Journal of Food Measurement and Characterization

, Volume 13, Issue 3, pp 1661–1673 | Cite as

Enhancing bio-recovery of bioactive compounds extracted from Citrus medica L. Var. sarcodactylis: optimization performance of integrated of pulsed-ultrasonic/microwave technique

  • Amer Ali Mahdi
  • Marwan M. A. Rashed
  • Waleed Al-Ansi
  • Mohamed Ismael Ahmed
  • Mohammed Obadi
  • Qi Jiang
  • Husnain Raza
  • Hongxin WangEmail author
Original Paper


This study mainly aimed to optimize a sustainable and green process for extracting bioactive compounds from Foshou fruit by using an integrated technique based on ultrasonic-microwave assisted extraction (UMAE). Response surface methodology (RSM) based on a Box–Behnken design was applied to determine optimal conditions. The following optimized UMAE processing parameters were obtained: sonication time (96.13 s), microwave power (305.28 W), and solid/solvent ratio (1:37). Based on a total phenolic compound extraction yield of 9.21 mg gallic acid (GA) equ/g dry weight (DW), a 2,2-diphenyl-1-picrylhydrazyl (DPPH) scavenging activity with a half maximal inhibitory concentration (IC50) of 27.52 μg GA equ, and an antioxidant capacity detected by 2,2′-azino-bis-3-ethylbenzthiazoline-6-sulphonic acid (ABTS) assay of 8.79 mg trolox equ/g DW. The optimized UMAE extract was superior to those obtained using microwave-assisted extraction (MAE) or conventional solvent extraction (CSE) methods. Scanning electron microscopy (SEM) analysis showed that the three extraction methods affected the sample tissue microstructure. Among them, UMAE caused the most marked structural disruption. UPLC-PDA-Q-TOF-MS analysis identified 67 phenolic compounds in the optimized UMAE extract of the Foshou fruit extract. This study indicated that the integrated UMAE technique is a suitable and safe technique to enhance the qualitative and quantitative extraction of phenolic compounds from Foshou fruit. These phenolic compounds can be used as a functional food ingredient in industrial production.

Graphical abstract


Citrus medica L. var. sarcodactylis Swingle Ultrasonic/microwave-assisted extraction Response surface methodology Green extraction Antioxidant UPLC-PDA-Q-TOF-MS 



This research was financially supported by the China Scholarship Council (CSC), Beijing, China and carried out in the Laboratory of the National Engineering Research Center for Functional Food at Jiangnan University, Wuxi, China.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


