Effect of Biochar on 17β-Estradiol Degradation in Composted Poultry Manure: Residue and Bioassay Analysis

  • Rong Rong
  • Zhiming Li
  • Yusheng ZhengEmail author
  • Fengsong Zhang
Original Paper


While composting is normally a valid approach to decrease 17β-estradiol (E2) contents of manure prior to land application, E2 residues in compost pose a risk to the environment. Biochar is a useful material in composting due to its microstructure. The study aims to compare the effect of amending poultry manure (PM) with two different biochars at three levels on E2 degradation. The seven treatments consisted of compost with no biochar (control) and compost with 5%, 10%, or 15% wheat stalk biochar (WSB) or rice husk biochar (RHB). The results indicated composting with WSB and RHB reduced E2 extractable contents by 71.0–78.5% and 74.2–88.1%, versus 67.8% without biochar. The abundance of two bacteria capable of E2 degradation: Bacillus licheniformis and Bacillus subtilis, increased significantly (p < 0.05) over control in biochar-amended treatments. Moreover, the estrogenic activity (assessed by proliferative assay of MCF-7 cells) of the compost was diminished by the addition of biochar. Our results suggest that E2 degradation was accelerated by adding RHB, possibly by RHB’s provision of a better microenvironment due to larger surface area and pore volume than WSB. Thus, the addition of 15% RHB is recommended for the treatment of PM compost to enhance E2 degradation.

Graphic Abstract


Biochar 17β-Estradiol E2-degrading bacteria Composting Poultry manure 



This research was supported by the National Natural Science Foundation of China (41201513) and the Student’s Platform for Innovation and Entrepreneurship Training Program (201810589016). We are grateful to the anonymous referees and the editorial board for reviewing this paper.

Compliance with Ethical Standards

Conflicts of interest

There are no conflicts to declare.

Supplementary material

12649_2019_788_MOESM1_ESM.docx (16 kb)
Supplementary file1 (DOCX 15 kb)


