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Upgrading agrifood co-products via solid fermentation yields environmental benefits under specific conditions only

Nature Food volume 3, pages 911–920 (2022)Cite this article

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Abstract

Transforming residual biomass into edible ingredients is increasingly promoted to alleviate the environmental impacts of food systems. Yet, these approaches mostly rely on emerging technologies and constrained resources, and their environmental benefits remain unclear. By combining process-based consequential life cycle analysis, uncertainty assessment and biomass resource estimation, we quantified the impacts of deploying waste-to-nutrition pathways, here applied to the upgrading of agrifood co-products by solid-state fermentation (SSF). The benefits of reducing the demand for soybean meal by enhancing the protein concentration of feed through SSF do not compensate for the environmental burdens induced by the process on climate change, water depletion and land use. Besides unlocking feed markets to low-feed-quality streams, SSF outperforms energy valorization for most environmental impacts but is less competitive to mitigate climate change. Yet, SSF yields overall environmental benefits when unlocking food markets rather than supplying feed and energy services. Systematic methodological harmonization is required to assess the potential of novel ingredients, as outcomes vary according to the displaced food and feed baskets, and related land use changes.

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Fig. 1: Conventional and alternative management practices for agrifood co-products.
Fig. 2: Environmental impacts of four agrifood co-product management practices.
Fig. 3: Effects of SSF on ingredients avoided by the incorporation of agrifood co-products into feed.

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Data availability

The datasets generated and analysed during the current study are available in the Dataverse repository at https://doi.org/10.48531/JBRU.CALMIP/C2X5I2.

References

  1. Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855 (2015).

    Article  PubMed  Google Scholar 

  2. Karlsson, J. O., Parodi, A., van Zanten, H. H. E., Hansson, P.-A. & Röös, E. Halting European Union soybean feed imports favours ruminants over pigs and poultry. Nat. Food 2, 38–46 (2021).

    Article  Google Scholar 

  3. Wilfart, A. et al. Réduire les impacts environnementaux des aliments pour les animaux d’élevage. INRA Prod. Anim. 31, 289–306 (2019).

    Article  Google Scholar 

  4. Muscat, A. et al. Principles, drivers and opportunities of a circular bioeconomy. Nat. Food 2, 561–566 (2021).

    Article  Google Scholar 

  5. Parodi, A. et al. The potential of future foods for sustainable and healthy diets. Nat. Sustain. 1, 782–789 (2018).

    Article  Google Scholar 

  6. Javourez, U., O’Donohue, M. & Hamelin, L. Waste-to-nutrition: a review of current and emerging conversion pathways. Biotechnol. Adv. 53, 107857 (2021).

    Article  CAS  PubMed  Google Scholar 

  7. Hamelin, L., Borzęcka, M., Kozak, M. & Pudełko, R. A spatial approach to bioeconomy: quantifying the residual biomass potential in the EU-27. Renew. Sustain. Energy Rev. 100, 127–142 (2019).

    Article  Google Scholar 

  8. Fritsche, U. et al. Future Transitions for the Bioeconomy Towards Sustainable Development and a Climate-Neutral Economy: Foresight Scenarios for the EU Bioeconomy in 2050 (Publications Office of the European Union, 2021).

  9. Resource Efficiency Champions: Co-product, an Essential Part of Animal Nutrition (FEFAC, 2019).

  10. Kasapidou, E., Sossidou, E. & Mitlianga, P. Fruit and vegetable co-products as functional feed ingredients in farm animal nutrition for improved product quality. Agriculture 5, 1020–1034 (2015).

    Article  CAS  Google Scholar 

  11. Garcia-Bernet, D. & Ferraro, V. Coproduits et déchets alimentaires: un vivier pour l’élaboration de produits bio-sourcés. IAA 72, 24–27 (2021).

    Google Scholar 

  12. Strong, P. J. et al. Filamentous fungi for future functional food and feed. Curr. Opin. Biotechnol. 76, 102729 (2022).

