Skip to main content
Log in

Pyrolysis Treatment Enables Safe Application of Sewage Sludge in Horticulture: Tracking Potentially Toxic Elements Through the Biochar-Soil–Plant System in Tomato

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

Biochar production via pyrolysis is a promising option for treating sewage sludge (SS). Here we investigated the uptake of potentially toxic elements (PTEs) from SS and its biochar (450 °C) into cherry tomato (Lycopersicon esculentum L.) plants and their fruits in pot experiments (2, 5 and 10%), to assess the health risks associated with fruit consumption. We further studied the ability of the PTE-rich amendments to immobilize PTEs already present in soil through spiking of soil (pH 7.4) with Cd, Cu and Zn. Our findings suggest that tomato consumption is not a human health risk when grown in soil amended with SS and its biochar; in most treatments PTE uptake into fruits was similar to the control. Vegetative plant growth was highest in SS-amended soils. Yet 5 and 10% biochar-amended soils significantly increased tomato fruit yield relative to untreated SS application (400–500% higher than 10% SS-amended soil) and significantly decreased fruit uptake of Cu and Zn. Importantly, biochar also significantly immobilized PTEs present in contaminated (spiked) soil. As expected, available (DTPA-extractable) PTE contents were typically lower in biochar-amended soil and sequential extraction indicated that the PTEs were predominantly bound in more recalcitrant soil fractions (organic matter associated and Fe–Mn oxides-bound). We conclude that pyrolysis can be a key technology for treatment of PTE-rich SS and subsequent use of the produced biochar in urban, and potentially even PTE-contaminated, horticultural sites.

Graphic Abstract

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
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

All data generated or analysed during this study are included in this article (and its supplementary information files). Detailed data can be made available from the corresponding author upon request.

References

  1. Gao, N., Kamran, K., Quan, C., Williams, P.T.: Thermochemical conversion of sewage sludge: a critical review. Prog. Energy Combust. Sci. 79, 100843 (2020)

    Article  Google Scholar 

  2. Urbaniak, M., Wyrwicka, A., Tołoczko, W., Serwecińska, L., Zieliński, M.: The effect of sewage sludge application on soil properties and willow (Salix sp.) cultivation. Sci. Total Environ. 586, 66–75 (2017)

    Article  Google Scholar 

  3. Racek, J., Sevcik, J., Chorazy, T., Kucerik, J., Hlavinek, P.: Biochar—recovery material from pyrolysis of sewage sludge: a review. Waste Biomass Valoriz. 11, 3677–3709 (2020)

    Article  Google Scholar 

  4. Zielińska, A., Oleszczuk, P.: The conversion of sewage sludge into biochar reduces polycyclic aromatic hydrocarbon content and ecotoxicity but increases trace metal content. Biomass Bioenergy. 75, 235–244 (2015)

    Article  Google Scholar 

  5. Kominko, H., Gorazda, K., Wzorek, Z.: The possibility of organo-mineral fertilizer production from sewage sludge. Waste Biomass Valoriz. 8, 1781–1791 (2017)

    Article  Google Scholar 

  6. Boguniewicz-Zablocka, J., Klosok-Bazan, I., Capodaglio, A.G.: Sustainable management of biological solids in small treatment plants: overview of strategies and reuse options for a solar drying facility in Poland. Environ. Sci. Pollut. Res. 28, 24680–24693 (2021)

    Article  Google Scholar 

  7. Collivignarelli, M.C., Abbà, A., Frattarola, A., Carnevale Miino, M., Padovani, S., Katsoyiannis, I., Torretta, V.: Legislation for the reuse of biosolids on agricultural land in Europe: overview. Sustainability 11, 6015 (2019)

    Article  Google Scholar 

  8. Ross, J.J., Zitomer, D.H., Miller, T.R., Weirich, C.A., McNamara, P.J.: Emerging investigators series: pyrolysis removes common microconstituents triclocarban, triclosan, and nonylphenol from biosolids. Environ. Sci. Water Res. Technol. 2, 282–289 (2016)

    Article  Google Scholar 

  9. Hoffman, T.C., Zitomer, D.H., McNamara, P.J.: Pyrolysis of wastewater biosolids significantly reduces estrogenicity. J. Hazard. Mater. 317, 579–584 (2016)

    Article  Google Scholar 

  10. Buss, W.: Pyrolysis solves the issue of organic contaminants in sewage sludge while retaining carbon—making the case for sewage sludge treatment via pyrolysis. ACS Sustainable Chem. Eng. (2021, in press)

