97.

    CAS  Google Scholar 

  • Lee, J. H., Zhou, J. L., & Kim, S. D. (2011). Effects of biodegradation and sorption by humic acid on the estrogenicity of 17β-estradiol. Chemosphere, 85, 1383–1389.

    CAS  Google Scholar 

  • Lei, B., Huang, S., Zhou, Y., Wang, D., & Wang, Z. (2009). Levels of six estrogens in water and sediment from three rivers in Tianjin area, China. Chemosphere, 76, 36–42.

    CAS  Google Scholar 

  • Lei, B., Kang, J., Yu, Y., Zha, J., Li, W., & Wang, Z. (2013). β-Estradiol 17-valerate affects embryonic development and sexual differentiation in Japanese medaka (Oryzias latipes). Aquatic Toxicology, 134-135, 128–134.

    CAS  Google Scholar 

  • Li, S., Liu, J., Sun, M., Ling, W., & Zhu, X. (2017). Isolation, characterization, and degradation performance of the 17β-estradiol-degrading bacterium Novosphingobium sp. E2S. Int J Environ Res Public Health, 14(2), 115.

    Google Scholar 

  • Li, C., Li, H., Yao, T., Su, M., Ran, F., Han, B., & Gun, S. (2019). Microbial inoculation influences bacterial community succession and physicochemical characteristics during pig manure composting with corn straw. Bioresource Technology, 289, 121653.

    CAS  Google Scholar 

  • Li, C., Chen, X., Wen, L., Cheng, Y., An, X., Li, T., & Hou, N. (2020). An enhancement strategy for the biodegradation of high-concentration aliphatic nitriles: utilizing the glucose-mediated carbon catabolite repression mechanism. Environmental Pollution, 265, 114302.

    CAS  Google Scholar 

  • Liu, Z.-H., Kanjo, Y., & Mizutani, S. (2009). Removal mechanisms for endocrine disrupting compounds (EDCs) in wastewater treatment - physical means, biodegradation, and chemical advanced oxidation: a review. Science of the Total Environment, 407, 731–748.

    CAS  Google Scholar 

  • Liu, J., Liu, J., Xu, D., Ling, W., Li, S., & Chen, M. (2016). Isolation, immobilization, and degradation performance of the 17β-estradiol-degrading bacterium Rhodococcus sp. JX-2. Water Air & Soil Pollution, 227(11), 422.

    Google Scholar 

  • Liu, N., Liu, Y., Zeng, G., Gong, J., Tan, X., Junwen, & Yin, Z. (2020). Adsorption of 17β-estradiol from aqueous solution by raw and direct/pre/post-KOH treated lotus seedpod biochar. International Journal of Environmental Science & Technology, 87, 10–23.

    Google Scholar 

  • Muller, M., Combalbert, S., Delgenès, N., Bergheaud, V., Rocher, V., Benoît, P., & Hernandez-Raquet, G. (2010). Occurrence of estrogens in sewage sludge and their fate during plant-scale anaerobic digestion. Chemosphere, 81, 65–71.

    CAS  Google Scholar 

  • Noguera-Oviedo, K., & Aga, D. S. (2016). Chemical and biological assessment of endocrine-disrupting chemicals in a full-scale dairy manure anaerobic digester with thermal pretreatment. Science of the Total Environment, 550, 827–834.

    CAS  Google Scholar 

  • Olsen, P., Bach, K., Barlebo, H. C., Ingerslev, F., Hansen, M., & Sørensen, B. H. (2007). Leaching of estrogenic hormones from manure-treated structured soils. Environmental Science & Technology, 41, 3911–3917.

    Google Scholar 

  • Pan, J., Li, R., Zhai, L., Zhang, Z., Ma, J., & Liu, H. (2019). Influence of palygorskite addition on biosolids composting process enhancement. Journal of Cleaner Production, 217, 371–379.

    CAS  Google Scholar 

  • Pauwels, B., Wille, K., Noppe, H., Brabander, H. D., Wiele, T. V. D., Verstraete, W., & Boon, N. (2008). 17α-ethinylestradiol cometabolism by bacteria degrading estrone, 17β-estradiol, and estriol. Biodegradation, 19, 683–693.

