Skip to main content
SpringerLink
Log in

Chemically characterized nanoencapsulated Homalomena aromatica Schott. essential oil as green preservative against fungal and aflatoxin B1 contamination of stored spices based on in vitro and in situ efficacy and favorable safety profile on mice

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Present study deals with the efficacy of nanoencapsulated Homalomena aromatica essential oil (HAEO) as a potent green preservative against toxigenic Aspergillus flavus strain (AF-LHP-NS 7), storage fungi, AFB1, and free radical-mediated deterioration of stored spices. GC–MS analysis revealed linalool (68.51%) as the major component of HAEO. HAEO was encapsulated into chitosan nanomatrix (CS-HAEO-Ne) and characterized through SEM, FTIR, and XRD. CS-HAEO-Ne completely inhibited A. flavus growth and AFB1 biosynthesis at 1.25 μL/mL and 1.0 μL/mL, respectively in comparison to unencapsulated HAEO (1.75 μL/mL and 1.25 μL/mL, respectively). CS-HAEO-Ne caused significant reduction in ergosterol content in treated A. flavus and provoked leakage of cellular ions (Ca+2, Mg+2, and K+) as well as 260 nm and 280 nm absorbing materials. Depletion of methylglyoxal level in treated A. flavus cells illustrated the novel antiaflatoxigenic efficacy of CS-HAEO-Ne. CS-HAEO-Ne exhibited superior antioxidant efficacy (IC50 (DPPH) = 4.5 μL/mL) over unencapsulated HAEO (IC50 (DPPH) = 15.9 μL/mL) and phenolic content. CS-HAEO-Ne depicted excellent in situ efficacy by inhibiting fungal infestation, AFB1 contamination, lipid peroxidation, and mineral loss with acceptable sensorial profile. Moreover, broad safety paradigm (LD50 value = 7150.11 mg/kg) of CS-HAEO-Ne also suggests its application as novel green preservative to enhance shelf life of stored spices.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Data availability

All data analyzed during this study are included in this manuscript.

References

  • Ali M, Sayem SAJ, Quah Y, Lee EB, Birhanu BT, Suk K, Park SC (2021) Investigation of potential antioxidants, thrombolytic and neuropharmacological activities of Homalomena aromatica leaves using experimental and in silico approaches. Molecules 26:975

    CAS  Google Scholar 

  • Antognelli C, Mezzasoma L, Fettucciari K, Talesa VN (2013) A novel mechanism of methylglyoxal cytotoxicity in prostate cancer cells. Int J Biochem Cell Biol 45:836–844

    CAS  Google Scholar 

  • Attallah OA, Shetta A, Elshishiny F, Mamdouh W (2020) Essential oil loaded pectin/chitosan nanoparticles preparation and optimization via Box–Behnken design against MCF-7 breast cancer cell lines. RSC Advances 10:8703–8708

    CAS  Google Scholar 

  • Bahuguna A, Ramalingam S, Arumugam A, Natarajan D, Kim M (2020) Molecular and in silico evidences explain the anti-inflammatory effect of Trachyspermum ammi essential oil in lipopolysaccharide induced macrophages. Process Biochem 96:138–145

    CAS  Google Scholar 

  • Balasubramani S, Rajendhiran T, Moola AK, Diana RKB (2017) Development of nanoemulsion from Vitex negundo L. essential oil and their efficacy of antioxidant, antimicrobial and larvicidal activities (Aedes aegypti L.). Environ Sci Pollut Res 24:15125–15133

    CAS  Google Scholar 

  • Bhattacharya T, Maishu SP, Akter R, Rahman M, Akhtar MF, Saleem A, Bin-Jumah M, Kamel M, Abdel Latif MA, Abdel-Daim MM (2021) A review on natural sources derived protein nanoparticles as anticancer agents. Curr Top Med Chem 21

  • Branca C, D'Angelo G, Crupi C, Khouzami K, Rifici S, Ruello G, Wanderlingh U (2016) Role of the OH and NH vibrational groups in polysaccharide-nanocomposite interactions: a FTIR-ATR study on chitosan and chitosan/clay films. Polymer 99:614–622

    CAS  Google Scholar 

  • Carneiro JNP, da Cruz RP, Campina FF, do Socorro Costa M, Dos Santos ATL, Sales DL, Bezerra CF, da Silva LE, de Araujo JP, do Amaral W, Rebelo RA, Begnini IM, de Lima LF, Coutinho DM, Morais-Braga MFB (2020) GC/MS analysis and antimicrobial activity of the Piper mikanianum (Kunth) Steud. essential oil. Food Chem Toxicol 135:1–8

