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The in vitro antimicrobial activity assessment of ultrasound assisted Lycium barbarum fruit extracts and pomegranate fruit peels

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Abstract

The present study aimed at assessing the antimicrobial properties of a water and ethanol ultrasound-assisted extraction (UAE) of dry goji berries and of lyophilised powdered pomegranate peel in vitro. Minimum inhibitory concentration (MIC) and minimal bactericidal concentration (MBC) methods, turbidity (cell density) measurement, and well diffusion assay were used to determine the antimicrobial activity against several species of foodborne bacteria (Gram – , Escherichia coli, Salmonella typhimurium, Campylobacter jejuni), (Gram + Staphylococcus aureus, Listeria monocytogenes, Clostridium perfringens), yeasts (Yarrowia lipolytica, Metschnikowia fructicola, and Rhodotorula mucilaginosa), and fungi (Penicillium expansum, Aspergillus niger, Fusarium oxysporum, and Rhizoctonia solani). Carbohydrate and phenolic contents were measured, and DPPH (2,2-diphenyl-1-picrylhydrazyl) and ABTS (2,2΄-Azino-bis-(3-ethyl-benzthiazoline-sulphonic acid)) radical scavenging assays were used for the assessment of antioxidant activity. Fourier transform infrared (FTIR) spectrums of all samples were also evaluated in order to determine their chemical profiles. The lyophilised pomegranate peel exhibited the highest antioxidant, antimicrobial, and antifungal activity among all samples, while among the goji berry samples-who had only antibacterial and very little or no antifungal activity—the lyophilised aqueous extract with the lowest content of maltodextrin (2%) and highest phenolic content, had also the highest antioxidant, antimicrobial, and antifungal activity. The antioxidant and antimicrobial bioactivities seemed to be related to the content of polyphenols, the low concentration of maltodextrin in the encapsulated lyophilised samples and the use of optimised ultrasound assisted extraction. Minimum inhibitory concentration or zones of inhibition were in many (but not all) cases lower for the aqueous extracts compared to the ethanol or ethanol/hexane extracts of goji berries. In conclusion, the lyophilized powder of pomegranate peels and the aqueous extracts of goji berries encapsulated with minimal maltodextrin content and high polyphenol content exhibited high antioxidant and antimicrobial activity which could be utilized in food preservation or plant protection.

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References

  1. S. Leontopoulos, K. Petrotos, V. Anatolioti, P. Skenderidis, S. Tsilfoglou, I. Vagelas, Int. J. Food Biosyst. Eng. 6, 23 (2017)

    Google Scholar 

  2. P. Skenderidis, E. Kerasioti, E. Karkanta, D. Stagos, D. Kouretas, K. Petrotos, C. Hadjichristodoulou, A. Tsakalof, Toxicol. Rep. 5, 251–257 (2018)

    Article  Google Scholar 

  3. M. Protti, I. Gualandi, R. Mandrioli, S. Zappoli, D. Tonelli, L. Mercolini, J. Pharm. Biomed. Anal. 143, 252 (2017)

    Article  CAS  Google Scholar 

  4. C.N. Aguilar, A. Aguilera-Carbo, A. Robledo, J. Ventura, R. Belmares, D. Martinez, R. Rodríguez-Herrera, J. Contreras, Food Technol. Biotechnol. 46, 218 (2008)

    CAS  Google Scholar 

  5. P. Skenderidis, K. Petrotos, I. Giavasis, C. Hadjichristodoulou, A. Tsakalof, J. Food Process Eng 40(5), e12522 (2016)

    Article  Google Scholar 

  6. H. Amagase, B. Sun, C. Borek, Nutr. Res. 29, 19 (2009)

    Article  CAS  Google Scholar 

  7. K. Le, F. Chiu, K. Ng, Food Chem. 105, 353 (2007)

    Article  CAS  Google Scholar 

  8. O. Potterat, Planta Med. 76, 7 (2010)

    Article  CAS  Google Scholar 

  9. D. Qian, Y. Zhao, G. Yang, L. Huang, Molecules 22, 911 (2017)

    Article  Google Scholar 

  10. A. Mocan, L. Vlase, D.C. Vodnar, A.M. Gheldiu, R. Oprean, G. Crisan, Molecules 20(8), 15060–15071 (2015). https://doi.org/10.3390/molecules200815060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. B. Kulczyński, A. Gramza-Michałowska, Pol. J. Food Nutr. Sci. 66, 67 (2016)

