Organic micropollutants’ distribution within sludge organic matter fractions explains their dynamic during sewage sludge anaerobic digestion followed by composting

  • Quentin Aemig
  • Nicolas Doussiet
  • Alice Danel
  • Nadine Delgenès
  • Julie Jimenez
  • Sabine Houot
  • Dominique PatureauEmail author
Research Article


The simultaneous fate of organic matter and 4 endocrine disruptors (3 polycyclic aromatic hydrocarbons (PAHs) (fluoranthene, benzo(b)fluoranthene, and benzo(a)pyrene) and nonylphenols (NP)) was studied during the anaerobic digestion followed by composting of sludge at lab-scale. Sludge organic matter was characterized, thanks to chemical fractionation and 3D fluorescence deciphering its accessibility and biodegradability. Total chemical oxygen demand (COD) removal was 41% and 56% during anaerobic digestion and composting, respectively. 3D fluorescence highlighted the quality changes of organic matter. During continuous anaerobic digestion, organic micropollutants’ removal was 22 ± 14%, 6 ± 5%, 18 ± 9%, and 0% for fluoranthene, benzo(b)fluoranthene, benzo(a)pyrene, and nonylphenols, respectively. Discontinuous composting allowed to go further on the organic micropollutants’ removal as 34 ± 8%, 31 ± 20%, 38 ± 10%, and 52 ± 6% of fluoranthene, benzo(b)fluoranthene, benzo(a)pyrene, and nonylphenols were dissipated, respectively. Moreover, the accessibility of PAH and NP expressed by their presence in the various sludge organic matter fractions and its evolution during both treatments was linked to both the quality evolution of the organic matter and the physicochemical properties of the PAH and NP; the presence in most accessible fractions explained the amount of PAH and NP dissipated.


Anaerobic digestion Composting Organic matter Polycyclic aromatic hydrocarbons Nonylphenols Accessibility 



Accelerated solvent extraction






Chemical oxygen demand (gO2 L−1)


Continuous stirred tank reactor


Digested secondary sludge


European Union




Green wastes


High-performance liquid chromatography


Hydraulic retention time


Initial mixture of compost


End of the maturation phase of compost


Non-extractable organic matter




Polycyclic aromatic hydrocarbons


Poorly extractable organic matter


Readily extractable organic matter


Slowly extractable organic matter


Solubilizable fraction from particulate organic matter


Secondary sludge


End of the temperature decrease phase of compost


End of the thermophilic phase of compost


Total solids (g L−1)


Wastewater treatment plant

Z1, Z2, Z3, Z4, Z5, Z6, and Z7

3D fluorescence zones



This work was supported by the French Environment and Energy Management Agency (ADEME) and the French National Agency for Biodiversity (AFB).

Supplementary material

11356_2018_4014_MOESM1_ESM.docx (24 kb)
ESM 1 (DOCX 24 kb)