    Google Scholar 

  • Cetin Babaoglu H, Bayrak A, Ozdemir N, Ozgun N (2017) Encapsulation of clove essential oil in hydroxypropyl beta-cyclodextrin for characterization, controlled release, and antioxidant activity. J Food Process Preserv 41:1–8

    Google Scholar 

  • Chaudhari AK, Singh VK, Das S, Prasad J, Dwivedy AK, Dubey NK (2020) Improvement of in vitro and in situ antifungal, AFB1 inhibitory and antioxidant activity of Origanum majorana L. essential oil through nanoemulsion and recommending as novel food preservative. Food ChemToxicol 143:1–12

    Google Scholar 

  • Chen ZY, Brown RL, Damann KE, Cleveland TE (2004) Identification of a maize kernel stress-related protein and its effect on aflatoxin accumulation. Phytopathology 94:938–945

    CAS  Google Scholar 

  • Cortes-Higareda M, de Lorena Ramos-Garcia M, Correa-Pacheco ZN, Del Rio-Garcia JC, Bautista-Banos S (2019) Nanostructured chitosan/propolis formulations: characterization and effect on the growth of Aspergillus flavus and production of aflatoxins. Heliyon 5:1–7

    Google Scholar 

  • de Leon-Martinez LD, Solis-Mercado J, Rodriguez-Aguilar M, Diaz-Barriga F, Ortiz DG, Flores-Ramirez R (2019a) Assessment of aflatoxin B1-lysine adduct in serum of infant population of the Huasteca Potosina, Mexico–a pilot study. World Mycotoxin J 12:421–429

    Google Scholar 

  • de Leon-Martinez LD, Diaz-Barriga F, Barbier O, Ortiz DLG, Ortega-Romero M, Perez-Vazquez F, Flores-Ramirez R (2019b) Evaluation of emerging biomarkers of renal damage and exposure to aflatoxin B1 in Mexican indigenous women: a pilot study. Environ Sci Pollut Res 26:12205–12216

    Google Scholar 

  • de Leon-Martinez LD, Lopez-Mendoza CM, Teran-Figueroa Y, Flores-Ramirez R, Diaz-Barriga F, Alcantara-Quintana LE (2021) Detection of aflatoxin B1 adducts in Mexican women with cervical lesions. World Mycotoxin J:1–12

  • Delshadi R, Bahrami A, Tafti AG, Barba FJ, Williams LL (2020) Micro and nano-encapsulation of vegetable and essential oils to develop functional food products with improved nutritional profiles. Trends Food Sci Technol 104:72–83

    CAS  Google Scholar 

  • Dhifi W, Bellili S, Jazi S, Bahloul N, Mnif W (2016) Essential oils’ chemical characterization and investigation of some biological activities: a critical review. Medicines 3:1–16

    Google Scholar 

  • Diaz de Leon-Martinez L, Rodriguez-Aguilar M, Wong-Arce A, Diaz-Barriga F, Banuelos-Hernandez B, Rosales-Mendoza S, Flores-Ramirez R (2020) Evaluation of acute and chronic exposure to aflatoxin B1 in indigenous women of the Huasteca Potosina, Mexico. Environ Sci Pollut Res 27:30583–30591

    CAS  Google Scholar 

  • Dzhanfezova T, Barba-Espin G, Muller R, Joernsgaard B, Hegelund JN, Madsen B, Larsen DH, Vega MM, Toldam-Andersen TB (2020) Anthocyanin profile, antioxidant activity and total phenolic content of a strawberry (Fragaria× ananassa Duch) genetic resource collection. Food Biosci 36:1–7

    Google Scholar 

  • El-Sayed A, Kamel M (2020) Advances in nanomedical applications: diagnostic, therapeutic, immunization, and vaccine production. Environ Sci Pollut Res 27:19200–19213

    CAS  Google Scholar 

  • Esmaeili A, Asgari A (2015) In vitro release and biological activities of Carum copticum essential oil (CEO) loaded chitosan nanoparticles. Int J Biol Macromol 81:283–290

    CAS  Google Scholar 

  • Fagbohun E, Ogundahunsi AS (2019) Effects of storage on nutritional, mineral composition and mycoflora of stored sundried Citrullus lanatus Thunberg (Melon) seeds. Int J Biochem Res Rev 28:1–7

    Google Scholar 

  • Feyzioglu GC, Tornuk F (2016) Development of chitosan nanoparticles loaded with summer savory (Satureja hortensis L.) essential oil for antimicrobial and antioxidant delivery applications. LWT- Food Sci Technol 70:104–110