    Article  Google Scholar 

  12. H. Amagase, N.R. Farnsworth, Food Res. Int. 44, 1702 (2011)

    Article  CAS  Google Scholar 

  13. A.P. Carvalho, M. Mendes, M.M. Moreira, D. Cruz, J.M. Magalhães, M.F. Barroso, M.J. Ramalhosa, A. Duarte, L. Guido, A.M. Gomes, C.D. Matos, Int. J. Food Sci. Technol. 51, 1401 (2016)

    Article  CAS  Google Scholar 

  14. K. Vilkhu, R. Mawson, L. Simons, D. Bates, Innov. Food Sci. Emerg. Technol. 9, 161 (2008)

    Article  CAS  Google Scholar 

  15. S. Leontopoulos, P. Skenderidis, H. Kalorizou, K. Petrotos, J. Food Biosys. Eng. 7, 1 (2017)

    Google Scholar 

  16. P. Robert, C. Fredes, Molecules (Basel, Switz.) 20, 5875 (2015)

    Article  CAS  Google Scholar 

  17. A. Munin, F. Edwards-Lévy, Pharmaceutics 3, 793 (2011)

    Article  CAS  Google Scholar 

  18. K.B. Petrotos, F.K. Karkanta, P.E. Gkoutsidis, I. Giavasis, N. Papatheodorou, A. C. Ntontos 6, 170 (2012)

    Google Scholar 

  19. K.M.M. John, A.A. Bhagwat, D.L. Luthria, Food Chem. 235, 145 (2017)

    Article  CAS  Google Scholar 

  20. A. Malik, F. Afaq, S. Sarfaraz, V.M. Adhami, D.N. Syed, H. Mukhtar, Proc. Natl. Acad. Sci. U.S.A. 102, 14813 (2005)

    Article  CAS  Google Scholar 

  21. Y. Li, C. Guo, J. Yang, J. Wei, J. Xu, S. Cheng, Food Chem. 96, 254 (2006)

    Article  CAS  Google Scholar 

  22. M. Hajimahmoodi, M.R. Oveisi, N. Sadeghi, B. Jannat, M. Hadjibabaie, E. Farahani, M.R. Akrami, R. Namdar, Pak. J. Biol. Sci. 11, 1600 (2008)

    Article  CAS  Google Scholar 

  23. S. Gozlekci, O. Saracoglu, E. Onursal, M. Ozgen, Pharmacogn. Mag. 7, 161 (2011)

    Article  CAS  Google Scholar 

  24. A. Sood, M. Gupta, Food Biosci. 12, 100 (2015)

    Article  CAS  Google Scholar 

  25. Z. Kalaycıoğlu, F.B. Erim, Food Chem. 221, 496 (2017)

    Article  Google Scholar 

  26. M. Çam, Y. Hışıl, Food Chem. 123, 878 (2010)

    Article  Google Scholar 

  27. U.A. Fischer, R. Carle, D.R. Kammerer, Food Chem. 127, 807 (2011)

    Article  CAS  Google Scholar 

  28. T. Ismail, P. Sestili, S. Akhtar, J. Ethnopharmacol. 143, 397 (2012)

    Article  CAS  Google Scholar 

  29. S.V. Leontopoulos, P. Skenderidis, V. Anatolioti, M.I. Kokkora, S. Tsilfoglou, K.B. Petrotos, I. Vagelas, J. Food Biosyst. Eng. 6(1), 38 (2017)