    CAS  Google Scholar 

  • Peng, X., Yu, Y., Tang, C., Tan, J., Huang, Q., & Wang, Z. (2008). Occurrence of steroid estrogens, endocrine-disrupting phenols, and acid pharmaceutical residues in urban riverine water of the Pearl River Delta, South China. Science of the Total Environment, 397, 158–166.

    CAS  Google Scholar 

  • Pollard, A. T., & Morra, M. J. (2017). Estrogens: properties, behaviors, and fate in dairy manure-amended soils. Environmental Technology, 25, 452–462.

    CAS  Google Scholar 

  • Prater, J. R., Horton, R., & Thompson, M. L. (2015). Reduction of estrone to 17 β-estradiol in the presence of swine manure colloids. Chemosphere, 119, 642–645.

    CAS  Google Scholar 

  • Prost, K., Bradel, P. L., Lehndorff, E., & Amelung, W. (2018). Steroid dissipation and formation in the course of farmyard manure composting. Organic Geochemistry, 118, 47–57.

    CAS  Google Scholar 

  • Rahmani, K., Faramarzi, M. A., Mahvi, A. H., Gholami, M., Esrafili, A., Forootanfar, H., & Farzadkia, M. (2015). Elimination and detoxification of sulfathiazole and sulfamethoxazole assisted by laccase immobilized on porous silica beads. International Biodeterioration & Biodegradation, 97, 107–114.

    CAS  Google Scholar 

  • Raman, D. R., Williams, E. L., Layton, A. C., Burns, R. T., Easter, J. P., Daugherty, A. S., Mullen, M. D., & Sayler, G. S. (2004). Estrogen content of dairy and swine wastes. Environmental Science & Technology, 38, 3567–3573.

    CAS  Google Scholar 

  • Rastogi, M., Nandal, M., & Khosla, B. (2020). Microbes as vital additives for solid waste composting. Heliyon, 6(2).

  •  Ren, D., Huang, B., Yang, B., Chen, F., Pan, X., & Dionysiou, D. D. (2017). Photobleaching alters the photochemical and biological reactivity of humic acid towards 17α-ethynylestradiol. Environmental Pollution, 220, 1386–1393.

  • Ren, D., Ren, Z., Chen, F., Wang, B., & Huang, B. (2019). Predictive role of spectral slope ratio towards 17α-ethynylestradiol photodegradation sensitized by humic acids. Environmental Pollution, 112959.

  • Romantschuk, M., Sarand, I., Petänen, T., Peltola, R., Jonsson-Vihanne, M., Koivula, T., & Haahtela, K. (2000). Means to improve the effect of in situ bioremediation of contaminated soil: an overview of novel approaches. Environmental Pollution, 107, 179–185.

    CAS  Google Scholar 

  • Sánchez, Ó. J., Ospina, D. A., & Montoya, S. (2017). Compost supplementation with nutrients and microorganisms in composting process. Waste Management, 69, 136–153.

    Google Scholar 

  • Schwarz, M., & Bonhotal, J. (2016). The fate of Ivermectin in manure composting. Cornell waste management institute, 817 Bradfield hall, Ithaca, NY 14853. Cornell Waste Management Institute.

  • Schwarz, M., Bonhotal, J., Harrison, E., Brinton, W., & Storms, P. (2010). Effectiveness of composting road-killed deer in New York state. Compost Science & Utilization, 18, 232–241.

    Google Scholar 

  • Singh, A. (2015). Aerobic and anaerobic transformations in estrogens and nutrients in swine manure: environmental consequences. Agriculture, 5, 697–712.

    Google Scholar 

  • Song, H.-L., Nakano, K., Taniguchi, T., Nomura, M., & Nishimura, O. (2009). Estrogen removal from treated municipal effluent in small-scale constructed wetlands with different depths. Bioresource Technology, 100, 2945–2951.

    CAS  Google Scholar 

  • Stumpe, B., & Marschner, B. (2007). Long-term sewage sludge application and wastewater irrigation on the mineralization and sorption of 17β-estradiol and testosterone in soils. Science of the Total Environment, 374, 282–291.

    CAS  Google Scholar 

  • Sumpter, J. P., & Jobling, S. (1995). Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environmental Health Perspectives, 103, 173–178.