    CAS  Google Scholar 

  • Food and Agriculture organization (FAO) (2004) Regulations for mycotoxins in food and feed in 2003. FAO, Food and Nutrition, paper 81. FAO, Rome

    Google Scholar 

  • Gupta M (2010) Pharmacological properties and traditional therapeutic uses of important Indian spices: A review. Int J Food Prop 13:1092–1116

    Google Scholar 

  • Hasheminejad N, Khodaiyan F, Safari M (2019) Improving the antifungal activity of clove essential oil encapsulated by chitosan nanoparticles. Food Chem 275:113–122

    CAS  Google Scholar 

  • Hosseini SF, Zandi M, Rezaei M, Farahmandghavi F (2013) Two-step method for encapsulation of oregano essential oil in chitosan nanoparticles: preparation, characterization and in vitro release study. Carbohydr Polym 95:50–56

    CAS  Google Scholar 

  • Hu J, Wang X, Xiao Z, Bi W (2015) Effect of chitosan nanoparticles loaded with cinnamon essential oil on the quality of chilled pork. LWT-Food Sci Technol 63:519–526

    CAS  Google Scholar 

  • International agency for research on cancer (IARC) (2012) Chemical agents and related occupations. IARC monographs on the evaluation of carcinogenic risks to humans, Volume 100F.

  • Iseri OD, Korpe DA, Sahin FI, Haberal M (2013) Hydrogen peroxide pretreatment of roots enhanced oxidative stress response of tomato under cold stress. Acta Physiol Plant 35:1905–1913

    CAS  Google Scholar 

  • Kabir M, Rahman M, Akter R, Behl T, Kaushik D, Mittal V, Pandey P, Akhtar MF, Saleem A, Albadrani GM, Kamel M (2021) Potential role of curcumin and its nanoformulations to treat various types of cancers. Biomolecules 11:392

    CAS  Google Scholar 

  • Khan A, Ahmad A, Akhtar F, Yousuf S, Xess I, Khan LA, Manzoor N (2010) Ocimum sanctum essential oil and its active principles exert their antifungal activity by disrupting ergosterol biosynthesis and membrane integrity. Res Microbiol 161:816–823

    CAS  Google Scholar 

  • Kovesi B, Cserhati M, Erdelyi M, Zandoki E, Mezes M, Balogh K (2020) Lack of dose-and time-dependent effects of aflatoxin B1 on gene expression and enzymes associated with lipid peroxidation and the glutathione redox system in chicken. Toxins 12:1–11

    Google Scholar 

  • Kumar A, Kujur A, Singh PP, Prakash B (2019) Nanoencapsulated plant-based bioactive formulation against food-borne molds and aflatoxin B1 contamination: Preparation, characterization and stability evaluation in the food system. Food Chem 287:139–150

    CAS  Google Scholar 

  • Li MF, Chen L, Xu MZ, Zhang JL, Wang Q, Zeng QZ, Wei XC, Yuan Y (2018) The formation of zein-chitosan complex coacervated particles: relationship to encapsulation and controlled release properties. Int J Biol Macromol 116:1232–1239

    CAS  Google Scholar 

  • Lupetti A, Danesi R, Campa M, Del Tacca M, Kelly S (2002) Molecular basis of resistance to azole antifungals. Trends Mol Med 8:76–81

    CAS  Google Scholar 

  • Marques CS, Carvalho SG, Bertoli LD, Villanova JCO, Pinheiro PF, dos Santos DCM, Yoshida MI, de Freitas JCC, Cipriano DF, Bernardes PC (2019) β-Cyclodextrin inclusion complexes with essential oils: obtention, characterization, antimicrobial activity and potential application for food preservative sachets. Food Res Int 119:499–509

    CAS  Google Scholar 

  • OECD (2008) Guideline for Testing of Chemicals, No. 425, Acute Oral Toxicity–Acute Oral Toxicity–Up-and-Down-Procedure (UDP). Organisation for economic co-operation and development, Paris, p 27

    Google Scholar 

  • Pabast M, Shariatifar N, Beikzadeh S, Jahed G (2018) Effects of chitosan coatings incorporating with free or nano-encapsulated Satureja plant essential oil on quality characteristics of lamb meat. Food Control 91:185–192

    CAS  Google Scholar 

  • Perazzo FF, Carvalho JCT, Carvalho JE, Rehder VLG (2003) Central properties of the essential oil and the crude ethanol extract from aerial parts of Artemisia annua L. Pharmacol Res 48:497–502

    CAS  Google Scholar 

  • Pickova D, Ostry V, Malir J, Toman J, Malir F (2020) A review on mycotoxins and microfungi in spices in the light of the last five years. Toxins 12:1–33