    Google Scholar 

  30. E. Haslam, J. Nat. Prod. 59, 205 (1996)

    Article  CAS  Google Scholar 

  31. S. Naz, R. Siddiqi, S. Ahmad, S.A. Rasool, S.A. Sayeed, J. Food Sci. 72, M341 (2007)

    Article  CAS  Google Scholar 

  32. L.C. Braga, J.W. Shupp, C. Cummings, M. Jett, J.A. Takahashi, L.S. Carmo, E. Chartone-Souza, A.M.A. Nascimento, J. Ethnopharmacol. 96, 335 (2005)

    Article  CAS  Google Scholar 

  33. N.S. Al-Zoreky, Int. J. Food Microbiol. 134, 244 (2009)

    Article  CAS  Google Scholar 

  34. G.M. El-Sherbini, K.M. Ibrahim, E.T. El Sherbiny, N.M. Abdel-Hady, T.A. Morsy, J. Egypt. Soc. Parasitol. 40, 229 (2010)

    PubMed  Google Scholar 

  35. O.M. Albarri, I. Var, A. Boushihassal, M. Meral, C. Önlen, M.H. Mohamed, F. Köksal, J. Biotechnol. Sci. Res. 3(6), 175 (2017)

    Google Scholar 

  36. Y. Roos, M. Karel, Biotechnol. Prog. 6, 159 (1990)

    Article  CAS  Google Scholar 

  37. O.V. Alekseeva, A.V. Noskov, S.S. Guseinov, A.V. Agafonov, Prot. Met. Phys. Chem. Surf. 51, 253 (2015)

    Article  CAS  Google Scholar 

  38. A.L. Waterhouse, Current Protocols in Food Analytical Chemistry (Wiley, Hoboken, 2001)

    Google Scholar 

  39. W. Brand-Williams, M.E. Cuvelier, C. Berset, Food Sci. Technol. 28, 25 (1995)

    CAS  Google Scholar 

  40. E. Kerasioti, D. Stagos, A. Priftis, S. Aivazidis, A.M. Tsatsakis, A.W. Hayes, D. Kouretas, Food Chem. 155, 271 (2014)

    Article  CAS  Google Scholar 

  41. J.C. Boulet, P. Williams, T. Doco, Carbohydr. Polym. 69, 79 (2007)

    Article  CAS  Google Scholar 

  42. S. Lohumi, C. Mo, J.-S. Kang, S.-J. Hong, B.-K. Cho, J. Biosyst. Eng. 38, 312 (2013)

    Article  Google Scholar 

  43. CLSI, Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically Approved Standard, 9th edn. (CLSI, Wayne, 2012)

    Google Scholar 

  44. S.V. Leontopoulos, I. Giavasis, K. Petrotos, M. Kokkora, C. Makridis, Agric. Agric. Sci. Proc. 4, 327 (2015)

    Google Scholar 

  45. N.G. Baydar, O. Sagdic, G. Ozkan, S. Cetin, Int. J. Food Sci. Technol. 41(7), 799 (2006)

    Article  CAS  Google Scholar 

  46. P. Dalgaard, T. Ross, L. Kamperman, K. Neumeyer, T.A. McMeekin, Int. J. Food Microbiol. 23, 391 (1994)

    Article  CAS  Google Scholar 

  47. B. Shan, Y. Cai, J.D. Brooks, H. Corke, Int. J. Food Microbiol. 117, 112 (2007)

    Article  CAS  Google Scholar 

  48. S.V. Leontopoulos, K.B. Petrotos, M.I. Kokkora, I. Giavasis, C. Papaioannou, Desalin. Water Treat. 57, 20646 (2016)

    CAS  Google Scholar 

  49. C. Valgas, S.M. de Souza, E.F.A. Smânia, A. Smânia Jr., Braz. J. Microbiol. 38, 369 (2007)

    Article  Google Scholar 

  50. A. Benchennouf, S. Grigorakis, S. Loupassaki, Pharm. Biol. 55, 596 (2017)

    Article  CAS  Google Scholar 

  51. N. Ullah, J. Ali, F.A. Khan, M. Khurram, A. Hussain, Middle-East J. Sci. Res. 11, 396 (2012)

    CAS  Google Scholar 

  52. A.C. Pedro, J.B.B. Maurer, S.F. Zawadzki-Baggio, S. Ávila, G.M. Maciel, C.W. Haminiuk, Ind. Crops Prod. 112, 90 (2018)