  1. 1.
    Lange, I.G., Daxenberger, A., Schiffer, B., Witters, H., Ibarreta, D., Meyer, H.H.: Sex hormones originating from different livestock production systems: fate and potential disrupting activity in the environment. Anal. Chim. Acta 473(1), 27–37 (2002)CrossRefGoogle Scholar
  2. 2.
    Nazari, E., Suja, F.: Effects of 17β-estradiol (E2) on aqueous organisms and its treatment problem: a review. Rev. Environ. Health 31(4), 465–491 (2016)CrossRefGoogle Scholar
  3. 3.
    Orozco-Hernandez, L., Gutierrez-Gomez, A.A., Sanjuan-Reyes, N., Islas-Flores, H., Garcia-Medina, S., Galar-Martinez, M., Dublan-Garcia, O., Natividad, R., Gomez-Olivan, L.M.: 17β-Estradiol induces cyto-genotoxicity on blood cells of common carp (Cyprinus carpio). Chemosphere 191, 118–127 (2018)CrossRefGoogle Scholar
  4. 4.
    Denny, J.S., Tapper, M.A., Schmieder, P.K., Hornung, M.W., Jensen, K.M., Ankley, G.T., Henry, T.R.: Comparison of relative binding affinities of endocrine active compounds to fathead minnow and rainbow trout estrogen receptors. Environ. Toxicol. Chem. 24(11), 2948–2953 (2005)CrossRefGoogle Scholar
  5. 5.
    Bartelt-Hunt, S., Snow, D.D., Damon-Powell, T., Miesbach, D.: Occurrence of steroid hormones and antibiotics in shallow groundwater impacted by livestock waste control facilities. J. Contam. Hydrol. 123(3), 94–103 (2011)CrossRefGoogle Scholar
  6. 6.
    Dutta, S., Inamdar, S., Tso, J., Aga, D.S., Sims, J.T.: Free and conjugated estrogen exports in surface-runoff from poultry litter-amended soil. J. Environ. Qual. 39(5), 1688–1698 (2010)CrossRefGoogle Scholar
  7. 7.
    Kulcu, R., Yaldiz, O.: The composting of agricultural wastes and the new parameter for the assessment of the process. Ecol. Eng. 69(4), 220–225 (2014)CrossRefGoogle Scholar
  8. 8.
    Toumpeli A, Pavlatou-Ve AK, Kostopoulou SK, Mamolos AP, Siomos AS, Kalburtji KL (2013) Composting Phragmites australis Cav. plant material and compost effects on soil and tomato (Lycopersicon esculentum Mill.) growth. J. Environ. Manag. 128(20):243–251CrossRefGoogle Scholar
  9. 9.
    Duong, T.T., Penfold, C., Marschner, P.: Amending soils of different texture with six compost types: impact on soil nutrient availability, plant growth and nutrient uptake. Plant Soil 354(1–2), 197–209 (2012)CrossRefGoogle Scholar
  10. 10.
    Zhang, H., Shi, J., Liu, X., Zhan, X., Dang, J., Bo, T.: Occurrence of free estrogens, conjugated estrogens, and bisphenol A in fresh livestock excreta and their removal by composting in North China. Environ. Sci. Pollut. Res. Int. 21(16), 9939–9947 (2014)CrossRefGoogle Scholar
  11. 11.
    Hakk, H., Millner, P., Larsen, G.: Decrease in water-soluble 17β-estradiol and testosterone in composted poultry manure with time. J. Environ. Qual. 34(3), 943–950 (2005)CrossRefGoogle Scholar
  12. 12.
    Hammett, K.M., Mullin, E.J., Aga, D.S., Felton, G.K., Fisher, D.J., Yonkos, L.T.: In vitro and in vivo assessment of aqueously extractable estrogens in poultry manure after pilot-scale composting. J. Environ. Qual. 46(3), 614–622 (2017)CrossRefGoogle Scholar
  13. 13.
    Ogawa, M., Okimori, Y., Krull, E., Singh, B., Joseph, S.: Pioneering works in biochar research, Japan. Soil. Res. 48(7), 489–500 (2010)CrossRefGoogle Scholar
  14. 14.
    Zhang, J., Chen, G., Sun, H., Zhou, S., Zou, G.: Straw biochar hastens organic matter degradation and produces nutrient-rich compost. Bioresour. Technol. 200, 876–883 (2016)CrossRefGoogle Scholar
  15. 15.
    Liu, N., Zhou, J., Han, L., Ma, S., Sun, X., Huang, G.: Role and multi-scale characterization of bamboo biochar during poultry manure aerobic composting. Bioresour. Technol. 241, 190–199 (2017)CrossRefGoogle Scholar
  16. 16.