    Google Scholar 

  • Policegoudra RS, Goswami S, Aradhya SM, Chatterjee S, Datta S, Sivaswamy R, Chattopadhyay P, Singh L (2012) Bioactive constituents of Homalomena aromatica essential oil and its antifungal activity against dermatophytes and yeasts. J Mycol Med 22:83–87

    CAS  Google Scholar 

  • Potorti AG, Tropea A, Lo Turco V, Pellizzeri V, Belfita A, Dugo G, Di Bella G (2020) Mycotoxins in spices and culinary herbs from Italy and Tunisia. Nat Prod Res 34:167–171

    CAS  Google Scholar 

  • Prakash B, Kujur A, Yadav A, Kumar A, Singh PP, Dubey NK (2018) Nanoencapsulation: an efficient technology to boost the antimicrobial potential of plant essential oils in food system. Food Control 89:1–11

    CAS  Google Scholar 

  • Rajkumar V, Gunasekaran C, Paul CA, Dharmaraj J (2020a) Development of encapsulated peppermint essential oil in chitosan nanoparticles: characterization and biological efficacy against stored-grain pest control. Pestic Biochem Phys 170:1–9

    Google Scholar 

  • Rajkumar V, Gunasekaran C, Dharmaraj J, Chinnaraj P, Paul CA, Kanithachristy I (2020b) Structural characterization of chitosan nanoparticle loaded with Piper nigrum essential oil for biological efficacy against the stored grain pest control. Pestic Biochem Phys 166:1–9

    Google Scholar 

  • RASFF (2019) Rapid alert system for food and feed. Annual report-2019. https://ec.europa.eu/food/safety/rasff/index_en.htm

  • Rasooli I, Abyaneh MR (2004) Inhibitory effects of Thyme oils on growth and aflatoxin production by Aspergillus parasiticus. Food Control 15:479–483

    CAS  Google Scholar 

  • Ribeiro JC, Ribeiro WLC, Camurça-Vasconcelos ALF, Macedo ITF, Santos JML, Paula HCB, Filho JVA, Magalhaes RD, Bevilaqua CML (2014) Efficacy of free and nanoencapsulated Eucalyptus citriodora essential oils on sheep gastrointestinal nematodes and toxicity for mice. Vet Parasitol 204:243–248

    CAS  Google Scholar 

  • Ricci D, Fraternale D, Giamperi L, Bucchini A, Epifano F, Burini G, Curini M (2005) Chemical composition, antimicrobial and antioxidant activity of the essential oil of Teucrium marum (Lamiaceae). J Ethnopharmacol 98:195–200

    CAS  Google Scholar 

  • Roy SJ, Baruah PS, Lahkar L, Gurung L, Saikia D, Tanti B (2019) Phytochemical analysis and antioxidant activities of Homalomena aromatic Schott. J Pharmacogn Phytochem 8:1379–1385

    Google Scholar 

  • Sathivel S, Liu Q, Huang J, Prinyawiwatkul W (2007) The influence of chitosan glazing on the quality of skinless pink salmon (Oncorhynchus gorbuscha) fillets during frozen storage. Journal Food Eng 83:366–373

    CAS  Google Scholar 

  • Schlosser I, Prange A (2018) Antifungal activity of selected natural preservatives against the foodborne molds Penicillium verrucosum and Aspergillus westerdijkiae. FEMS Microbiol Lett 365:1–8

    Google Scholar 

  • Sheijooni-Fumani N, Hassan J, Yousefi SR (2011) Determination of aflatoxin B1 in cereals by homogeneous liquid–liquid extraction coupled to high performance liquid chromatography-fluorescence detection. J Sep Sci 34:1333–1337

    CAS  Google Scholar 

  • Singh N, Rao AS, Nandal A, Kumar S, Yadav SS, Ganaie SA, Narasimhan B (2020a) Phytochemical and pharmacological review of Cinnamomum verum J. Presl-a versatile spice used in food and nutrition. Food Chem 338:1–24

    Google Scholar 

  • Singh A, Chaudhari AK, Das S, Singh VK, Dwivedy AK, Shivalingam RK, Dubey NK (2020b) Assessment of preservative potential of Bunium persicum (Boiss) essential oil against fungal and aflatoxin contamination of stored masticatories and improvement in efficacy through encapsulation into chitosan nanomatrix. Environ Sci Pollut Res 27:27635–27650

    CAS  Google Scholar 

  • Singh V, Kumar K, Purohit D, Verma R, Pandey P, Bhatia S, Malik V, Mittal V, Rahman MH, Albadrani GM, Arafah MW (2021) Exploration of therapeutic applicability and different signaling mechanism of various phytopharmacological agents for treatment of breast cancer. Biomed Pharmacother 139:111584