    Article  CAS  PubMed  Google Scholar 

  13. Ritota, M. & Manzi, P. Pleurotus spp. cultivation on different agri-food by-products: example of biotechnological application. Sustainability 11, 5049 (2019).

    Article  CAS  Google Scholar 

  14. van Kuijk, S. J. A., Sonnenberg, A. S. M., Baars, J. J. P., Hendriks, W. H. & Cone, J. W. Fungal treated lignocellulosic biomass as ruminant feed ingredient: a review. Biotechnol. Adv. 33, 191–202 (2015).

    Article  PubMed  Google Scholar 

  15. Villas-Boas, S., Esposito, E. & Mitchell, D. Microbial conversion of lignocellulosic residues for production of animal feeds. Anim. Feed Sci. Technol. 98, 1–12 (2002).

    Article  CAS  Google Scholar 

  16. Ibarruri, J., Goiri, I., Cebrián, M. & García-Rodríguez, A. Solid state fermentation as a tool to stabilize and improve nutritive value of fruit and vegetable discards: effect on nutritional composition, in vitro ruminal fermentation and organic matter digestibility. Animals 11, 1653 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Espinosa-Páez, E. et al. Increasing antioxidant activity and protein digestibility in Phaseolus vulgaris and Avena sativa by fermentation with the Pleurotus ostreatus fungus. Molecules 22, 2275 (2017).

    Article  PubMed Central  Google Scholar 

  18. Granucci, N. Fruit Residues: Low Cost Substrates for Development of New Food Products (Univ. of Auckland, 2018).

  19. Stoffel, F. et al. Production of edible mycoprotein using agroindustrial wastes: influence on nutritional, chemical and biological properties. Innov. Food Sci. Emerg. Technol. 58, 102227 (2019).

    Article  CAS  Google Scholar 

  20. Mazac, R. et al. Incorporation of novel foods in European diets can reduce global warming potential, water use and land use by over 80%. Nat. Food 3, 286–293 (2022).

    Article  Google Scholar 

  21. Cottrell, R. S., Blanchard, J. L., Halpern, B. S., Metian, M. & Froehlich, H. E. Global adoption of novel aquaculture feeds could substantially reduce forage fish demand by 2030. Nat. Food 1, 301–308 (2020).

    Article  Google Scholar 

  22. Teigiserova, D. A., Hamelin, L. & Thomsen, M. Towards transparent valorization of food surplus, waste and loss: clarifying definitions, food waste hierarchy, and role in the circular economy. Sci. Total Environ. 706, 136033 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Caldeira, C. et al. Sustainability of food waste biorefinery: a review on valorisation pathways, techno-economic constraints, and environmental assessment. Bioresour. Technol. 312, 123575 (2020).

    Article  CAS  PubMed  Google Scholar 

  24. Escobar, N. & Laibach, N. Sustainability check for bio-based technologies: a review of process-based and life cycle approaches. Renew. Sust. Energy Rev. 135, 110213 (2021).

    Article  CAS  Google Scholar 

  25. Agreste: Infographics—Farming France (Ministère de l’Agriculture et de l’Alimentation, 2021); https://agriculture.gouv.fr/infographics-farming-france

  26. The French Approach to Circular Economy and Coherent Product Policies (United Nations Environment Programme, 2022); https://buildingcircularity.org/the-french-approach-to-circular-economy-and-coherent-product-policies/

  27. Villas-Boas, S. G. & Granucci, N. Process and composition for an improved flour product. US patent 20180146688A1 (2018).

  28. Dronne, Y. Les matières premières agricoles pour l’alimentation humaine et animale: l’UE et la France. INRA Prod. Anim. 31, 181–200 (2018).

