Skip to main content
Log in

Antimicrobial and antioxidant activity of phenolic extracts from walnut (Juglans regia L.) green husk by using pressure-driven membrane process

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

In this study, antioxidant (DPPH and metal chelating), DNA cleavage, biofilm, and antimicrobial properties of extracted phenol from the walnut green husk (WGH) and its different concentrate and permeate samples were evaluated. For maximum phenolic compound extraction from the WGH first, the effects of solvent type (deionized water, methanol, n-hexane, acetone, and ethanol), solvent temperature (25–75 °C), and extraction time (0.5–24 h) were optimized. Then to concentrate phenolic compounds a pressure-driven membrane process was used with four different membrane types. The phenol contents of the concentrate samples were found to be microfiltration (MF) concentrate 4400 mg/L, ultrafiltration (UF) concentrate 4175 mg/L, nanofiltration (NF) concentrate 8155 mg/L, and reverse osmosis (RO) concentrate 8100 mg/L. LC-MSMS was used to determine the quantification of phenolic compounds in permeate and concentrate streams. In addition, all of the concentrate samples with high phenol content showed a high antioxidant activity as 100% with MF concentrate, UF concentrate, NF concentrated and RO concentrated. Likewise, concentrate samples were found to have very high antibiofilm activity as 82.86% for NF concentrate againts S. aureus, 85.80% for NF concentrate against P. aureginosa, 80.95% for RO concentrate against S. aureus, and 83.61% for RO-concentrate against P. aureginosa. When the antimicrobial activity of the extracted phenol from WGH and its different concentrate and permeate samples were evaluated by micro dilution and disk diffusion methods, it was found that the ability of the concentrate samples to inhibit bacterial growth was much higher than permeate ones. In addition, extracted phenol from WGH and its different concentrate and permeate samples showed significant DNA nuclease activity.

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
Fig. 5

Similar content being viewed by others

Data availability statement

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

DPPH:

2, 2-Diphenyl-1-picrylhydrazyl

MF:

Microfiltration

MIC:

Minimum inhibition concentration

NF:

Nanofiltration

RO:

Reverse osmosis

UF:

Ultrafiltration

WGH:

Walnut green husk

References

  • Ağırtaş M, Karataş C, Ozdemir S (2015) Synthesis of some metallophthalocyanineswith dimethyl 5-(phenoxy)-isophthalate substituents and evaluation of theirantioxidant-antibacterial activities. Spectrochim Acta Part A Mol Biomolspectrosc 135:20–24

    Article  Google Scholar 

  • Agullo A, Pereira E, Freire M, Valentão P, Andrade P, Alvarez J et al (2013) Influence of solvent on the antioxidant and antimicrobial properties of walnut (Juglans regia L.) green husk extracts. Ind Crops Products 42:126–132

    Article  Google Scholar 

  • Akinmoladun AC, Falaiye E, Ojo OB, Adeoti A, Amoo ZA, Olaleye MT (2022) Effect of extraction technique, solvent polarity, and plant matrix on the antioxidant properties of Chrysophyllum albidum G Don. (African Star Apple). Bull Natl Res Centre. https://doi.org/10.1186/s42269-022-00718-y

    Article  Google Scholar 

  • Aminov R (2010) A brief history of the antibiotic era: lessons learned and challenges for the future. Front Microbiol 8(1):134. https://doi.org/10.3389/fmicb.2010.00134

    Article  Google Scholar 

  • Arend GD, Adorno WT, Rezzadori K, Di Luccio M, Chaves VC, Reginatto FH, Petrus JCC (2017) Concentration of phenolic compounds from strawberry (Fragaria X ananassa Duch) juice by nanofiltration membrane. J Food Eng 201:36–41. https://doi.org/10.1016/J.JFOODENG.2017.01.014