  11. Roberts, D.A., Cole, A.J., Whelan, A., de Nys, R., Paul, N.A.: Slow pyrolysis enhances the recovery and reuse of phosphorus and reduces metal leaching from biosolids. Waste Manag. 64, 133–139 (2017)

    Article  Google Scholar 

  12. Frišták, V., Pipíška, M., Soja, G.: Pyrolysis treatment of sewage sludge: a promising way to produce phosphorus fertilizer. J. Clean Prod. 172, 1772–1778 (2018)

    Article  Google Scholar 

  13. Callegari, A., Capodaglio, A.G.: Properties and beneficial uses of (bio)chars, with special attention to products from sewage sludge pyrolysis. Resources 7, 1–22 (2018)

    Article  Google Scholar 

  14. Bolognesi, S., Bernardi, G., Callegari, A., Dondi, D., Capodaglio, A.G.: Biochar production from sewage sludge and microalgae mixtures: properties, sustainability and possible role in circular economy. Biomass Conv. Bioref. 11, 289–299 (2021)

    Article  Google Scholar 

  15. Buss, W., Bogush, A., Ignatyev, K., Mašek, O.: Unlocking the fertilizer potential of waste-derived biochar. ACS Sustain. Chem. Eng. 8, 12295–12303 (2020)

    Article  Google Scholar 

  16. Buss, W., Graham, M.C., Shepherd, J.G., Mašek, O.: Suitability of marginal biomass-derived biochars for soil amendment. Sci. Total Environ. 547, 314–322 (2016)

    Article  Google Scholar 

  17. Racek, J., Sevcik, J., Komendova, R., Kucerik, J., Hlavinek, P.: Heavy metal fixation in biochar after microwave pyrolysis of sewage sludge. Desalin. Water Treat. 159, 79–92 (2019)

    Article  Google Scholar 

  18. Méndez, A., Gómez, A., Paz-Ferreiro, J., Gascó, G.: Effects of sewage sludge biochar on plant metal availability after application to a Mediterranean soil. Chemosphere 89, 1354–1359 (2012)

    Article  Google Scholar 

  19. Agrafioti, E., Bouras, G., Kalderis, D., Diamadopoulos, E.: Biochar production by sewage sludge pyrolysis. J Anal. Appl. Pyrolysis 101, 72–78 (2013)

    Article  Google Scholar 

  20. Jin, J., Li, Y., Zhang, J., Wu, S., Cao, Y., Liang, P., Zhang, J., Wong, M.H., Wang, M., Shan, S., Christie, P.: Influence of pyrolysis temperature on properties and environ-mental safety of heavy metals in biochars derived from municipal sewage sludge. J. Hazard. Mater. 320, 417–426 (2016)

    Article  Google Scholar 

  21. Yue, Y., Cui, L., Lin, Q., Li, G., Zhao, X.: Efficiency of sewage sludge biochar in improving urban soil properties and promoting grass growth. Chemosphere 173, 551–556 (2017)

    Article  Google Scholar 

  22. Schwarz, D., Thompson, A.J., Kläring, H.P.: Guidelines to use tomato in experiments with a controlled environment. Front. Plant Sci. 5, 625 (2014)

    Article  Google Scholar 

  23. Yu, K., Van Geel, M., Ceulemans, T., Geerts, W., Ramos, M.M., Serafim, C., Sousa, N., Castro, P.M.L., Kastendeuch, P., Najjar, G., Ameglio, T., Ngao, J., Saudreau, M., Honnay, O., Somers, B.: Vegetation reflectance spectroscopy for biomonitoring of heavy metal pollution in urban soils. Environ. Pollut. 243, 1912–1922 (2018)

    Article  Google Scholar 

  24. Yuan, X., Xue, N., Han, Z.: A meta-analysis of heavy metals pollution in farmland and urban soils in China over the past 20 years. J. Environ. Sci. 101, 217–226 (2021)

    Article  Google Scholar 

  25. Beesley, L., Moreno-Jiménez, E., Gomez-Eyles, J.L.: Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environ. Pollut. 158, 2282–2287 (2010)

    Article  Google Scholar 

  26. Rowell, D.L.: Soil Science: Methods and Applications, 1st edn., p. 345. Longman Group, Harlow (1994)

    Google Scholar 

  27. He, Z., Shentu, J., Yang, X., Baligar, V.C., Zhang, T., Stofella, P.J.: Heavy metal contamination of soils: sources, indicators, and assessment. J. Environ. Indic. 9, 17–18 (2015)