    Article  Google Scholar 

  29. Rapport Grand Public 2021 (Haut Conseil pour le Climat, 2021).

  30. Un Mix de Gaz 100% Renouvelable en 2050? Etude de Faisabilité Technico-économique (ADEME, 2018).

  31. Dou, Z. et al. Proof of concept for developing novel feeds for cattle from wasted food and crop biomass to enhance agri-food system efficiency. Sci. Rep. 12, 13630 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  32. Karan, S. K. & Hamelin, L. Crop residues may be a key feedstock to bioeconomy but how reliable are current estimation methods? Resour. Conserv. Recycl. 164, 105211 (2021).

    Article  Google Scholar 

  33. Sevigné-Itoiz, E., Mwabonje, O., Panoutsou, C. & Woods, J. Life cycle assessment (LCA): informing the development of a sustainable circular bioeconomy? Phil. Trans. R. Soc. A 379, 20200352 (2021).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  34. Saxe, H., Hamelin, L., Hinrichsen, T. & Wenzel, H. Production of pig feed under future atmospheric CO2 concentrations: changes in crop content and chemical composition, land use, environmental impact, and socio-economic consequences. Sustainability 10, 3184 (2018).

    Article  CAS  Google Scholar 

  35. de Quelen, F., Brossard, L., Wilfart, A., Dourmad, J.-Y. & Garcia-Launay, F. Eco-friendly feed formulation and on-farm feed production as ways to reduce the environmental impacts of pig production without consequences on animal performance. Front. Vet. Sci. 8, 703 (2021).

    Article  Google Scholar 

  36. Garcia-Launay, F. et al. Multiobjective formulation is an effective method to reduce environmental impacts of livestock feeds. Br. J. Nutr. 120, 1298–1309 (2018).

    Article  CAS  PubMed  Google Scholar 

  37. Muñoz, I. Country-specific life cycle inventories for human excretion of food products. Int. J. Life Cycle Assess. 26, 1794–1804 (2021).

    Article  Google Scholar 

  38. Albizzati, P. F., Tonini, D. & Astrup, T. F. A quantitative sustainability assessment of food waste management in the European Union. Environ. Sci. Technol. 55, 16099–16109 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  39. Møller, H., Samsonstuen, S., Øverland, M., Modahl, I. S. & Olsen, H. F. Local non-food yeast protein in pig production—environmental impacts and land use efficiency. Livest. Sci. 104925 (2022).

  40. Guidance for the Development of Product Environmental Footprint Category Rules (PEFCRs), Version 6.3 (European Commission, 2017).

  41. King, L. J. in One Health (eds Atlas, R. M. & Maloy, S.) 1–15 (John Wiley & Sons, 2014).

  42. EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA). Guidance on the preparation and presentation of an application for authorisation of a novel food in the context of Regulation (EU) 2015/2283. EFSA J. 14, e04594 (2016).

  43. Grundy, E. A. C. et al. Interventions that influence animal-product consumption: a meta-review. Future Foods 5, 100111 (2022).

    Article  CAS  Google Scholar 

  44. van Selm, B. et al. Circularity in animal production requires a change in the EAT-Lancet diet in Europe. Nat. Food 3, 66–73 (2022).

    Article  Google Scholar 

  45. Zhou, S., Ma, F., Zhang, X. & Zhang, J. Carbohydrate changes during growth and fruiting in Pleurotus ostreatus. Fungal Biol. 120, 852–861 (2016).

    Article  CAS  PubMed  Google Scholar 

  46. Villas-Boas, S. G., Esposito, E. & de Mendonça, M. M. Bioconversion of apple pomace into a nutritionally enriched substrate by Candida utilis and Pleurotus ostreatus. World J. Microbiol. Biotechnol. 19, 461–467 (2003).

    Article  CAS  Google Scholar 

  47. Tallentire, C. W., Mackenzie, S. G. & Kyriazakis, I. Can novel ingredients replace soybeans and reduce the environmental burdens of European livestock systems in the future? J. Clean. Prod. 187, 338–347 (2018).