    CAS  Google Scholar 

  • Sun, K., Liang, S., Kang, F., Gao, Y., & Huang, Q. (2016). Transformation of 17 β-estradiol in humic acid solution by ε -MnO2 nanorods as probed by high-resolution mass spectrometry combined with 13 C labeling. Environmental Pollution, 214, 211–218.

    CAS  Google Scholar 

  • Sun, S., Zhang, Y., Liu, K., Chen, X., Jiang, C., Huang, M., & Li, C. (2019). Insight into biodegradation of cellulose by psychrotrophic bacterium Pseudomonas sp. LKR-1 from the cold region of China: optimization of cold-active cellulase production and the associated degradation pathways. Cellulose, 27(1), 315–333.

    Google Scholar 

  • Tompsett, A. R., Wiseman, S., Higley, E., Giesy, J. P., & Hecker, M. (2013). Effects of exposure to 17α-ethynylestradiol during larval development on growth, sexual differentiation, and abundances of transcripts in the liver of the wood frog (Lithobates sylvaticus). Aquatic Toxicology, 126, 42–51.

    CAS  Google Scholar 

  • Tong, X., Li, Y., Zhang, F., Chen, X., Zhao, Y., Hu, B., & Zhang, X. (2019). Adsorption of 17β-estradiol onto humic-mineral complexes and effects of temperature, pH, and bisphenol a on the adsorption process. Environmental Pollution, 254, 112924.

    CAS  Google Scholar 

  • Tyler, C. R., Jobling, S., & Sumpter, J. P. (1998). Endocrine disruption in wildlife: a critical review of the evidence. Critical Reviews in Toxicology, 28, 319–361.

    CAS  Google Scholar 

  • Wang, L., Ying, G.-G., Chen, F., Zhang, L.-J., Zhao, J.-L., Lai, H.-J., & Tao, R. (2012). Monitoring of selected estrogenic compounds and estrogenic activity in surface water and sediment of the Yellow River in China using combined chemical and biological tools. Environmental Pollution, 165, 241–249.

    CAS  Google Scholar 

  • Weber, S., Leuschner, P., Kämpfer, P., Dott, W., & Hollender, J. (2004). Degradation of estradiol and Ethinyl estradiol by activated sludge and by a defined mixed culture. Applied Microbiology and Biotechnology, 67, 106–112.

    Google Scholar 

  • Wei, Z., Wang, J. J., Hernandez, A. B., Warren, A., Park, J.-H., & Meng,& Y., Jeong, C. (2019). Effect of biochar amendment on sorption-desorption and dissipation of 17α-ethinylestradiol in sandy loam and clay soils. Science of the Total Environment, 686, 959–967.

    CAS  Google Scholar 

  • Wei, Y., Zhao, Y., Zhao, X., Gao, X., Zheng, Y., Zuo, H., & Wei, Z. (2020). Roles of different humin and heavy-metal resistant bacteria from composting on heavy metal removal. Bioresource Technology, 296, 122375.

    CAS  Google Scholar 

  • Writer, J. H., Ryan, J. N., Keefe, S. H., & Barber, L. B. (2011). Fate of 4-Nonylphenol and 17β-estradiol in the redwood river of Minnesota. Environmental Science & Technology, 46, 860–868.

    Google Scholar 

  • Xu, N., Zhang, B., Tan, G., Li, J., & Wang, H. (2015). Influence of biochar on sorption, leaching, and dissipation of bisphenol a and 17α-ethynylestradiol in soil. Environmental Science-Processes & Impacts, 17, 1722–1730.

    CAS  Google Scholar 

  • Xu, P., Zhou, X., Xu, D., Xiang, Y., Ling, W., & Chen, M. (2018). Contamination and risk assessment of estrogens in livestock manure: a case study in Jiangsu Province, China. International Journal of Environmental Research & Public Health, 15(1), 125.

    Google Scholar 

  • Yang, Y.-Y. (2010). Degradation and transport pathways of steroid hormones from human and animal waste (dissertation). Fort Collins, Colorado: Colorado State University.

    Google Scholar 

  • Yin, Z., Liu, Y., Tan, X., Jiang, L., Zeng, G., & Liu, & S., Li, M. (2019). Adsorption of 17β-estradiol by a novel attapulgite/biochar nanocomposite: characteristics and influencing factors. Process Safety and Environmental Protection, 121, 155–164.