  1. Aemig Q, Chéron C, Delgenès N, Jimenez J, Houot S, Steyer JP, Patureau D (2016) Distribution of polycyclic aromatic hydrocarbons (PAHs) in sludge organic matter pools as a driving force of their fate during anaerobic digestion. Waste Manag 48:389–396CrossRefGoogle Scholar
  2. Ahel M, Giger W, Molnar E, Ibric S (2000) Determination of nonylphenol polyethoxylates and their lipophilic metabolites in sewage effluents by normal-phase high-performance liquid chromatography and fluorescence detection. Croat Chem Acta 73:209–227Google Scholar
  3. Amir S, Hafidi H, Merlina G, Hamdi H, Revel JC (2005) Fate of polycylic aromatic hydrocarbons during composting of lagooning sewage sludge. Chemosphere 58:449–458CrossRefGoogle Scholar
  4. Artola-Garicano E, Borkent I, Damen K, Jager T, Vaes WHJ (2003) Sorption kinetics and microbial biodegradation activity of hydrophobic chemicals in sewage sludge: model and measurements based on free concentrations. Environ Sci Technol 37:116–122CrossRefGoogle Scholar
  5. Barret M, Carrère H, Delgadillo L, Patureau D (2010a) PAH fate during the anaerobic digestion of contaminated sludge: do bioavailability and/or cometabolism limit their biodegradation? Water Res 44:3797–3806CrossRefGoogle Scholar
  6. Barret M, Carrère H, Latrille E, Wieniewsky C, Patureau D (2010b) Micropollutant and sludge characterization for modeling sorption equilibria. Environ Sci Technol 44:1100–1106CrossRefGoogle Scholar
  7. Barret M, Barcia GC, Guillon A, Carrere H, Patureau D (2010c) Influence of feed characteristics on the removal of micropollutants during the anaerobic digestion of contaminated sludge. J Hazard Mater 181(1–3):241–247CrossRefGoogle Scholar
  8. Barret M, Delgadillo-Mirquez L, Trably E (2012) Anaerobic removal of trace organic contaminants in sewage sludge: 15 years of experience. Pedosphere 22:508–517CrossRefGoogle Scholar
  9. Blanchard M, Teil MJ, Ollivon D, Legenti L, Chevreuil M (2004) Polycyclic aromatic hydrocarbons and polychlorobiphenyls in wastewaters and sewage sludges from the Paris area (France). Environ Res 95:184–197CrossRefGoogle Scholar
  10. Bozkurt H, Sanin FD (2014) Toxicity of nonylphenol diethoxylate in lab-scale anaerobic digesters. Chemosphere 104:69–75CrossRefGoogle Scholar
  11. Brandli RC, Bucheli TD, Kupper T, Furrer R, Stadelmann FX, Tarradellas J (2005) Persistent organic pollutants in source-separated compost and its feedstock materials - a review of field studies. J Environ Qual 34(3):735–760CrossRefGoogle Scholar
  12. Buffiere P, Loisel D, Bernet N, Delgenes JP (2006) Towards new indicators for the prediction of solid waste anaerobic digestion properties. Water Sci Technol 53(8):233–241CrossRefGoogle Scholar
  13. Cea-Barcia G, Carrère H, Steyer JP, Patureau D (2013) Evidence for PAH removal coupled to the first steps of anaerobic digestion in sewage sludge. Int J Chem Eng 2013:1–6. CrossRefGoogle Scholar
  14. Chen W, Westerhoff P, Leenheer JA, Booksh K (2003) Fluorescence excitation-emission matrix regional integration to quantify spectra for dissolved organic matter. Environ Sci Technol 37:5701–5710CrossRefGoogle Scholar
  15. Delgadillo-Mirquez L, Lardon L, Steyer J-P, Patureau D (2011) A new dynamic model for bioavailability and cometabolism of micropollutants during anaerobic digestion. Water Res 45:4511–4521CrossRefGoogle Scholar
  16. Dionisi D, Bertin L, Bornoroni L, Capodicasa S, Papini MP, Fava F (2006) Removal of organic xenobiotics in activated sludges under aerobic conditions and anaerobic digestion of the adsorbed species. J Chem Technol Biotechnol 81:1496–1505CrossRefGoogle Scholar
  17. Francou C, Linères M, Derenne S, Le Villio-Poitrenaud M, Houot S (2008) Influence of green waste, biowaste and paper–cardboard initial ratios on organic matter transformations during composting. Bioresour Technol 99:8926–8934CrossRefGoogle Scholar
  18. Hafidi M, Amir S, Jouraiphy A, Winterton P, El Gharous M, Merlina G, Revel J-C (2008) Fate of polycyclic aromatic hydrocarbons during composting of activated sewage sludge with green waste. Bioresour Technol 99(18):8819–8823Google Scholar
  19. Hartlieb N, Ertunc T, Schaeffer A, Klein W (2003) Mineralization, metabolism and formation of non-extractable residues of 14C-labelled organic contaminants during pilot-scale composting of municipal biowaste. Environ Pollut 126:83–91CrossRefGoogle Scholar
  20. He XS, Xi BD, Li X, Pan HW, An D, Bai SG, Li D, Cui DY (2013) Fluorescence excitation-emission matrix spectra coupled with parallel factor and regional integration analysis to characterize organic matter humification. Chemosphere 93:2208–2215CrossRefGoogle Scholar
  21. Jimenez J, Gonidec E, Cacho Rivero JA, Latrille E, Vedrenne F, Steyer JP (2014) Prediction of anaerobic biodegradability and bioaccessibility of municipal sludge by coupling sequential extractions with fluorescence spectroscopy: towards ADM1 variables characterization. Water Res 50:359–372CrossRefGoogle Scholar
  22. Jimenez J, Aemig Q, Doussiet N, Feurgard I, Steyer JP, Patureau D, Houot S (2015) Towards a unified organic waste characterization of organic matter accessibility and complexity. Bioresour Technol 194:344–353CrossRefGoogle Scholar
