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Efficacy of different citrus essential oils to inhibit the growth and B1 aflatoxin biosynthesis of Aspergillus flavus

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Abstract

Food contamination by aflatoxin B1 (AFB1), produced by mycotoxigenic strains of Aspergillus spp., causes severe medical and economic implications. Essential oils (EOs) are mixtures of eco-friendly natural volatile substances. Their ability to inhibit fungal growth has been investigated, while no data are available about their efficacy in inhibition of AFB1 biosynthesis. This study investigates the efficacy of five different citrus EOs to inhibit the growth and AFB1 synthesis of A. flavus through in vitro tests for a future application in food matrices. AFB1 detection was carried out by LC-ESI-TQD analytical approach. Lemon (Citrus limon (L.) Burm. f.), bergamot (Citrus bergamia Risso), and bitter orange (Citrus aurantium L.) EOs were the most effective causing a 97.88%, 97.04%, and 96.43% reduction in mycelial growth, respectively. Sweet orange and mandarin EOs showed the lowest percentage of mycelial growth reduction. Citrus EOs showed different capacity of AFB1 inhibition (lemon > bitter orange > bergamot > sweet orange > mandarin). Our results showed a dose-dependent antifungal activity of lemon, bitter orange, and bergamot EOs which at 2% (v/v) inhibited both mycelium growth and AFB1 genesis of A. flavus. Our results show that EOs’ use can be a pivotal key to recovery and reuse of citrus fruit wastes and to be used as eco-friendly fungicides for improvement of food safety. The use of EOs obtained at low cost from the residues of citric industry presents an interesting option for improving the profitability of the agriculture.

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References

  • Abrar M, Anjum FM, Butt MS, Pasha I, Randhawa MA, Saeed F, Waqas K (2013) Aflatoxins: biosynthesis, occurrence, toxicity and remedies. Crit Rev Food Sci Nutr 53:862–874. https://doi.org/10.1080/10408398.2011.563154

    Article  CAS  Google Scholar 

  • Aloui H, Khwaldia K, Licciardello F, Mazzaglia A, Muratore G, Hamdi M, Restuccia C (2014) Efficacy of the combined application of chitosan and locust bean gum with different citrus essential oils to control postharvest spoilage caused by Aspergillus flavus in dates. Int J Food Microbiol 170:21–28. https://doi.org/10.1016/j.ijfoodmicro.2013.10.017

    Article  CAS  Google Scholar 

  • Alpsoy L (2010) Inhibitory effect of essential oil on aflatoxin activities. Afr J Biotechnol 9(17):2474–2481

    CAS  Google Scholar 

  • Bejarano Rodriguez RJ, Centeno Briceño SJ (2009) Citrus lemon extract for aflatoxin and aflatoxigenic fungi control in concentrated chicken feed produced in Venezuela. Rev Soc Venez Microbiol 29:57–61

    Google Scholar 

  • Caccioni DRL, Guizzardi M, Biondi DM, Renda A, Ruberto G (1998) Relationship between volatile components of citrus fruit essential oils and antimicrobial action on Penicillium digitatum and Penicillium italicum. Int J Food Microbiol 43:73–79. https://doi.org/10.1016/S0168-1605(98)00099-3

    Article  CAS  Google Scholar 

  • Dambolena JS, López AG, Cánepa MC, Theumer MG, Zygadlo JA (2008) Inhibitory effect of cyclic terpenes (limonene, menthol, menthone and thymol) on Fusarium verticillioides MRC 826 growth and fumonisin B1 biosynthesis. Toxicon 51:37–44. https://doi.org/10.1016/j.toxicon.2007.07.005

    Article  CAS  Google Scholar 

  • Derakhshan Z, Ferrante M, Tadi M, Ansari F, Heydari A, Hosseini MS, Conti GO, Sadrabad EK (2018) Antioxidant activity and total phenolic content of ethanolic extract of pomegranate peels, juice and seeds. Food Chem Toxicol 114:108–111. https://doi.org/10.1016/j.fct.2018.02.023

    Article  CAS  Google Scholar 

  • Dos Santos Oliveira M, Badiale FE (2008) Screening of antifungal and antimycotoxigenic activity of plant phenolic extracts. World Mycotoxin J 1(2):139–146. https://doi.org/10.3920/WMJ2008.1006

    Article  Google Scholar 

  • Dwivedy AK, Prakash B, Chanotiya CS, Bisht D, Dubey NK (2017) Chemically characterized Mentha cardiaca L. essential oil as plant based preservative in view of efficacy against biodeteriorating fungi of dry fruits, aflatoxin secretion, lipid peroxidation and safety profile assessment. Food Chem Toxicol 106:175–184