    Article  CAS  Google Scholar 

  53. R.F. Yang, C. Zhao, X. Chen, S.W. Chan, J.Y. Wu, J. funct. foods 17, 903 (2015)

    Article  CAS  Google Scholar 

  54. D. Donno, G.L. Beccaro, M.G. Mellano, A.K. Cerutti, G. Bounous, J. funct. foods 18, 1070 (2015)

    Article  CAS  Google Scholar 

  55. N.I. Fit, F. Chirila, G. Nadas, E. Pall, R. Muresan, Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca. Vet. Med. 70, 72–613 (2013)

    Google Scholar 

  56. A. Asănică, C. Manole, V. Tudor, A. Dobre, R.I. Teodorescu, AgroLife Sci. J. 5(1), 15 (2016)

    Google Scholar 

  57. H. Vardin, A. Tay, B. Ozen, L. Mauer, Food Chem. 108, 742 (2008)

    Article  CAS  Google Scholar 

  58. L. Zuo, S. Sun, Q. Zhou, J. Tao, I. Noda, J. Pharm. Biomed. Anal. 30, 1491 (2003)

    Article  CAS  Google Scholar 

  59. D. Mlambo, Detection of Quercetin using Polymer Coated Quartz Crystal Microbalance and the Modification of á-Zirconium Phosphate to Develop a Sorbent for Organic Pollutant Removal. Doctoral dissertation, Marquette University (2010). Retrieved from https://epublications.marquette.edu/dissertations_mu/77/

  60. D. Wu, S. Lam, K. Cheong, F. Wei, P. Lin, Z. Long, X. Lv, J. Zhao, S. Ma, S. Li, J. Pharm. Biomed. Anal. 129, 210 (2016)

    Article  CAS  Google Scholar 

  61. A. Mocan, L. Vlase, D.C. Vodnar, C. Bischin, D. Hanganu, A.-M. Gheldiu, R. Oprean, R. Silaghi-Dumitrescu, G. Crisan, Molecules (Basel, Switzerland) 19, 10056 (2014)

    Article  Google Scholar 

  62. I. Dahech, W. Farah, M. Trigui, A.B. Hssouna, H. Belghith, K.S. Belghith, F.B. Abdallah, Int. J. Biol. Macromol. 60, 328 (2013)

    Article  CAS  Google Scholar 

  63. A. Salvat, L. Antonacci, R.H. Fortunato, E.Y. Suarez, H.M. Godoy, Phytomedicine 11, 230 (2004)

    Article  CAS  Google Scholar 

  64. K. Barathikannan, B. Venkatadri, A. Khusro, N.A. Al-Dhabi, P. Agastian, M.V. Arasu, H.S. Choi, Y.O. Kim, BMC Complement. Altern. Med. 16, 264 (2016)

    Article  Google Scholar 

  65. M.E. Legaz, M.M. Pedrosa, R. de Armas, C.W. Rodrı́guez, V. de los Rios, C. Vicente, Anal. Chim. Acta 372, 201 (1998)

    Article  Google Scholar 

  66. P. Skenderidis, D. Lampakis, I. Giavasis, S. Leontopoulos, K. Petrotos, C. Hadjichristodoulou, Antioxidants 8, 60 (2019)

    Article  CAS  Google Scholar 

  67. T. Maruyama, S. Katoh, M. Nakajima, H. Nabetani, T.P. Abbott, A. Shono, K. Satoh, J. Membr. Sci. 192, 201 (2001)

    Article  CAS  Google Scholar 

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Correspondence to Prodromos Skenderidis.

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Skenderidis, P., Mitsagga, C., Giavasis, I. et al. The in vitro antimicrobial activity assessment of ultrasound assisted Lycium barbarum fruit extracts and pomegranate fruit peels. Food Measure 13, 2017–2031 (2019). https://doi.org/10.1007/s11694-019-00123-6

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