    Article  CAS  Google Scholar 

  • Caballero E, Soto C, Jara J (2019) Thermal stability data of juglone from extracts of walnut (Juglans regia) green husk, and technologies used to concentrate juglone. Data Brief 25:104081. https://doi.org/10.1016/J.DIB.2019.104081

    Article  Google Scholar 

  • Carvalho M, Ferreira PJ, Mendes VS, Silva R, Pereira JA, Jerónimo C, Silva BM (2010) Human cancer cell antiproliferative and antioxidant activities of Juglans regia L. Food Chem Toxicol 48(1):441–447. https://doi.org/10.1016/J.FCT.2009.10.043

    Article  CAS  Google Scholar 

  • Chandramohan Y, Padmanaban V, Bethunaickan R, Tripathy S, Swaminathan S, Ranganathan UD (2019) In vitro interaction profiles of the new antitubercular drugs bedaquiline and delamanid with moxifloxacin against clinical Mycobacterium tuberculosis isolates. J Glob Antimicrob Resist 19:348–353. https://doi.org/10.1016/j.jgar.2019.06.013

  • Che Sulaiman IS, Basri M, Fard Masoumi HR, Chee WJ, Ashari SE, Ismail M (2017) Effects of temperature, time, and solvent ratio on the extraction of phenolic compounds and the anti-radical activity of Clinacanthus nutans Lindau leaves by response surface methodology. Chem Cent J 11(1):1–11. https://doi.org/10.1186/s13065-017-0285-1

    Article  CAS  Google Scholar 

  • Darvishi E, Kahrizi D, Arkan E (2019) Comparison of different properties of zinc oxide nanoparticles synthesized by the green (using Juglans regia L. leaf extract) and chemical methods. J Mol Liq 286:110831. https://doi.org/10.1016/j.molliq.2019.04.108

  • Dolatabadi S, Moghadam HN, Mahdavi-Ourtakand M (2018) Evaluating the anti -biofilm and antibacterial effects of Juglans regia L. extracts against clinical isolates of Pseudomonas aeruginosa. Microb Pathog 118:285–289. https://doi.org/10.1016/j.micpath.2018.03.055

  • FAO (2020) Statistical Yearbook. Agricultural production. https://www.fao.org/home/en

  • Fernández-Agulló A, Pereira E, Freire MS, Valentão P, Andrade PB, González-álvarez J, Pereira JA (2013) Influence of solvent on the antioxidant and antimicrobial properties of walnut (Juglans regia L.) green husk extracts. Ind Crops Products 42(1):126–132. https://doi.org/10.1016/J.INDCROP.2012.05.021

    Article  Google Scholar 

  • Goli AH, Barzegar M, Sahari MA (2005) Antioxidant activity and total phenolic compounds of pistachio (Pistachia vera) hull extracts. Food Chem 92(3):521–525. https://doi.org/10.1016/j.foodchem.2004.08.020

    Article  CAS  Google Scholar 

  • Gomes F, Martins N, Barros L, Rodrigues ME, Oliveira M, Beatriz PP, Henriques M, Ferreira ICFR (2018) Plant phenolic extracts as an effective strategy to control Staphylococcus aureus the dairy industry pathogen. Ind Crops Prod 112:515–520. https://doi.org/10.1016/j.indcrop.2017.12.027

  • Jahanban-Esfahlan A, Jahanban-Esfahlan R, Tabibiazar M, Roufegarinejad L, Amarowicz R (2020) Recent advances in the use of walnut (Juglans regia L.) shell as a valuable plant-based bio-sorbent for the removal of hazardous materials. Res Adv 10:7026. https://doi.org/10.1039/c9ra10084a

    Article  CAS  Google Scholar 

  • Jaitz L, Siegl K, Eder R, Rak G, Abranko L, Koellensperger G, Hann S (2010) LC–MS/MS analysis of phenols for classification of red wine according to geographic origin grape variety and vintage. Food Chem 122(1):366–372. https://doi.org/10.1016/j.foodchem.2010.02.053