    Google Scholar 

  28. Rollwagen, B.A., Zasoski, R.J.: Nitrogen source effects on rhizosphere pH and nutrient accumulation by Pacific Northwest conifers. Plant Soil 105, 79–86 (1988)

    Article  Google Scholar 

  29. Cao, H., Chen, J., Zhang, J., Zhang, H., Qiao, L., Men, Y.: Heavy metals in rice and garden vegetables and their potential health risks to inhabitants in the vicinity of an industrial zone in Jiangsu, China. J. Environ. Sci. 22, 1792–1799 (2010)

    Article  Google Scholar 

  30. Mattina, M.J.I., Lannucci-Berger, W., Musante, C., White, J.C.: Concurrent plant uptake of heavy metals and persistent organic pollutants from soil. Environ. Pollut. 124, 375–378 (2003)

    Article  Google Scholar 

  31. Muñoz, O., Zamorano, P., Garcia, O., Bastías, J.M.: Arsenic, cadmium, mercury, sodium, and potassium concentrations in common foods and estimated daily intake of the population in Valdivia (Chile) using a total diet study. Food Chem. Toxicol. 109, 1125–1134 (2017)

    Article  Google Scholar 

  32. Jalali, M., Karimi Mojahed, J.: Assessment of the health risks of heavy metals in soils and vegetables from greenhouse production systems in Iran. Int. J. Phytoremediat. 22, 834–848 (2020)

    Article  Google Scholar 

  33. ISIRI.: Food and feed-maximum limit of heavy metals. Institute of Standards and Industrial Research of Iran. pp. 210–212 (2010)

  34. US-EPA.: Integrated risk information system. https://www.epa.gov/science-andtechnology/health-science. United States, Environmental Protection Agency (2007)

  35. Pajević, S., Arsenov, D., Nikolić, N., Borišev, M., Orčić, D., Župunski, M., Mimica-Dukić, N.: Heavy metal accumulation in vegetable species and health risk assessment in Serbia. Environ. Monit. Assess. 190, 459 (2018)

    Article  Google Scholar 

  36. Pietrzak, U., McPhail, D.C.: Copper accumulation, distribution and fractionation in vineyard soils of Victoria, Australia. Geoderma 122, 151–166 (2004)

    Article  Google Scholar 

  37. Lindsay, W.L., Norvell, W.A.: Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci. Soc. Am. J. 42, 421–428 (1978)

    Article  Google Scholar 

  38. Tessier, A., Campbell, P.G., Bisson, M.: Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem. 51, 844–851 (1979)

    Article  Google Scholar 

  39. Jaradat, Q.M., Massadeh, A.M., Zaitoun, M.A., Maitah, B.M.: Fractionation and sequential extraction of heavy metals in the soil of scrapyard of discarded vehicles. Environ. Monit. Assess. 112, 197–210 (2006)

    Article  Google Scholar 

  40. Kabala, C., Singh, B.R.: Fractionation and mobility of copper, lead, and zinc in soil profiles in the vicinity of a copper smelter. J. Environ. Qual. 30, 485–492 (2001)

    Article  Google Scholar 

  41. SAS Institute Inc: SAS Software, Version 9.1 of the SAS System for Windows. SAS Institute Inc, Cary (2004)

    Google Scholar 

  42. Hossain, M.K., Strezov, V., Chan, K.Y., Ziolkowski, A., Nelson, P.F.: Influence of pyrolysis temperature on production and nutrient properties of wastewater sludge biochar. J. Environ. Manag. 92, 223–228 (2011)

    Article  Google Scholar 

  43. Buss, W., Graham, M.C., Shepherd, J.G., Mašek, O.: Risks and benefits of marginal biomass-derived biochars for plant growth. Sci. Total Environ. 569–570, 496–506 (2016)

    Article  Google Scholar 

  44. Song, X.D., Xue, X.Y., Chen, D.Z., He, P.J., Dai, X.H.: Application of biochar from sewage sludge to plant cultivation: influence of pyrolysis temperature and biochar-to-soil ratio on yield and heavy metal accumulation. Chemosphere 109, 213–220 (2014)

    Article  Google Scholar 

  45. Waqas, M., Li, G., Khan, S., Shamshad, I., Reid, B.J., Qamar, Z., Chao, C.: Application of sewage sludge and sewage sludge biochar to reduce polycyclic aromatic hydrocarbons (PAH) and potentially toxic elements (PTE) accumulation in tomato. Environ. Sci. Pollut. Res. 22, 12114–12123 (2015)