    Article  CAS  Google Scholar 

  • EFSA (2014) Scientific opinion on the risks for human and animal health related to the presence of modified forms of certain mycotoxins in food and feed. EFSA J 12:3916–4023

    Google Scholar 

  • Egbuta MA, Mwanza M, Babalola OO (2017) Health risks associated with exposure to filamentous fungi. Int J Environ Res Public Health 14:E719. https://doi.org/10.3390/ijerph14070719

    Article  CAS  Google Scholar 

  • Fakhri Y, Mohseni-Bandpei A, Oliveri Conti G, Ferrante M, Cristaldi A et al (2018) Systematic review and health risk assessment of arsenic and lead in the fished shrimps from the Persian gulf. Food Chem Toxicol 113:278–286. https://doi.org/10.1016/j.fct.2018.01.046

    Article  CAS  Google Scholar 

  • Fallahzadeh RA, Miri M, Taghavi M, Gholizadeh A, Anbarani R, Hosseini-Bandegharaei A, Ferrante M, Oliveri Conti G (2018) Spatial variation and probabilistic risk assessment of exposure to fluoride in drinking water. Food Chem Toxicol 113:314–321. https://doi.org/10.1016/j.fct.2018.02.001

    Article  CAS  Google Scholar 

  • FAO (2004) Worldwide regulations for mycotoxins in food and feed in 2003. Food and Agriculture organization ot the United Nations Rome 2004. http://www.fao.org/3/y5499e/y5499e00.htm

  • Ferhat MA, Meklati BY, Chemat F (2007) Comparison of different isolation methods of essential oil from citrus fruits: cold pressing, hydrodistillation and microwave ‘dry’ distillation. Flavour Fragr J 22:494–504. https://doi.org/10.1002/ffj.1829

    Article  CAS  Google Scholar 

  • Ferrante M, Conti GO (2017) Environment and neurodegenerative diseases: an update on miRNA role. Microrna 6:157–165. https://doi.org/10.2174/2211536606666170811151503

    Article  CAS  Google Scholar 

  • Ferrante M, Oliveri Conti G (2018) Food safety and risk evaluation. Food Chem Toxicol 121:309–310. https://doi.org/10.1016/j.fct.2018.08.077

    Article  CAS  Google Scholar 

  • Fiore M, Oliveri Conti G, Caltabiano R, Buffone A, Zuccarello P, Cormaci L, Cannizzaro MA, Ferrante M (2019) Role of emerging environmental risk factors in thyroid cancer: a brief review. Int J Environ Res Public Health 16(7):E1185

    Article  Google Scholar 

  • Fung F, Wang HS, Menon S (2018) Food safety in the 21st century. Biom J 41(2):88–95

    Google Scholar 

  • Garcia D, Ramos AJ, Sanchis V, Marí S (2012) Effect of Equisetum arvense and Stevia rebaudiana extracts on growth and mycotoxin production by Aspergillus flavus and Fusarium verticillioides in maize seeds as affected by water activity. Int J Food Microbiol 153:21–27. https://doi.org/10.1016/j.ijfoodmicro.2011.10.010

    Article  CAS  Google Scholar 

  • Hope R, Cairns-Fuller V, Aldred D, Magan N (2005) Use of antioxidants and essential oils for controlling mycotoxins in grain. BCPC Crop Sci Technol 5B:429–436

    Google Scholar 

  • IARC (2012) Monographs on the evaluation of carcinogenic risks to humans: chemical agents and related occupations. A review of human carcinogens, vol 100F. International Agency for Research on Cancer, Lyon, pp 224–248

    Google Scholar 

  • Jing L, Lei Z, Li L, Xie R, Xi W, Guan Y, Sumner LW, Zhou Z (2014) Antifungal activity of Citrus essential oils. J Agric Food Chem 62:3011–3033. https://doi.org/10.1021/jf5006148

    Article  CAS  Google Scholar 

  • Kazemi M (2015) Effect of Carum copticum essential oil on growth and aflatoxin formation by Aspergillus strains. Nat Prod Res 29:1065–1068

    Article  CAS  Google Scholar 

  • Keramati H, Ghorbani R, Fakhri Y, Mousavi KA, Conti GO, Ferrante M et al (2018) Radon 222 in drinking water resources of Iran: a systematic review, meta-analysis and probabilistic risk assessment (Monte Carlo simulation). Food Chem Toxicol 115:460–469. https://doi.org/10.1016/j.fct.2018.03.042

    Article  CAS  Google Scholar 

  • Khlangwiset P, Wu F (2010) Costs and efficacy of public health interventions to reduce aflatoxin–induced human disease. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 27:998–1014. https://doi.org/10.1080/19440041003677475