  • Kadiroğlu P, Ekici H (2018) Yeşil ceviz kabuklarının biyoaktif özelliklerinin FT-IR spektroskopi yöntemiyle tahmin edilmesi. Akademik Gıda 16(1):20–26. https://doi.org/10.24323/AKADEMIK-GIDA.415643

    Article  Google Scholar 

  • Karimi N, Minaei S, Hasani D, Eyvani A (2008) Parameters involved in walnut peeling process. J Agric Machinery Sci 4(4):389–393

    Google Scholar 

  • Kavak DD, Altıok E, Bayraktar O, Ülkü S (2010) Pistacia terebinthus extract: As a potential antioxidant antimicrobial and possible β-glucuronidase inhibitor. J Mol Catal B Enzym 64(3–4):167–171. https://doi.org/10.1016/j.molcatb.2010.01.029

  • Kong X, Bao S, Song W, Hua Y, Zhang C, Chen Y, Li X (2021) Contributions of ethanol fractionation on the properties of vegetable protein hydrolysates and differences in the characteristics of metal (Ca Zn Fe)-chelating peptides. LWT 146:111482. https://doi.org/10.1016/j.lwt.2021.111482

  • Lee JH, Kim YG, Khadke SK, Yamano A, Woo JT, Lee J (2019) Antimicrobial and antibiofilm activities of prenylated flavanones from Macaranga tanarius. Phytomedicine 63:153033. https://doi.org/10.1016/j.phymed.2019.153033

  • Li X, Deng S (2020) Synergistic inhibition effect of walnut green husk extract and potassium iodide on the corrosion of cold rolled steel in trichloroacetic acid solution. J Market Res 9(6):15604–15620. https://doi.org/10.1016/J.JMRT.2020.11.018

    Article  CAS  Google Scholar 

  • Lu C, Liu H, Shangguan W, Chen S, Zhong Q (2021) Antibiofilm activities of the cinnamon extract against Vibrio parahaemolyticus and Escherichia coli. Arch Microbiol 203(1):125–135. https://doi.org/10.1007/s00203-020-02008-5

  • Lv Y, Wei K, Meng X, Huang Y, Zhang T, Li Z (2017) Separation and identification of iron-chelating peptides from defatted walnut flake by nanoLC-ESI–MS/MS and de novo sequencing. Process Biochem 59:223–228. https://doi.org/10.1016/j.procbio.2017.05.010

  • Machado MTC, Mello BCBS, Hubinger MD (2015) Evaluation of pequi (Caryocar Brasiliense Camb.) aqueous extract quality processed by membranes. Food Bioprod Process 95:304–312. https://doi.org/10.1016/J.FBP.2014.10.013

    Article  CAS  Google Scholar 

  • Mehdizadeh T, Zamani A, Froushani SMA (2020) Preparation of Cu nanoparticles fixed on cellulosic walnut shell material and investigation of its antibacterial antioxidant and anticancer effects. Heliyon 6(3):e03528. https://doi.org/10.1016/j.heliyon.2020.e03528

  • Mokrani A, Madani K (2016) Effect of solvent, time and temperature on the extraction of phenolic compounds and antioxidant capacity of peach (Prunus persica L.) fruit. Sep Purif Technol 162:68–76. https://doi.org/10.1016/J.SEPPUR.2016.01.043

    Article  CAS  Google Scholar 

  • Naczk M, Shaidi F (2004) Extraction and analysis of phenolics in food. J Chromatogr A 1504:95–111

    Article  Google Scholar 

  • Nile SH, Nile A, Liu J, Kim DH, Kai G (2019) Exploitation of apple pomace towards extraction of triterpenic acids antioxidant potential cytotoxic effects and inhibition of clinically important enzymes. Food Chem Toxicol 131:110563. https://doi.org/10.1016/j.fct.2019.110563

