{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,30]],"date-time":"2026-01-30T06:35:28Z","timestamp":1769754928282,"version":"3.49.0"},"reference-count":45,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,12,3]],"date-time":"2019-12-03T00:00:00Z","timestamp":1575331200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,12,3]],"date-time":"2019-12-03T00:00:00Z","timestamp":1575331200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Many plants have medicinal properties due to substances known as phytochemicals. To utilize these plants in practice, numerous procedures, such as extraction, isolation and characterization methods and toxicology and bioactivity studies, must be designed and implemented. Integrated approach to process <jats:italic>Carpobrotus edulis<\/jats:italic>, a weed medicinal plant widely spread in Portugal, was developed into a closed loop of two processes: microwave assisted extraction (MAE) and activation (MAA), to produce both phytochemicals and biochar. The use of MAE for phytochemical extraction was shown to be more energy efficient than conventional Soxhlet extraction: the process time was decreased by 7\u20138 times, and the energy efficiency was increased by up to 97%. The yield of the extracts is of 27%. Qualitative and quantitative identification\/characterization of the phytochemicals were performed by LC-MS and phytochemical screening assays. The results clearly indicated that <jats:italic>Carpobrotus edulis<\/jats:italic> is rich by flavonoids (up to 24%). The use of MAA to process the residual biomass could shorten the activation time, resulting in reduced energy consumption. Biochar with a high yield of 65% (on a biomass basis) and a well-developed texture (surface area of 68.9\u2009m<jats:sup>2<\/jats:sup>\/g; total pore volume of 0.10\u2009cm<jats:sup>3<\/jats:sup>\/g; micropore volume of 0.07\u2009cm<jats:sup>3<\/jats:sup>\/g) is obtained.<\/jats:p>","DOI":"10.1038\/s41598-019-53817-8","type":"journal-article","created":{"date-parts":[[2019,12,3]],"date-time":"2019-12-03T11:04:18Z","timestamp":1575371058000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Integrated Green Chemical Approach to the Medicinal Plant Carpobrotus edulis Processing"],"prefix":"10.1038","volume":"9","author":[{"given":"Sergiy","family":"Lyubchyk","sequence":"first","affiliation":[]},{"given":"Olesia","family":"Shapovalova","sequence":"additional","affiliation":[]},{"given":"Olena","family":"Lygina","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3068-4920","authenticated-orcid":false,"given":"Maria Concei\u00e7ao","family":"Oliveira","sequence":"additional","affiliation":[]},{"given":"Nurbol","family":"Appazov","sequence":"additional","affiliation":[]},{"given":"Andriy","family":"Lyubchyk","sequence":"additional","affiliation":[]},{"given":"Adilia Januario","family":"Charmier","sequence":"additional","affiliation":[]},{"given":"Svetlana","family":"Lyubchik","sequence":"additional","affiliation":[]},{"given":"Armando J. L.","family":"Pombeiro","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2019,12,3]]},"reference":[{"key":"53817_CR1","unstructured":"Research and Markets. Europe phytochemicals and plant extracts market by applications - analysis and forecast to 2019. http:\/\/www.researchandmarkets.com\/research\/x6lww9\/europe (2015)."},{"key":"53817_CR2","unstructured":"World Health Organisation (WHO), World Conservation Union (IUCN) & World Wide Fund for Nature (WWF). Guidelines on the Conservation of Medicinal Plants. (WHO\/IUCN\/WWF, 1993)."},{"key":"53817_CR3","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1111\/j.1472-4642.2008.00503.x","volume":"14","author":"M Vil\u00e0","year":"2008","unstructured":"Vil\u00e0, M. et al. Widespread resistance of Mediterranean island ecosystems to the establishment of three alien species. Divers. Distrib. 14, 839\u2013851 (2008).","journal-title":"Divers. Distrib."