  1. 1.
    C. Ramadugu, M.L. Keremane, X. Hu, D. Karp, C.T. Federici, T. Kahn, M.L. Roose, R.F. Lee, Sci. Hortic. 195, 124–137 (2015)CrossRefGoogle Scholar
  2. 2.
    Z. Wu, H. Li, Y. Yang, Y. Zhan, D. Tu, Ind. Crops Prod. 46, 311–316 (2013)CrossRefGoogle Scholar
  3. 3.
    F. Shahidi, P. Ambigaipalan, J. Funct. Foods 18, 820–897 (2015)CrossRefGoogle Scholar
  4. 4.
    M.M. Özcan, S. Doğu, N. Uslu, J. Food Meas. Charact. 12, 902–905 (2018)CrossRefGoogle Scholar
  5. 5.
    L. Shen, H.F. Ji, H.Y. Zhang, Biochem. Biophys. Res. Commun. 362, 543–545 (2007)CrossRefGoogle Scholar
  6. 6.
    K. Ameer, H.M. Shahbaz, J.H. Kwon, Compr. Rev. Food Sci. Food Saf. 16, 295–315 (2017)CrossRefGoogle Scholar
  7. 7.
    M.L. Luna-Guevara, J.J. Luna-Guevara, P. Hernández-Carranza, H. Ruíz-Espinosa, C.E. Ochoa-Velasco, In: Studies in Natural Products Chemistry, ed. By A. Rahman (Elsevier B.V., 2018) p. 79Google Scholar
  8. 8.
    M. Plaza, C. Turner, Trends Anal. Chem. 76, 39–54 (2015)CrossRefGoogle Scholar
  9. 9.
    B.K. Tiwari, Trends Anal. Chem. 71, 100–109 (2015)CrossRefGoogle Scholar
  10. 10.
    S. Armenta, S. Garrigues, M. de la Guardia, TrAC, Trends Anal. Chem. 71, 2–8 (2015)CrossRefGoogle Scholar
  11. 11.
    F. Chemat, N. Rombaut, A.G. Sicaire, A. Meullemiestre, A.S. Fabiano-Tixier, M. Abert-Vian, Ultrason. Sonochem. 34, 540–560 (2017)CrossRefGoogle Scholar
  12. 12.
    Y. Liu, S. Wei, M. Wu, S. Yang, J. Food Meas. Charact. 12, 967–973 (2018)CrossRefGoogle Scholar
  13. 13.
    J. Azmir, I. Zaidul, M. Rahman, K. Sharif, A. Mohamed, F. Sahena, M. Jahurul, K. Ghafoor, N. Norulaini, A. Omar, J. Food Eng. 117, 426–436 (2013)CrossRefGoogle Scholar
  14. 14.
    H.K. Kala, R. Mehta, K.K. Sen, R. Tandey, V. Mandal, Trends Anal. Chem. 85, 140–152 (2016)CrossRefGoogle Scholar
  15. 15.
    S. Prabakaran, L. Ramu, S. Veerappan, B. Pemiah, N. Kannappan, J. Food Meas. Charact. 11, 1531–1541 (2017)CrossRefGoogle Scholar
  16. 16.
    J. Płotka-Wasylka, M. Rutkowska, K. Owczarek, M. Tobiszewski, J. Namieśnik, Trends Anal. Chem. 91, 12–25 (2017)CrossRefGoogle Scholar
  17. 17.
    G. Brunner, J. Supercrit. Fluid 47, 373–381 (2009)CrossRefGoogle Scholar
  18. 18.
    G. Astray, B. Gullón, J. Labidi, P. Gullón, Ind. Crops Prod. 92, 290–299 (2016)CrossRefGoogle Scholar
  19. 19.
    S. Nag, N. Sit, J. Food Meas. Charact. 12, 1734–1743 (2018)CrossRefGoogle Scholar
  20. 20.
    J.L. Pilkington, C. Preston, R.L. Gomes, Ind. Crops Prod. 58, 15–24 (2014)CrossRefGoogle Scholar
  21. 21.
    P. Lucci, J. Saurina, O. Núñez, TrAC, Trends Anal. Chem. 88, 1–24 (2017)CrossRefGoogle Scholar
  22. 22.
    A. Kaufmann, TrAC, Trends Anal. Chem. 63, 113–128 (2014)CrossRefGoogle Scholar
  23. 23.
    F. Dahmoune, L. Boulekbache, K. Moussi, O. Aoun, G. Spigno, K. Madani, Ind. Crops Prod. 50, 77–87 (2013)CrossRefGoogle Scholar
  24. 24.
    G. Spigno, L. Tramelli, D.M. De Faveri, J. Food Eng. 81, 200–208 (2007)CrossRefGoogle Scholar
  25. 25.
    M.A. Bezerra, R.E. Santelli, E.P. Oliveira, L.S. Villar, L.A. Escaleira, Talanta 76, 965–977 (2008)CrossRefGoogle Scholar
  26. 26.
    G.L. Chen, S.G. Chen, Y.Y. Zhao, C.X. Luo, J. Li, Y.Q. Gao, Ind. Crops Prod. 57, 150–157 (2014)CrossRefGoogle Scholar
  27. 27.
    M.M. Rashed, Q. Tong, M.H. Abdelhai, M.A. Gasmalla, J.B. Ndayishimiye, L. Chen, F. Ren, Ultrason. Sonochem. 29, 39–47 (2016)CrossRefGoogle Scholar
  28. 28.
    M.M. Rashed, Q. Tong, A. Nagi, J. Li, N.U. Khan, L. Chen, A. Rotail, A.M. Bakry, Ind. Crops Prod. 100, 236–245 (2017)CrossRefGoogle Scholar
  29. 29.
    L. Zhang, Z.C. Tu, H. Wang, Z.F. Fu, Q.H. Wen, H.X. Chang, X.Q. Huang, Food Res. Int. 70, 101–109 (2015)CrossRefGoogle Scholar
  30. 30.