  • Oliveira I, Sousa A, Ferreira ICFR, Bento A, Estevinho L, Pereira JA (2008a) Total phenols, antioxidant potential and antimicrobial activity of walnut (Juglans regia L.) green husks. Food Chem Toxicol 46(7):2326–2331. https://doi.org/10.1016/J.FCT.2008.03.017

    Article  CAS  Google Scholar 

  • Ozay Y, Ozdemir S, Gonca S, Canli O, Dizge N (2021) Phenolic compounds recovery from pistachio hull using pressure-driven membrane process and a cleaner production of biopesticide. Environ Technol Innov 24:101993. https://doi.org/10.1016/J.ETI.2021.101993

    Article  CAS  Google Scholar 

  • Pinelo M, Rubilar M, Jerez M, Sineiro J, Núñez MJ (2005) Effect of solvent, temperature, and solvent-to-solid ratio on the total phenolic content and antiradical activity of extracts from different components of grape pomace. J Agric Food Chem 53(6):2111–2117. https://doi.org/10.1021/jf0488110

    Article  CAS  Google Scholar 

  • Ramezani N, Raji F, Rezakazemi M, Younas M (2020) Juglone extraction from walnut (Juglans regia L.) green husk by supercritical CO2: Process optimization using Taguchi method. J Environ Chem Eng 8(3):103776. https://doi.org/10.1016/J.JECE.2020.103776

    Article  CAS  Google Scholar 

  • Shrestha R, Khanal S, Poudel P, Khadayat K, Ghaju S, Bhandari A, Lekhak S, Pant ND, Sharma M, Marasini BP (2019) Extended spectrum β-lactamase producing uropathogenic Escherichia coli and the correlation of biofilm with antibiotics resistance in Nepal. Ann Clin Microbiol Antimicrob 18(1):42. https://doi.org/10.1186/s12941-019-0340-y

  • Silva EM, Souza JNS, Rogez H, Rees JF, Larondelle Y (2007) Antioxidant activities and polyphenolic contents of fifteen selected plant species from the Amazonian region. Food Chem 101(3):1012–1018. https://doi.org/10.1016/J.FOODCHEM.2006.02.055

    Article  CAS  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol 299:152–178. https://doi.org/10.1016/S0076-6879(99)99017-1

    Article  CAS  Google Scholar 

  • Sobisch LY, Rogowski KM, Fuchs J, Schmieder W, Vaishampayan A, Oles P, Novikova N, Grohmann E (2019) Biofilm Forming Antibiotic Resistant Gram-Positive Pathogens Isolated From Surfaces on the International Space Station. Front Microbiol 10:543. https://doi.org/10.3389/fmicb.2019.00543

  • Zakavi F, Hagh L, Daraeighadikolaei A, Farajzadeh Sheikh A, Leilavi Shooshtari Z (2013)Antibacterial effectof Juglans regiabark against oral pathologic bacteria. Int J Dent

  • Zarei M, Ghanbari R, Tajabadi N, Abdul-Hamid A, Bakar F (2016) Generation, fractionation, and characterization of iron-chelating protein hydrolysate from palm kernel cake proteins. J Food Sci 81:C341–C347

    Article  CAS  Google Scholar 

Download references

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Author information

Authors and Affiliations

Authors

Contributions

HA and ND contributed to the study conception and design. Material preparation and analysis were performed by YO, SO, OC, and GT. YO and EOK wrote the manuscript with support from ND and SO, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Nadir Dizge.

Ethics declarations

Conflicts of interest

The authors declare that they have no competing interests.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1625 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arslan, H., Ondul Koc, E., Ozay, Y. et al. Antimicrobial and antioxidant activity of phenolic extracts from walnut (Juglans regia L.) green husk by using pressure-driven membrane process. J Food Sci Technol 60, 73–83 (2023). https://doi.org/10.1007/s13197-022-05588-w

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-022-05588-w

Keywords

Navigation