},{"key":"53817_CR4","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1111\/j.1365-294X.2005.02417.x","volume":"14","author":"KA Schierenbeck","year":"2005","unstructured":"Schierenbeck, K. A., Symonds, V. V., Gallagher, K. G. & Bell, J. Genetic variation and phylogeographic analyses of two species of Carpobrotus and their hybrids in California. Mol. Ecol. 14, 539\u2013547 (2005).","journal-title":"Mol. Ecol."},{"key":"53817_CR5","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1016\/S2221-6189(14)60022-6","volume":"3","author":"N Tamilselvan","year":"2014","unstructured":"Tamilselvan, N., Thirumalai, T., Shyamala, P. & David, E. A review on some poisonous plants and their medicinal values. Journal of Acute Disease 3, 85\u201389 (2014).","journal-title":"Journal of Acute Disease"},{"key":"53817_CR6","doi-asserted-by":"publisher","first-page":"438","DOI":"10.1016\/j.ijantimicag.2011.01.016","volume":"37","author":"A Martins","year":"2011","unstructured":"Martins, A. et al. Antibacterial properties of compounds isolated from Carpobrotus edulis. Int. J. Antimicrob. Agents 37, 438\u2013444 (2011).","journal-title":"Int. J. Antimicrob. Agents"},{"key":"53817_CR7","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/S0378-8741(01)00197-0","volume":"76","author":"E van der Watt","year":"2001","unstructured":"van der Watt, E. & Pretorius, J. C. Purification and identification of active antibacterial components in Carpobrotus edulis L. J. Ethnopharmacol. 76, 87\u201391 (2001).","journal-title":"J. Ethnopharmacol."},{"key":"53817_CR8","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1016\/j.fitote.2004.09.020","volume":"76","author":"M Martins","year":"2005","unstructured":"Martins, M. et al. Inhibition of the Carpobrotus edulis methanol extract on the growth of phagocytosed multidrug-resistant Mycobacterium tuberculosis and methicillin-resistant Staphylococcus aureus. Fitoterapia 76, 96\u201399 (2005).","journal-title":"Fitoterapia"},{"key":"53817_CR9","doi-asserted-by":"crossref","unstructured":"Xu, Z. & Howard, L. R. Analysis of antioxidant-rich phytochemicals (John Wiley & Sons, 2012).","DOI":"10.1002\/9781118229378"},{"key":"53817_CR10","doi-asserted-by":"publisher","first-page":"400","DOI":"10.2533\/chimia.2011.400","volume":"65","author":"JL Wolfender","year":"2011","unstructured":"Wolfender, J. L., Eugster, P. J., Bohni, N. & Cuendet, M. Advanced methods for natural product drug discovery in the field of nutraceuticals. Chimia (Aarau) 65, 400\u2013406 (2011).","journal-title":"Chimia (Aarau)"},{"key":"53817_CR11","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1186\/1475-2891-3-5","volume":"3","author":"J Boyer","year":"2004","unstructured":"Boyer, J. & Liu, R. H. Apple phytochemicals and their health benefits. Nutr. J. 3, 5\u20135 (2004).","journal-title":"Nutr. J."},{"key":"53817_CR12","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1186\/1472-6882-12-215","volume":"12","author":"BE Omoruyi","year":"2012","unstructured":"Omoruyi, B. E., Bradley, G. & Afolayan, A. J. Antioxidant and phytochemical properties of Carpobrotus edulis (L.) bolus leaf used for the management of common infections in HIV\/AIDS patients in Eastern Cape Province. BMC Complement. Altern. Med. 12, 215 (2012).","journal-title":"BMC Complement. Altern. Med."},{"key":"53817_CR13","first-page":"1","volume":"8","author":"S Sasidharan","year":"2011","unstructured":"Sasidharan, S., Chen, Y., Saravanan, D., Sundram, K. M. & Latha, L. Y. Extraction, isolation and characterization of bioactive compounds from plants\u2019 extracts. Afr. J. Tradit. Complement. Altern. Med. 8, 1\u201310 (2011).","journal-title":"Afr. J. Tradit. Complement. Altern. Med."