    W. He, M. Zeng, J. Chen, Y. Jiao, F. Niu, G. Tao, S. Zhang, F. Qin, Z. He, J. Agric. Food Chem. 64, 171–177 (2015)CrossRefGoogle Scholar
  31. 31.
    European Molecular Biology Laboratory European Bioinformatics Institute. Accessed 25 Feb 2017
  32. 32.
    Royal Society of Chemistry ChemSpider. Accessed 25 Feb 2017
  33. 33.
    C. Proestos, M. Komaitis, LWT Food Sci. Technol. 41, 652–659 (2008)CrossRefGoogle Scholar
  34. 34.
    H. Liu, N. Qiu, H. Ding, R. Yao, Food Res. Int. 41, 363–370 (2008)CrossRefGoogle Scholar
  35. 35.
    G. Jayaprakasha, B.S. Patil, Food Chem. 101, 410–418 (2007)CrossRefGoogle Scholar
  36. 36.
    S. Castillo, J. Dávila-Aviña, N. Heredia, S. Garcia, Food Sci. Biotechnol. 26, 453–459 (2017)CrossRefGoogle Scholar
  37. 37.
    Y. Sun, L. Qiao, Y. Shen, P. Jiang, J. Chen, X. Ye, J. Food Sci. 78, 37–42 (2013)CrossRefGoogle Scholar
  38. 38.
    F. Menichini, R. Tundis, M.R. Loizzo, M. Bonesi, D. D’Angelo, P. Lombardi, V. Mastellone, J. Enzyme Inhib. Med. Chem. 31, 1270–1276 (2016)CrossRefGoogle Scholar
  39. 39.
    B. Orlikova, D. Tasdemir, F. Golais, M. Dicato, M. Diederich, Biochem. Pharmacol. 82, 620–631 (2011)CrossRefGoogle Scholar
  40. 40.
    A.S. Wilkinson, M.W. Taing, J.T. Pierson, C.N. Lin, R.G. Dietzgen, P.N. Shaw, M.J. Gidley, G.R. Monteith, S.J. Robertsthomson, Food Funct. 6, 1847–1854 (2015)CrossRefGoogle Scholar
  41. 41.
    L.Y. Tian, X. Bai, X.H. Chen, J.B. Fang, S.H. Liu, J.C. Chen, Phytomedicine 17, 533–539 (2010)CrossRefGoogle Scholar
  42. 42.
    L.P. Qiu, K.P. Chen, Fitoterapia 84, 140–157 (2013)CrossRefGoogle Scholar
  43. 43.
    M.M. Salem, K.A. Werbovetz, J. Nat. Prod. 68, 108–111 (2005)CrossRefGoogle Scholar
  44. 44.
    P. Kittakoop, S. Nopichai, N. Thongon, P. Charoenchai, Y. Thebtaranonth, Helv. Chim. Acta 87, 175–179 (2004)CrossRefGoogle Scholar
  45. 45.
    M. Feldman, S. Tanabe, F. Epifano, S. Genovese, M. Curini, D. Grenier, J. Nat. Prod. 74, 26–31 (2011)CrossRefGoogle Scholar
  46. 46.
    S.F. Wu, F.R. Chang, S.Y. Wang, T.L. Hwang, C.L. Lee, S.L. Chen, C.C. Wu, Y.C. Wu, J. Nat. Prod. 74, 989–996 (2011)CrossRefGoogle Scholar
  47. 47.
    L. Cui, P.T. Thuong, H.S. Lee, D. Njamen, J.T. Mbafor, Z.T. Fomum, J. Lee, Y.H. Kim, W.K. Oh, Planta Med. 74, 422–426 (2008)CrossRefGoogle Scholar
  48. 48.
    Y.C. Shen, L.T. Wang, A.T. Khalil, L.C. Chiang, P.W. Cheng, Chem. Pharm. Bull. 36, 244–247 (2005)CrossRefGoogle Scholar
  49. 49.
    I. Chihiro, I. Masataka, M. Yoshitaka, C.F. Valdir, M. Teruo, T. Harukuni, N. Hoyoku, F. Hiroshi, J. Nat. Prod. 65, 267–272 (2002)CrossRefGoogle Scholar
  50. 50.
    R. Jiang, J.R. Zhou, P.M. Hon, S.L. Li, Y. Zhou, L.L. Li, W. Ye, H. Xu, P. Shaw, P.P. But, J. Nat. Prod. 70, 283–286 (2007)CrossRefGoogle Scholar
  51. 51.
    Q.M. Xu, Z.M. Zou, L.Z. Xu, S.L. Yang, Chem. Pharm. Bull. 53, 826–828 (2005)CrossRefGoogle Scholar
  52. 52.
    T. Rukachaisirikul, A. Saekee, C. Tharibun, S. Watkuolham, A. Suksamrarn, Arch. Pharmacal Res. 30, 1398–1403 (2007)CrossRefGoogle Scholar
  53. 53.
    M.M. Rashed, A.D. Ghaleb, J. Li, A. Nagi, Y. Hua-wei, Z. Wen-you, Q. Tong, ACS Sustain. Chem. Eng. 6, 1639–1649 (2018)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Food Science and Technology, School of Food Science and TechnologyJiangnan UniversityWuxiChina
  2. 2.National Engineering Research Center for Functional FoodJiangnan UniversityWuxiChina
  3. 3.Department of Food Science and Technology, Faculty of AgricultureSana’a UniversitySana’aYemen
  4. 4.Solid-State Fermentation Resource Utilization Key Laboratory of Sichuan Province, College of Life Science & Food EngineeringYibin UniversityYibinChina
  5. 5.Department of Food Science and TechnologyNyala Technical College South DarfurNyalaSudan

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