    CAS  Google Scholar 

  • Ying, G.-G., Kookana, R. S., & Ru, Y.-J. (2002). Occurrence and fate of hormone steroids in the environment. Environment International, 28, 545–551.

    CAS  Google Scholar 

  • Yu, C.-P., Ahuja, R., Sayler, G., & Chu, K.-H. (2005). Quantitative molecular assay for fingerprinting microbial communities of wastewater and estrogen-degrading consortia. Applied and Environmental Microbiology, 71, 1433–1444.

    CAS  Google Scholar 

  • Yu, C.-P., Roh, H., & Chu, K.-H. (2007). 17β-estradiol-degrading bacteria isolated from activated sludge. Environmental Science & Technology, 41, 486–492.

    CAS  Google Scholar 

  • Yu, C.-P., Deeb, R. A., & Chu, K.-H. (2013). Microbial degradation of steroidal estrogens. Chemosphere, 91, 1225–1235.

    CAS  Google Scholar 

  • Yu, H., Jiang, J., Zhao, Q., Wang, K., Zhang, Y., Zheng, Z., & Hao, X. (2015). Bioelectrochemically-assisted anaerobic composting process enhancing compost maturity of dewatered sludge with synchronous electricity generation. Bioresource Technology, 193, 1–7.

    CAS  Google Scholar 

  • Yu, Q., Wang, P., Liu, D., Gao, R., Shao, H., Zhao, H., Ma, Z., Wang, D., & Huo, H. (2016). Degradation characteristics and metabolic pathway of 17β-estradiol (E2) by Rhodococcus sp. DS201. Biotechnology and Bioprocess Engineering, 21, 804–813.

    CAS  Google Scholar 

  • Zang, H., Wang, H., Miao, L., Cheng, Y., Zhang, Y., & Liu, &Y., Li, C. (2020). Carboxylesterase, a de-esterification enzyme, catalyzes the degradation of chlorimuron-ethyl in Rhodococcus erythropolis D310-1. Journal of Hazardous Materials, 387, 121684.

    CAS  Google Scholar 

  • Zhang, H., Shi, J., Liu, X., Zhan, X., & Chen, Q. (2014). Occurrence and removal of free estrogens, conjugated estrogens, and bisphenol a in manure treatment facilities in East China. Water Research, 58, 248–257.

    CAS  Google Scholar 

  • Zhang, J.-N., Yang, L., Zhang, M., Liu, Y.-S., Zhao, J.-L., He, L.-Y., & Ying, G.-G. (2019). Persistence of androgens, progestogens, and glucocorticoids during commercial animal manure composting process. Science of the Total Environment, 665, 91–99.

    CAS  Google Scholar 

  • Zhao, Y., Lu, Q., Wei, Y., Cui, H., Zhang, X., Wang, X., & Wei, Z. (2016). Effect of actinobacteria agent inoculation methods on cellulose degradation during composting based on redundancy analysis. Bioresource Technology, 219, 196–203.

    CAS  Google Scholar 

  • Zhao, X., Grimes, K. L., Colosi, L. M., & Lung, W.-S. (2019). Attenuation, transport, and management of estrogens: a review. Chemosphere, 230, 462–478.

    CAS  Google Scholar 

  • Zheng, W., Yates, S. R., & Bradford, S. A. (2008). Analysis of steroid hormones in a typical dairy waste disposal system. Environmental Science & Technology, 42, 530–535.

    CAS  Google Scholar 

Download references

Acknowledgments

The listed authors are grateful to the Natural Science Foundation of China, the Northeast Center branch of the National Engineering Laboratory for pollution control and Waste utilization in livestock and poultry production for providing literature facilities.

Funding

The work was supported by the National Natural Science Fund of China (Grant no. 41771559).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chunyan Li.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

Human and Animal Rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdellah, Y.A.Y., Zang, H. & Li, C. Steroidal Estrogens During Composting of Animal Manure: Persistence, Degradation, and Fate, a Review. Water Air Soil Pollut 231, 547 (2020). https://doi.org/10.1007/s11270-020-04904-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-020-04904-4

Keywords

Navigation