    Article  CAS  Google Scholar 

  • Kocevski D, Du M, Kan J, Jing C, Lačanin I, Pavlović H (2013) Antifungal effect of Allium tuberosum, Cinnamomum cassia, and Pogostemon cablin essential oils and their components against population of Aspergillus species. J Food Sci 78:M731–M737. https://doi.org/10.1111/1750-3841.12118

    Article  CAS  Google Scholar 

  • Kumar P, Mishra S, Kumar A, Kumar S, Prasad CS (2017) In vivo and in vitro control activity of plant essential oils against three strains of Aspergillus niger. Environ Sci Pollut Res Int 24:21948–21959. https://doi.org/10.1007/s11356-017-9730-x

    Article  CAS  Google Scholar 

  • Kumari S, Pundhir S, Priya P, Jeena G, Punetha A, Chawla K, Firdos JZ, Mondal S, Yadav G (2014) EssOilDB: a database of essential oils reflecting terpene composition and variability in the plant kingdom. Database (Oxford) 2014:bau120

    Article  Google Scholar 

  • Li C, Mi T, Conti GO, Yu Q, Wen K, Shen J, Ferrante M, Wang Z (2015) Development of a screening fluorescence polarization immunoassay for the simultaneous detection of fumonisins B1 and B2 in maize. J Agric Food Chem 63(20):4940–4946. https://doi.org/10.1021/acs.jafc.5b01845

    Article  CAS  Google Scholar 

  • Mie A, Andersen HR, Gunnarsson S, Kahl J, Kesse-Guyot E, Rembiałkowska E, Quaglio G, Grandjean P (2017) Human health implications of organic food and organic agriculture: a comprehensive review. Environ Health 16(1):111. https://doi.org/10.1186/s12940-017-0315-4

    Article  CAS  Google Scholar 

  • Mohajeri FA, Misaghi A, Gheisari H, Basti AA, Amiri A, Ghalebi SR, Derakhshan Z, Tafti RD (2018) The effect of Zataria multiflora Boiss essential oil on the growth and citrinin production of Penicillium citrinum in culture media and cheese. Food Chem Toxicol 118:691–694. https://doi.org/10.1016/j.fct.2018.06.021

    Article  CAS  Google Scholar 

  • Morcia C, Tumino G, Ghizzoni R, Bara A, Salhi N, Terzi V (2017) In vitro evaluation of sub-lethal concentrations of plant-derived antifungal compounds on FUSARIA growth and mycotoxin production. Molecules 2017(22):1271. https://doi.org/10.3390/molecules22081271

    Article  CAS  Google Scholar 

  • Nazzaro F, Fratianni F, Coppola R, De Feo V (2017) Essential oils and antifungal activity. Pharmaceuticals (Basel) 10(4):E86. https://doi.org/10.1111/srt.12750

    Article  Google Scholar 

  • Nogueira JHC, Gonçalez E, Galleti SR, Facanali R, Marques MOM, Felicio JD (2010) Ageratum conyzoides essential oil as aflatoxin suppressor of Aspergillus flavus. Int J Food Microbiol 137:55–60. https://doi.org/10.1016/j.ijfoodmicro.2009.10.017

    Article  CAS  Google Scholar 

  • Pandey AK, Sonker N, Singh P (2016) Efficacy of some essential oils against Aspergillus flavus with special reference to Lippia alba oil an inhibitor of fungal proliferation and aflatoxin B1 production in green gram seeds during storage. J Food Sci 81:M928–M934. https://doi.org/10.1111/1750-3841.13254

    Article  CAS  Google Scholar 

  • Perrone G, Gallo A (2017) Aspergillus species and their associated mycotoxins. Methods Mol Biol 1542:33–49

    Article  CAS  Google Scholar 

  • Prakash B, Kedia A, Mishra PK, Dubey NK (2015a) Plant essential oils as food preservatives to control moulds, mycotoxin contamination and oxidative deterioration of agri-food commodities–potential and challenges. Food Control 47:381–391

    Article  CAS  Google Scholar 

  • Prakash B, Singh P, Goni R, Raina AK, Dubey NK (2015b) Efficacy of Angelica archangelica essential oil, phenyl ethyl alcohol and α- terpineol against isolated molds from walnut and their antiaflatoxigenic and antioxidant activity. J Food Sci Technol 52:2220–2228

    Article  CAS  Google Scholar 

  • Raimondo M, Caracciolo F, Cembalo L, Chinnici G, Pecorino B, D’Amico M (2018) Making virtue out of necessity: managing the citrus waste supply chain for bioeconomy applications. Sustainability 10:4821. https://doi.org/10.3390/su10124821