    Wang, Q., Awasthi, M.K., Ren, X., Zhao, J., Li, R., Wang, Z., Wang, M., Chen, H., Zhang, Z.: Combining biochar, zeolite and wood vinegar for composting of pig manure: the effect on greenhouse gas emission and nitrogen conservation. Waste Manag. 74, 221–230 (2018)CrossRefGoogle Scholar
  17. 17.
    Li, W., Chen, G., Owens, G., Zhang, J.: Enhanced antibiotic removal by the addition of bamboo charcoal during pig manure composting. RSC Adv. 6(33), 27575–27583 (2016)CrossRefGoogle Scholar
  18. 18.
    Awasthi, M.K., Awasthi, S.K., Wang, Q., Wang, Z., Lahori, A.H., Ren, X., Chen, H., Wang, M., Zhao, J., Zhang, Z.: Influence of biochar on volatile fatty acids accumulation and microbial community succession during biosolids composting. Bioresour. Technol. 251, 158–164 (2018)CrossRefGoogle Scholar
  19. 19.
    He, X., Yin, H., Han, L., Cui, R., Fang, C., Huang, G.: Effects of biochar size and type on gaseous emissions during pig manure/wheat straw aerobic composting: insights into multivariate-microscale characterization and microbial mechanism. Bioresour. Technol. 271, 375–382 (2019)CrossRefGoogle Scholar
  20. 20.
    Lee, J.W., Kidder, M., Evans, B.R., Paik, S., Buchanan III, A.C., Garten, C.T., Brown, R.C.: Characterization of biochars produced from cornstovers for soil amendment. Environ. Sci. Technol. 44, 7970–7974 (2010)CrossRefGoogle Scholar
  21. 21.
    Boehm, H.P.: Some aspects of the surface chemistry of carbon blacks and other carbons. Carbon 32, 759–769 (1994)CrossRefGoogle Scholar
  22. 22.
    Chen, W., Liao, X., Wu, Y., Liang, J.B., Mi, J., Huang, J., Zhang, H., Wu, Y., Qiao, Z., Li, X., Wang, Y.: Effects of different types of biochar on methane and ammonia mitigation during layer manure composting. Waste Manag. 61, 506–515 (2017)CrossRefGoogle Scholar
  23. 23.
    Zhang, F.S., Xie, Y.F., Li, X.W., Wang, D.Y., Yang, L.S., Nie, Z.Q.: Accumulation of steroid hormones in soil and its adjacent aquatic environment from a typical intensive vegetable cultivation of North China. Sci. Total Environ. 538, 423–430 (2015)CrossRefGoogle Scholar
  24. 24.
    Qian, X., Sun, W., Gu, J., Wang, X.J., Zhang, Y.J., Duan, M.L., Li, H.C., Zhang, R.R.: Reducing antibiotic resistance genes, integrons, and pathogens in dairy manure by continuous thermophilic composting. Bioresour. Technol. 220, 425–432 (2016)CrossRefGoogle Scholar
  25. 25.
    Flor, S., He, X., Lehmler, H.J., Ludewig, G.: Estrogenicity and androgenicity screening of PCB sulfate monoesters in human breast cancer MCF-7 cells. Environ. Sci. Pollut. Res. 23(3), 2186–2200 (2016)CrossRefGoogle Scholar
  26. 26.
    Villalobos, M., Olea, N., Brotons, J.A., Olea-Serrano, M.F., Pedraza, V.: The E-Screen assay: a comparison of different MCF7 cell stocks. Environ. Health Perspect. 103(9), 844–850 (1995)CrossRefGoogle Scholar
  27. 27.
    Schiliro, T., Porfido, A., Spina, F., Varese, G.C., Gilli, G.: Oestrogenic activity of a textile industrial wastewater treatment plant effluent evaluated by the E-screen test and MELN gene-reporter luciferase assay. Sci. Total Environ. 432(16), 389–395 (2012)CrossRefGoogle Scholar
  28. 28.
    Yuan, S., Huang, C., Ji, X., Ma, M., Rao, K., Wang, Z.: Prediction of the combined effects of multiple estrogenic chemicals on MCF-7 human breast cancer cells and a preliminary molecular exploration of the estrogenic proliferative effects and related gene expression. Ecotoxicol. Environ. Saf. 160, 1–9 (2018)CrossRefGoogle Scholar
  29. 29.
    Wang, X., Zhao, Y., Wang, H., Zhao, X., Cui, H., Wei, Z.: Reducing nitrogen loss and phytotoxicity during beer vinasse composting with biochar addition. Waste Manag. 61, 150–156 (2017)CrossRefGoogle Scholar
  30. 30.
    Hua, L., Chen, Y., Wu, W., Ma, H.: Microorganism communities and chemical characteristics in sludge-bamboo charcoal composting system. Environ. Technol. 32(6), 663–672 (2011)CrossRefGoogle Scholar