    Article  Google Scholar 

  48. Recoules, E. et al. L’autonomie protéique: état des lieux et voies d’amélioration pour l’alimentation des volailles. INRA Prod. Anim. 29, 129–140 (2016).

    Article  Google Scholar 

  49. Møller, J. et al. Fodermiddeltabel—Sammensætning og Foderværdi af Fodermidler til Kvæg—Forskning—Aarhus Universitet (Dansk, 2005).

  50. Tonini, D., Hamelin, L. & Astrup, T. F. Environmental implications of the use of agro-industrial residues for biorefineries: application of a deterministic model for indirect land-use changes. GCB Bioenergy 8, 690–706 (2016).

    Article  CAS  Google Scholar 

  51. Vural Gursel, I. et al. Comparative cradle-to-grave life cycle assessment of bio-based and petrochemical PET bottles. Sci. Total Environ. 793, 148642 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  52. FAOSTAT (FAO, 2019); http://www.fao.org/faostat/en/

  53. Donner, M. et al. Valorising olive waste and by-products in the Mediterranean region: a socio-economic perspective. In Proc. 8th International Conference on Sustainable Solid Waste Management (2021); https://thessaloniki2021.uest.gr/proceedings.html

  54. Tu, J. et al. Solid state fermentation by Fomitopsis pinicola improves physicochemical and functional properties of wheat bran and the bran-containing products. Food Chem. 328, 127046 (2020).

    Article  CAS  PubMed  Google Scholar 

  55. Lena, G. D., Patroni, E. & Quaglia, G. B. Improving the nutritional value of wheat bran by a white-rot fungus. Int. J. Food Sci. 32, 513–519 (1997).

    Article  Google Scholar 

  56. Zhang, F., Wang, T., Wang, X. & Lü, X. Apple pomace as a potential valuable resource for full-components utilization: a review. J. Clean. Prod. 329, 129676 (2021).

    Article  CAS  Google Scholar 

  57. Environmental Management: Life Cycle Assessment—Principles and Framework (International Organization for Standardization, 2006).

  58. Schaubroeck, T. et al. Attributional & consequential life cycle assessment: definitions, conceptual characteristics and modelling restrictions. Sustainability 13, 7386 (2021).

    Article  CAS  Google Scholar 

  59. van Zanten, H. H. E., Bikker, P., Meerburg, B. G. & de Boer, I. J. M. Attributional versus consequential life cycle assessment and feed optimization: alternative protein sources in pig diets. Int. J. Life Cycle Assess. 23, 1–11 (2018).

    Article  Google Scholar 

  60. Brandão, M., Martin, M., Cowie, A., Hamelin, L. & Zamagni, A. in Encyclopedia of Sustainable Technologies (ed. Abraham, M. A.) 277–284 (Elsevier, 2017).

  61. Moreno Ruiz, E. et al. Documentation of Changes Implemented in the Ecoinvent Database v3.7 & v3.7.1 (Ecoinvent Association, 2020).

  62. Bailey, R. & Wellesley, L. Chokepoints and Vulnerabilities in Global Food Trade (Chatham House, 2017).

  63. Steubing, B., de Koning, D., Haas, A. & Mutel, C. L. The Activity Browser—an open source LCA software building on top of the Brightway framework. Soft. Impacts 3, 100012 (2020).

    Article  Google Scholar 

  64. Tonini, D., Albizzati, P. F. & Astrup, T. F. Environmental impacts of food waste: learnings and challenges from a case study on UK. Waste Manage. 76, 744–766 (2018).

    Article  Google Scholar 

  65. Hamelin, L., Naroznova, I. & Wenzel, H. Environmental consequences of different carbon alternatives for increased manure-based biogas. Appl. Energy 114, 774–782 (2014).