},{"key":"53817_CR14","doi-asserted-by":"crossref","unstructured":"Gang, D. R. Phytochemicals, plant growth, and the environment (Springer Science & Business Media, 2012).","DOI":"10.1007\/978-1-4614-4066-6"},{"key":"53817_CR15","doi-asserted-by":"publisher","first-page":"1154","DOI":"10.1126\/science.3890182","volume":"228","author":"MF Balandrin","year":"1985","unstructured":"Balandrin, M. F., Klocke, J. A., Wurtele, E. S. & Bollinger, W. H. Natural plant chemicals: sources of industrial and medicinal materials. Science 228, 1154\u20131160 (1985).","journal-title":"Science"},{"key":"53817_CR16","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1016\/j.jfoodeng.2013.01.014","volume":"117","author":"J Azmir","year":"2013","unstructured":"Azmir, J. et al. Techniques for extraction of bioactive compounds from plant materials: a review. J. Food. Eng. 117, 426\u2013436 (2013).","journal-title":"J. Food. Eng."},{"key":"53817_CR17","first-page":"2167","volume":"4","author":"N Azwanida","year":"2015","unstructured":"Azwanida, N. A review on the extraction methods use in medicinal plants, principle, strength and limitation. Med. Aromat. Plants 4, 2167\u20130412.1000196 (2015).","journal-title":"Med. Aromat. Plants"},{"key":"53817_CR18","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1016\/j.jclepro.2015.09.067","volume":"112","author":"J Moncada","year":"2016","unstructured":"Moncada, J., Tamayo, J. A. & Cardona, C. A. Techno-economic and environmental assessment of essential oil extraction from Oregano (Origanum vulgare) and Rosemary (Rosmarinus officinalis) in Colombia. J. Clean. Prod. 112, 172\u2013181 (2016).","journal-title":"J. Clean. Prod."},{"key":"53817_CR19","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1614\/WT-D-12-00109.1","volume":"27","author":"KN Harker","year":"2013","unstructured":"Harker, K. N. & O\u2019Donovan, J. T. Recent weed control, weed management, and integrated weed management. Weed Technol. 27, 1\u201311 (2013).","journal-title":"Weed Technol."},{"key":"53817_CR20","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1016\/j.indcrop.2013.05.019","volume":"49","author":"GFL Koay","year":"2013","unstructured":"Koay, G. F. L., Chuah, T.-G. & Choong, T. S. Y. Economic feasibility assessment of one and two stages dry fractionation of palm kernel oil. Ind. Crops Prod. 49, 437\u2013444 (2013).","journal-title":"Ind. Crops Prod."},{"key":"53817_CR21","doi-asserted-by":"crossref","unstructured":"Strezov, V. & Evans, T. J. Biomass processing technologies (CRC Press, 2014).","DOI":"10.1201\/b17093"},{"key":"53817_CR22","doi-asserted-by":"publisher","first-page":"1126","DOI":"10.1016\/j.rser.2015.12.185","volume":"57","author":"T Kan","year":"2016","unstructured":"Kan, T., Strezov, V. & Evans, T. J. Lignocellulosic biomass pyrolysis: a review of product properties and effects of pyrolysis parameters. Renewable and Sustainable Energy Reviews 57, 1126\u20131140 (2016).","journal-title":"Renewable and Sustainable Energy Reviews"},{"key":"53817_CR23","unstructured":"Anastas, P. T. & Warner, J. C. Green chemistry: theory and practice (Oxford University Press, 1998)."},{"key":"53817_CR24","doi-asserted-by":"publisher","DOI":"10.1093\/database\/bat070","author":"JA Rothwell","year":"2015","unstructured":"Rothwell, J. A. et al. Phenol-Explorer 3.6: a major update of the Phenol-Explorer database to incorporate data on the effects of food processing on polyphenol content. Database. https:\/\/doi.org\/10.1093\/database\/bat070 (2015).","journal-title":"Database"},{"key":"53817_CR25","doi-asserted-by":"publisher","first-page":"9387","DOI":"10.1021\/jf501011y","volume":"62","author":"LZ Lin","year":"2014","unstructured":"Lin, L. Z., Sun, J., Chen, P., Monagas, M. J. & Harnly, J. M. UHPLC-PDA-ESI\/HRMSn profiling method to identify and quantify oligomeric proanthocyanidins in plant products. J. Agric. Food Chem. 62, 9387\u20139400 (2014).","journal-title":"J. Agric. Food Chem."