    CAS  Google Scholar 

  • Siva S, Li C, Cui H, Meenatchi V, Lin L (2020) Encapsulation of essential oil components with methyl-β-cyclodextrin using ultrasonication: solubility, characterization, DPPH and antibacterial assay. Ultrason Sonochem 64:1–12

    Google Scholar 

  • Su H, Huang C, Liu Y, Kong S, Wang J, Huang H, Zhang B (2020) Preparation and characterization of Cinnamomum essential oil–chitosan nanocomposites: physical, structural, and antioxidant activities. Processes 8:1–13

    CAS  Google Scholar 

  • Thanushree MP, Sailendri D, Yoha KS, Moses JA, Anandharamakrishnan C (2019) Mycotoxin contamination in food: an exposition on spices. Trends Food Sci Technol 93:69–80

    CAS  Google Scholar 

  • Tian J, Huang B, Luo X, Zeng H, Ban X, He J, Wang Y (2012) The control of Aspergillus flavus with Cinnamomum jensenianum Hand.-Mazz essential oil and its potential use as a food preservative. Food Chem 130:520–527

    CAS  Google Scholar 

  • Upadhyay N, Singh VK, Dwivedy AK, Das S, Chaudhari AK, Dubey NK (2018) Cistus ladanifer L. essential oil as a plant based preservative against molds infesting oil seeds, aflatoxin B1 secretion, oxidative deterioration and methylglyoxal biosynthesis. LWT- Food Sci Technol 92:395–403

    CAS  Google Scholar 

  • Wu L, Liu M (2008) Preparation and properties of chitosan-coated NPK compound fertilizer with controlled-release and water-retention. Carbohydr Polym 72:240–247

    CAS  Google Scholar 

  • Yadav SK, Singla-Pareek SL, Reddy MK, Sopory SK (2005) Transgenic tobacco plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain higher reduced glutathione levels under salinity stress. FEBS Lett 579:6265–6271

    CAS  Google Scholar 

  • Yang Z, Wang H, Ying G, Yang M, Nian Y, Liu J, Kong W (2017) Relationship of mycotoxins accumulation and bioactive components variation in ginger after fungal inoculation. Front Pharmacol 8:331

    Google Scholar 

  • Zabka M, Pavela R, Slezakova L (2009) Antifungal effect of Pimenta dioica essential oil against dangerous pathogenic and toxinogenic fungi. Ind Crops Prod 30:250–253

    CAS  Google Scholar 

  • Zhu JJ, Zeng XP, Berkebile D, Du HJ, Tong Y, Qian K (2009) Efficacy and safety of catnip (Nepeta cataria) as a novel filth fly repellent. Med Vet Entomol 23:209–216

    CAS  Google Scholar 

Download references

Funding

This study was supported by the University Grant Commission (UGC) [grant no.: 16-9 (June 2018)/2019(NET/CSIR)], New Delhi, India.

Author information

Authors and Affiliations

  1. Laboratory of Herbal Pesticides, Centre of Advanced study (CAS) in Botany, Institute of Science, Banaras Hindu University, Varanasi, 221005, India

    Shikha Tiwari, Neha Upadhyay, Bijendra Kumar Singh, Vipin Kumar Singh & Nawal Kishore Dubey

Authors
  1. Shikha Tiwari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neha Upadhyay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bijendra Kumar Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vipin Kumar Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nawal Kishore Dubey
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Shikha Tiwari: conceptualization, writing-original review draft, funding acquisition; Neha Upadhyay: review and editing; formal analysis; Bijendra Kumar Singh: experimental analysis; Vipin Kumar Singh: review and editing, data curation; Nawal Kishore Dubey: writing-review and editing, supervision. All authors have reviewed and approved the final manuscript.

Corresponding author

Correspondence to Nawal Kishore Dubey.

Ethics declarations

Ethics approval

The animal-based experiment was performed according to the ethical standards of the institution.

Consent to participate

All authors participated in this work.

Consent for publication

All authors agree to publish this article in the Environmental Science and Pollution Research.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tiwari, ., Upadhyay, N., Singh, B.K. et al. Chemically characterized nanoencapsulated Homalomena aromatica Schott. essential oil as green preservative against fungal and aflatoxin B1 contamination of stored spices based on in vitro and in situ efficacy and favorable safety profile on mice. Environ Sci Pollut Res 29, 3091–3106 (2022). https://doi.org/10.1007/s11356-021-15794-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-15794-2

Keywords

Search

Navigation