    Article  Google Scholar 

  46. Hossain, M.K., Strezov, V., Nelson, P.F.: Comparative assessment of the effect of wastewater sludge biochar on growth, yield and metal bioaccumulation of cherry tomato. Pedosphere 25, 680–685 (2015)

    Article  Google Scholar 

  47. Bose, S., Bhattacharyya, A.K.: Heavy metal accumulation in wheat plant grown in soil amended with industrial sludge. Chemosphere 70, 1264–1272 (2008)

    Article  Google Scholar 

  48. McBride, M.B.: Chemisorption of Cd on calcite surfaces. Soil. Sci. Soc. Am. J. 44, 26–28 (1980)

    Article  Google Scholar 

  49. Bogusz, A., Oleszczuk, P.: Effect of biochar addition to sewage sludge on cadmium, copper and lead speciation in sewage sludge-amended soil. Chemosphere. 239, 124719 (2020)

    Article  Google Scholar 

  50. Vaccari, F.P., Maienza, A., Miglietta, F., Baronti, S., Di Lonardo, S., Giagnoni, L., Lagomarsino, A., Pozzi, A., Pusceddu, E., Ranieri, R., Valboa, G., Genesio, L.: Biochar stimulates plant growth but not fruit yield of processing tomato in a fertile soil. Agric. Ecosyst. Environ. 207, 163–170 (2015)

    Article  Google Scholar 

  51. Xing, J., Li, L., Li, G., Xu, G.: Feasibility of sludge-based biochar for soil remediation: characteristics and safety performance of heavy metals influenced by pyrolysis temperatures. Ecotoxicol. Environ. Saf. 180, 457–465 (2019)

    Article  Google Scholar 

  52. Ignatowicz, K.: The impact of sewage sludge treatment on the content of selected heavy metals and their fractions. Environ. Res. 156, 19–22 (2017)

    Article  Google Scholar 

  53. Huang, R., Zhang, B., Saad, E.M., Ingall, E.D., Tang, Y.: Speciation evolution of zinc and copper during pyrolysis and hydrothermal carbonization treatments of sewage sludges. Water Res. 132, 260–269 (2018)

    Article  Google Scholar 

  54. Yuan, H., Lu, T., Huang, H., Zhao, D., Kobayashi, N., Chen, Y.: Influence of pyrolysis temperature on physical and chemical properties of biochar made from sewage sludge. J. Anal. Appl. Pyrolysis. 112, 284–289 (2015)

    Article  Google Scholar 

  55. Hemati Matin, N., Jalali, M., Buss, W.: Synergistic immobilization of potentially toxic elements (PTEs) by biochar and nanoparticles in alkaline soil. Chemosphere 241, 124932 (2020)

    Article  Google Scholar 

Download references

Acknowledgements

We thank the University of Bu-Ali Sina for providing support for this study.

Author information

Authors and Affiliations

Authors

Contributions

ST: laboratory analyses, writing original draft. MJ: writing, review and editing. WB: writing, review and editing. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Samaneh Tahervand.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

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

Consent to Participate

No personal data are contained in this study that would require to ask for consent.

Consent to Publish

All co-authors have consented to the publication of this study.

Additional information

Publisher's Note

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

Appendix

Appendix

See Table 4 and Figs. 5, 6 and 7.

Table 4 Correlation coefficient between different forms of PTEs in rhizosphere soils and PTEs contents in aboveground parts (shoot + fruit) of cherry tomato (n = 7)
Fig. 5
figure 5

Scanning election microscopy (SEM) of the SS (a) and SS biochar (b) at 500 × magnification; SS (c) and SS biochar (d) at 1000 × magnification; SS (e) and SS biochar (f) at 3000 × magnification

Fig. 6
figure 6

FTIR spectra of SS and SS biochar

Fig. 7
figure 7

Mobility factor based on data from the sequential extraction of PTEs in rhizosphere soils (left columns in each figure) and bulk soils (right columns) in non-spiked (a, c and e) and spiked soils (b, d and f). Columns marked with the same letter are not significantly different (Duncan’s multiple range test) at the p < 0.05 level. Error bars represent standard deviations (n = 3). C control soil, SS sewage sludge, B sewage sludge biochar

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tahervand, S., Jalali, M. & Buss, W. Pyrolysis Treatment Enables Safe Application of Sewage Sludge in Horticulture: Tracking Potentially Toxic Elements Through the Biochar-Soil–Plant System in Tomato. Waste Biomass Valor 13, 1277–1292 (2022). https://doi.org/10.1007/s12649-021-01558-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-021-01558-z

Keywords

Navigation