},{"key":"53817_CR26","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.chroma.2006.06.026","volume":"1128","author":"B Sun","year":"2006","unstructured":"Sun, B., Leandro, M. C., de Freitas, V. & Spranger, M. I. Fractionation of red wine polyphenols by solid-phase extraction and liquid chromatography. J. Chromatogr. A 1128, 27\u201338 (2006).","journal-title":"J. Chromatogr. A"},{"key":"53817_CR27","doi-asserted-by":"publisher","first-page":"848","DOI":"10.1016\/j.foodres.2012.07.001","volume":"48","author":"II Rockenbach","year":"2012","unstructured":"Rockenbach, I. I. et al. Characterization of flavan-3-ols in seeds of grape pomace by CE, HPLC-DAD-MSn and LC-ESI-FTICR-MS. Food Res. Int. 48, 848\u2013855 (2012).","journal-title":"Food Res. Int."},{"key":"53817_CR28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/mas.20212","volume":"29","author":"V Vukics","year":"2010","unstructured":"Vukics, V. & Guttman, A. Structural characterization of flavonoid glycosides by multi-stage mass spectrometry. Mass Spectrom. Rev. 29, 1\u201316 (2010).","journal-title":"Mass Spectrom. Rev."},{"key":"53817_CR29","doi-asserted-by":"publisher","first-page":"108","DOI":"10.17221\/122\/2009-CJFS","volume":"28","author":"W Cai","year":"2010","unstructured":"Cai, W., Gu, X. & TaNG, J. Extraction, purification, and characterisation of the flavonoids from Opuntia milpa alta skin. Czech J. Food Sci. 28, 108\u2013116 (2010).","journal-title":"Czech J. Food Sci."},{"key":"53817_CR30","doi-asserted-by":"publisher","first-page":"2183","DOI":"10.1111\/ijfs.12857","volume":"50","author":"F Fu","year":"2015","unstructured":"Fu, F. & Wang, H. L. Metabolomics reveals consistency of the shoot system in Medicago truncatula by HPLC-UV-ESI-MS\/MS. Int. J. Food Sci. Technol. 50, 2183\u20132192 (2015).","journal-title":"Int. J. Food Sci. Technol."},{"key":"53817_CR31","doi-asserted-by":"crossref","unstructured":"Menaa, F. & Tr\u00e9ton, C. H. Polyphenols in chronic diseases and their mechanisms of action in Polyphenols in human health and disease (eds Watson, R. R., Preedy, V. R., & Zibadi, S.) 819-830 (Elsevier\/Academic Press, 2014).","DOI":"10.1016\/B978-0-12-398456-2.00063-3"},{"key":"53817_CR32","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/j.jaap.2012.11.015","volume":"100","author":"O Ma\u0161ek","year":"2013","unstructured":"Ma\u0161ek, O. et al. Microwave and slow pyrolysis biochar\u2014Comparison of physical and functional properties. J. Anal. Appl. Pyrolysis 100, 41\u201348 (2013).","journal-title":"J. Anal. Appl. Pyrolysis"},{"key":"53817_CR33","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1111\/gcbb.12018","volume":"5","author":"F Ronsse","year":"2013","unstructured":"Ronsse, F., van Hecke, S., Dickinson, D. & Prins, W. Production and characterization of slow pyrolysis biochar: influence of feedstock type and pyrolysis conditions. Glob. Change Biol. Bioenergy 5, 104\u2013115 (2013).","journal-title":"Glob. Change Biol. Bioenergy"},{"key":"53817_CR34","first-page":"393","volume":"30","author":"J Wannapeera","year":"2008","unstructured":"Wannapeera, J., Worasuwannarak, N. & Pipatmanomai, S. Product yields and characteristics of rice husk, rice straw and corncob during fast pyrolysis in a drop-tube\/fixed-bed reactor. Songklanakarin Journal of Science & Technology 30, 393\u2013404 (2008).","journal-title":"Songklanakarin Journal of Science & Technology"},{"key":"53817_CR35","doi-asserted-by":"publisher","first-page":"15","DOI":"10.18052\/www.scipress.com\/ILCPA.47.15","volume":"47","author":"M Elsayed","year":"2015","unstructured":"Elsayed, M. & Zalat, O. Factor affecting microwave assisted preparation of activated carbon from local raw materials. International Letters of Chemistry, Physics and Astronomy 47, 15\u201323 (2015).","journal-title":"International Letters of Chemistry, Physics and Astronomy"},{"key":"53817_CR36","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1002\/bbb.254","volume":"5","author":"TR Brown","year":"2011","unstructured":"Brown, T. R., Wright, M. M. & Brown, R. C. Estimating profitability of two biochar production scenarios: slow pyrolysis vs fast pyrolysis. Biofuel. Bioprod. Biorefin. 