    Article  CAS  Google Scholar 

  66. Bareha, Y., Affes, R., Moinard, V., Buffet, J. & Girault, R. A simple mass balance tool to predict carbon and nitrogen fluxes in anaerobic digestion systems. Waste Manage. 135, 47–59 (2021).

    Article  CAS  Google Scholar 

  67. Esnouf, A., Brockmann, D. & Cresson, R. Analyse du Cycle de Vie du Biométhane Issu de Ressources Agricoles—Rapport d’ACV (INRAE Transfert, 2021).

  68. Brockmann, D., Pradel, M. & Hélias, A. Agricultural use of organic residues in life cycle assessment: current practices and proposal for the computation of field emissions and of the nitrogen mineral fertilizer equivalent. Resour. Conserv. Recycl. 133, 50–62 (2018).

    Article  Google Scholar 

  69. Delin, S. Fertilizer value of phosphorus in different residues. Soil Use Manage. 32, 17–26 (2016).

    Article  Google Scholar 

  70. Tuszynska, A., Czerwionka, K. & Obarska-Pempkowiak, H. Phosphorus concentration and availability in raw organic waste and post fermentation products. J. Environ. Manage. 278, 111468 (2021).

    Article  CAS  PubMed  Google Scholar 

  71. Hergoualc’h, K. et al. in Agriculture, Forestry and Other Land Use Vol. 4 (eds Calvo Buendia, E. et al) Ch. 11 (IPCC, 2019).

  72. Gavrilova, O. et al. in Agriculture, Forestry and Other Land Use Vol. 4 (eds Calvo Buendia, E. et al) Ch. 10 (IPCC, 2019).

  73. Bisinella, V., Conradsen, K., Christensen, T. H. & Astrup, T. F. A global approach for sparse representation of uncertainty in life cycle assessments of waste management systems. Int. J. Life Cycle Assess. 21, 378–394 (2016).

    Article  Google Scholar 

  74. Clark, M. & Tilman, D. Comparative analysis of environmental impacts of agricultural production systems, agricultural input efficiency, and food choice. Environ. Res. Lett. 12, 064016 (2017).

    Article  ADS  Google Scholar 

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Acknowledgements

This work received funding from the French National Research Agency and the Occitania region under grant nos ANR-17-MGPA-0006 and 18015981 (U.J. and L.H.). Additional funding was provided by the Metaprogram GLOFOODS INRAE-CIRAD and by the French National Research Agency under grant no. ANR-18-EURE-0021 (U.J.). Financial assistance was provided by the France–Ecuador FSPI programme (E.A.R.D.). We thank S. Abbott for proofreading the manuscript. All the icons used in Figs. 1–3 and in the Supplementary Information are from www.flaticon.com and were made by Freepik, Good Ware, itim2101, wanicon, Icongek26, surang, Eucalyp, max.icons and Fliqqer.

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Authors and Affiliations

  1. TBI, Université de Toulouse, CNRS, INRAE, INSA, Toulouse, France

    U. Javourez & L. Hamelin

  2. Departamento de Procesos Químicos Alimentos y Biotecnología, Facultad de Ciencias Matemáticas, Físicas y Químicas, Universidad Técnica de Manabí, Portoviejo, Ecuador

    E. A. Rosero Delgado

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Contributions

U.J., E.A.R.D. and L.H. conceptualized the project and developed the methodology. U.J. and E.A.R.D. curated the data, conducted the formal analysis and carried out the investigation. L.H. acquired the funding, provided the resources, supervised the project and validated the results. U.J. visualized the results and wrote the original draft of the manuscript. E.A.R.D. and L.H. reviewed and edited the manuscript.

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Correspondence to U. Javourez.

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Javourez, U., Rosero Delgado, E.A. & Hamelin, L. Upgrading agrifood co-products via solid fermentation yields environmental benefits under specific conditions only. Nat Food 3, 911–920 (2022). https://doi.org/10.1038/s43016-022-00621-9

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