  31. 31.
    Agyarko-Mintah, E., Cowie, A., Van Zwieten, L., Singh, B.P., Smillie, R., Harden, S., Fornasier, F.: Biochar lowers ammonia emission and improves nitrogen retention in poultry litter composting. Waste Manag. 61, 129–137 (2017)CrossRefGoogle Scholar
  32. 32.
    Van Zwieten, L., Kimber, S., Morris, S., Chan, K.Y., Downie, A., Rust, J., Joseph, S., Cowie, A.: Effects of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant Soil 327(1–2), 235–246 (2010)CrossRefGoogle Scholar
  33. 33.
    Wang, C.T., Lee, Y.C., Liao, F.Y.: Effect of composting parameters on the power performance of solid microbial fuel cells. Sustainability 7(9), 12634–12643 (2015)CrossRefGoogle Scholar
  34. 34.
    Sanchez-Garcia, M., Albuquerque, J.A., Sanchez-Monedero, M.A., Roig, A., Cayuela, M.L.: Biochar accelerates organic matter degradation and enhances N mineralisation during composting of poultry manure without a relevant impact on gas emissions. Bioresour. Technol. 192, 272–279 (2015)CrossRefGoogle Scholar
  35. 35.
    Jindo, K., Suto, K., Matsumoto, K., Garcia, C., Sonoki, T., Sanchez-Monedero, M.A.: Chemical and biochemical characterisation of biochar-blended composts prepared from poultry manure. Bioresour. Technol. 110, 396–404 (2012)CrossRefGoogle Scholar
  36. 36.
    Dias, B.O., Silva, C.A., Higashikawa, F.S., Roig, A., Sanchez-Monedero, M.A.: Use of biochar as bulking agent for the composting of poultry manure: effect on organic matter degradation and humification. Bioresour. Technol. 101(4), 1239–1246 (2010)CrossRefGoogle Scholar
  37. 37.
    Yu, C.P., Roh, H., Chu, K.H.: 17β-Estradiol-degrading bacteria isolated from activated sludge. Environ. Sci. Technol. 41(2), 486–492 (2007)CrossRefGoogle Scholar
  38. 38.
    Fernandez, L., Louvado, A., Esteves, V.I., Gomes, N.C.M., Almeida, A., Cunha, A.: Biodegradation of 17β-estradiol by bacteria isolated from deep sea sediments in aerobic and anaerobic media. J. Hazard. Mater. 323, 359–366 (2017)CrossRefGoogle Scholar
  39. 39.
    Jiang L, Yang J, Chen J (2010) Isolation and characteristics of 17β-estradiol-degrading Bacillus spp. strains from activated sludge. Biodegradation 21(5):729–736CrossRefGoogle Scholar
  40. 40.
    Takeshi, Y., Fumiko, N., Junji, F., Koichi, W., Harumi, M., Takashi, M., Kazumasa, K., Hideyuki, S., Haruji, S., Hiroshi, O.: Degradation of estrogens by Rhodococcus zopfii and Rhodococcus equi isolates from activated sludge in wastewater treatment plants. Appl. Environ. Microbiol. 70(9), 5283–5289 (2004)CrossRefGoogle Scholar
  41. 41.
    Ravindran, B., Nguyen, D.D., Chaudhary, D., Chang, S.W., Kim, J., Lee, S.R., Shin, J.D., Jeon, B.H., Chung, S.J., Lee, J.J.: Influence of biochar on physico-chemical and microbial community during swine manure composting process. J. Environ. Manag. 232, 592–599 (2019)CrossRefGoogle Scholar
  42. 42.
    Lee, J., Cho, J., Kim, S.H., Kim, S.D.: Influence of 17β-estradiol binding by dissolved organic matter isolated from wastewater effluent on estrogenic activity. Ecotoxicol. Environ. Saf. 74(5), 1280–1287 (2011)CrossRefGoogle Scholar
  43. 43.
    Zhang, F., Yang, L., Liu, X., Li, Y., Fang, H., Wang, X., Alharbi, N.S., Li, J.: Sorption of 17β-estradiol to the dissolved organic matter from animal wastes: effects of composting and the role of fulvic acid-like aggregates. Environ. Sci. Pollut. Res. 25(17), 16875–16884 (2018)CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Bioengineering, College of Material and Chemical EngineeringHainan UniversityHaikouPeople’s Republic of China
  2. 2.Key Laboratory of Land Surface Pattern and Simulation, Institute of Geographic Sciences and Natural Resources ResearchChinese Academy of SciencesBeijingPeople’s Republic of China

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