5, 54\u201368 (2011).","journal-title":"Biofuel. Bioprod. Biorefin."},{"key":"53817_CR37","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1007\/BF01049915","volume":"5","author":"B Domon","year":"1988","unstructured":"Domon, B. & Costello, C. E. A systematic nomenclature for carbohydrate fragmentations in FAB-MS\/MS spectra of glycoconjugates. Glycoconj. J. 5, 397\u2013409 (1988).","journal-title":"Glycoconj. J."},{"key":"53817_CR38","doi-asserted-by":"publisher","first-page":"406","DOI":"10.1002\/bms.1200230705","volume":"23","author":"QM Li","year":"1994","unstructured":"Li, Q. M. & Claeys, M. Characterization and differentiation of diglycosyl flavonoids by positive ion fast atom bombardment and tandem mass spectrometry. Biol Mass Spectrom 23, 406\u2013416 (1994).","journal-title":"Biol Mass Spectrom"},{"key":"53817_CR39","doi-asserted-by":"publisher","first-page":"666","DOI":"10.4103\/0250-474X.100242","volume":"73","author":"R Madaan","year":"2011","unstructured":"Madaan, R., Bansal, G., Kumar, S. & Sharma, A. Estimation of Total Phenols and Flavonoids in Extracts of Actaea spicata Roots and Antioxidant Activity Studies. Indian J. Pharm. Sci. 73, 666\u2013669 (2011).","journal-title":"Indian J. Pharm. Sci."},{"key":"53817_CR40","first-page":"178","volume":"10","author":"C-C Chang","year":"2002","unstructured":"Chang, C.-C., Yang, M.-H., Wen, H.-M. & Chern, J.-C. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J. Food Drug Anal. 10, 178\u2013182 (2002).","journal-title":"J. Food Drug Anal."},{"key":"53817_CR41","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1021\/ja01269a023","volume":"60","author":"S Brunauer","year":"1938","unstructured":"Brunauer, S., Emmett, P. H. & Teller, E. Adsorption of gases in multimolecular layers. J. Am. Chem. Soc. 60, 309\u2013319 (1938).","journal-title":"J. Am. Chem. Soc."},{"key":"53817_CR42","first-page":"331","volume":"55","author":"MM Dubinin","year":"1947","unstructured":"Dubinin, M. M. & Radushkevich, L. V. Equation of the characteristic curve of activated charcoal. Proc. Acad. Sci. USSR Phys. Chem. Sect. 55, 331 (1947).","journal-title":"Proc. Acad. Sci. USSR Phys. Chem. Sect."},{"key":"53817_CR43","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1021\/ja01145a126","volume":"73","author":"EP Barrett","year":"1951","unstructured":"Barrett, E. P., Joyner, L. G. & Halenda, P. P. The determination of pore volume and area distributions in porous substances. I. Computations from nitrogen isotherms. J. Am. Chem. Soc. 73, 373\u2013380 (1951).","journal-title":"J. Am. Chem. Soc."},{"key":"53817_CR44","unstructured":"Sontheimer, H., Crittenden, J. C. & Summers, R. S. Activated carbon for water treatment. (DVGW-Forschungsstelle, 1988)."},{"key":"53817_CR45","unstructured":"http:\/\/www.ico.org\/proChects\/Good-Hygiene-Practices\/cnt\/cnt_sp\/sec_3\/docs_3.2\/Determine%20m%20c.pdf."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-53817-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-53817-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-53817-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,17]],"date-time":"2022-12-17T16:56:48Z","timestamp":1671296208000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-53817-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,3]]},"references-count":45,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["53817"],"URL":"https:\/\/doi.org\/10.1038\/s41598-019-53817-8","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,3]]},"assertion":[{"value":"20 February 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 November 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 December 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"18171"}}