  23. Jonker MTO (2008) Absorption of polycyclic aromatic hydrocarbons to cellulose. Chemosphere 70:778–782CrossRefGoogle Scholar
  24. Kara Murdoch F, Sanin FD (2016) Biotransformation of nonylphenol diethoxylate in anaerobic digesters: accumulation of metabolites and their effects on digester performance. Int Biodeterior Biodegrad 110:61–68CrossRefGoogle Scholar
  25. Kelessidis A, Stasinakis AS (2012) Comparative study of the methods used for treatment and final disposal of sewage sludge in European countries. Waste Manag 32:1186–1195CrossRefGoogle Scholar
  26. La Merrill MA (2016) The economic legacy of endocrine-disrupting chemicals. Lancet Diabetes Endocrinol 4:961–962.
  27. Lashermes G, Barriuso E, Houot S (2012a) Dissipation pathways of organic pollutants during the composting of organic wastes. Chemosphere 87:137–143CrossRefGoogle Scholar
  28. Lashermes G, Barriuso E, Le Villio-Poitrenaud M, Houot S (2012b) Composting in small laboratory pilots: performance and reproducibility. Waste Manag 32:271–277Google Scholar
  29. Laturnus F, Grøn C (2007) Organic contaminants from sewage sludge applied to agricultural soils. False alarm regarding possible problems for food safety? Environ Sci Pollut Res Int 14(Suppl 1):53–60CrossRefGoogle Scholar
  30. Mailler R, Gasperi J, Chebbo G, Rocher V (2014) Priority and emerging pollutants in sewage sludge and fate during sludge treatment. Waste Manag 34:1217–1226CrossRefGoogle Scholar
  31. Mailler R, Gasperi J, Patureau D, Vulliet E, Delgenes N, Danel A, Deshayes S, Eudes V, Guerin S, Moilleron R, Chebbo G, Rocher V (2017) Fate of emerging and priority micropollutants during the sewage sludge treatment: case study of Paris conurbation. Part 1: contamination of the different types of sewage sludge. Waste Manag 59:379–393CrossRefGoogle Scholar
  32. Martin Ruel S, Choubert J-MMJ-M, Budzinski H et al (2012) Occurrence and fate of relevant substances in wastewater treatment plants regarding Water Framework Directive and future legislations. Water Sci Technol 65:1179–1189CrossRefGoogle Scholar
  33. Mougin C, Dappozze F, Brault A, Malosse C, Schmidt JE, Amellal-Nassr N, Patureau D (2006) Phthalic acid and benzo[a]pyrene in soil–plant–water systems amended with contaminated sewage sludge. Environ Chem Lett 4:201–206CrossRefGoogle Scholar
  34. Muller M, Milori DMBP, Déléris S, Steyer JP, Dudal Y (2011) Solid-phase fluorescence spectroscopy to characterize organic wastes. Waste Manag 31:1916–1923CrossRefGoogle Scholar
  35. Olivella MA, Fernández I, Cano L, Jové P, Oliveras A (2012) Role of chemical components of cork on sorption of aqueous polycyclic aromatic hydrocarbons. Int J Environ Res 7:225–234Google Scholar
  36. Olivella MÀ, Jové P, Bianchi A, Bazzicalupi C, Cano L (2013) An integrated approach to understanding the sorption mechanism of phenanthrene by cork. Chemosphere 90:1939–1944CrossRefGoogle Scholar
  37. Pacyna JM, Sundseth K, Pacyna EG, Cousins AP, Hansson K, Guerra P, Eljerrat E, Krupanek J, Zielonka U (2009) Material flow analysis for selected priority substances. Sixth Framework Programme SOCOPSE – Source Control of Priority Substances in Europe. Deliverable: Workpackage 2. D2.1. 74pGoogle Scholar
  38. Paterakis N, Chiu TYY, Koh YKKKK et al (2012) The effectiveness of anaerobic digestion in removing estrogens and nonylphenol ethoxylates. J Hazard Mater 199–200:88–95CrossRefGoogle Scholar
  39. Patureau D, Delgenes N, Delgenes JP (2008) Impact of sewage sludge treatment processes on the removal of the endocrine disrupters nonylphenol ethoxylates. Chemosphere 72:586–591CrossRefGoogle Scholar
  40. Peltre C, Dignac MF, Derenne S, Houot S (2010) Change of the chemical composition and biodegradability of the Van Soest soluble fraction during composting: a study using a novel extraction method. Waste Manag 30:2448–2460CrossRefGoogle Scholar
  41. Samaras VG, Stasinakis AS, Thomaidis NS, Mamais D, Lekkas TD (2014) Fate of selected emerging micropollutants during mesophilic, thermophilic and temperature co-phased anaerobic digestion of sewage sludge. Bioresour Technol 162:365–372CrossRefGoogle Scholar
  42. Semple KT, Doick KJ, Jones KC, Burauel P, Craven A, Harms H (2004) Defining bioavailability and bioaccessibility of contaminated soil and sediment is complicated. Environ Sci Technol 38(12):228A–231ACrossRefGoogle Scholar
  43. Stasinakis AS (2012) Review on the fate of emerging contaminants during sludge anaerobic digestion. Bioresour Technol 121:432–440CrossRefGoogle Scholar
  44. Trably E, Delgènes N, Patureau D, Delgènes JP (2004) Statistical tools for the optimization of a highly reproducible method for the analysis of polycyclic aromatic hydrocarbons in sludge samples. Int J Environ Anal Chem 84:995–1008CrossRefGoogle Scholar
  45. Westerman PW, Bicudo JR (2005) Management considerations for organic waste use in agriculture. Bioresour Technol 96:215–221CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Quentin Aemig
    • 1
  • Nicolas Doussiet
    • 1
  • Alice Danel
    • 1
  • Nadine Delgenès
    • 1
  • Julie Jimenez
    • 1
  • Sabine Houot
    • 2
  • Dominique Patureau
    • 1
    Email author
  1. 1.LBE, Univ Montpellier, INRANarbonneFrance
  2. 2.UMR ECOSYS, INRA, AgroParisTechUniversité Paris-SaclayThiverval-GrignonFrance

Personalised recommendations