    Article  Google Scholar 

  • Rammanee K, Hongpattarakere T (2011) Effects of tropical citrus essential oils on growth, aflatoxin production, and ultrastructure alterations of Aspergillus flavus and Aspergillus parasiticus. Food Bioprocess Technol 4:1050–1059. https://doi.org/10.1007/s11947-010-0507-1

    Article  CAS  Google Scholar 

  • Razzaghi-Abyaneh M, Shams-Ghahfarokhi M, Rezaee M-B, Jaimand K, Alinezhad S, Saberi R (2009) Chemical composition and antiaflatoxigenic activity of Carum carvi L., Thymus vulgaris and Citrus aurantifolia essential oils. Food Control 20:1018–1024. https://doi.org/10.1016/j.foodcont.2008.12.007

    Article  CAS  Google Scholar 

  • Reynoso MM, Torres AM, Ramirez ML, Rodrigues MI, Chulze S, Magan N (2002) Efficacy of antioxidant mixtures on growth, fumonisin production and hydrolytic enzyme production by Fusarium verticillioides and F. proliferatum in vitro on maize-based media. Mycol Res 106:1093–1099. https://doi.org/10.1017/S0953756202006135

    Article  CAS  Google Scholar 

  • Salas MP, Pok PS, Resnik SL, Pacin A, Munitz M (2016) Use of citrus flavanones to prevent aflatoxin contamination using response surface methodology. Food Control 60:533–537. https://doi.org/10.1016/j.foodcont.2015.08.026

    Article  CAS  Google Scholar 

  • Sciacca S, Ferrante M, Oliveri Conti G (2012) Carcinogen role of food by mycotoxins and knowledge gap. In: Margarita Pesheva Teodora Stoycheva Martin Dimitrov. Carcinogen. INTECH, Rijeka, pp 133–162 ISBN: 979-953-307-466-4

    Google Scholar 

  • Sharma N, Tripathi A (2008) Effects of Citrus sinensis (L.) Osbeck epicarp essential oil on growth and morphogenesis of Aspergillus niger (L.) Van Tieghem. Microbiol Res 163:337–344. https://doi.org/10.1016/j.micres.2006.06.009

    Article  CAS  Google Scholar 

  • Singh P, Shukla R, Kumar A, Prakash B, Singh S, Dubey NK (2010) Effect of Citrus reticulata and Cymbopogon citratus essential oils on Aspergillus flavus growth and aflatoxin production on Asparagus racemosus. Mycopathologia 170:195–202. https://doi.org/10.1007/s11046-010-9311-8

    Article  Google Scholar 

  • Sumalan RM, Alexa E, Poiana MA (2013) Assessment of inhibitory potential of essential oils on natural mycoflora and Fusarium mycotoxins production in wheat. Chem Cent J 7:32. https://doi.org/10.1186/1752-153X-7-32

    Article  CAS  Google Scholar 

  • Umesha S, Manukumar HM, Chandrasekhar B, Shivakumara P, Shiva KJ, Raghava S, Avinash P, Shirin M, Bharathi TR, Rajini SB, Nandhini M, Vinaya Rani GG, Shobha M, Prakash HS (2017) Aflatoxins and food pathogens: impact of biologically active aflatoxins and their control strategies. J Sci Food Agric 97:1698–1707. https://doi.org/10.1002/jsfa.8144

    Article  CAS  Google Scholar 

  • Van Egmond HP, Jonker ARO (2004) Worldwide Regulations for Mycotoxins in Food and Feed in 2003. FAO food and nutrition paper 81, Report of the Food and Agriculture Organization of the United Nations, Rome

  • Velázquez-Nuñez MJ, Avila-Sosa R, Palou E, López-Malo A (2013) Antifungal activity of orange (Citrus sinensis var. Valencia) peel essential oil applied by direct addition or vapor contact. Food Control 31:1–4. https://doi.org/10.1016/j.foodcont.2012.09.029

    Article  CAS  Google Scholar 

  • Vergopoulou S, Galanopoulou D, Markaki P (2001) Methyl jasmonate stimulates aflatoxin B1 biosynthesis by Aspergillus parasiticus. J Agric Food Chem 49:3494–3498. https://doi.org/10.1021/jf010074+

    Article  CAS  Google Scholar 

  • Vinceti M, Filippini T, Violi F, Rothman KJ, Costanzini S, Malagoli C, Wise LA, Odone A, Signorelli C, Iacuzio L, Arcolin E, Mandrioli J, Fini N, Patti F, Lo Fermo S, Pietrini V, Teggi S, Ghermandi G, Scillieri R, Ledda C, Mauceri C, Sciacca S, Fiore M, Ferrante M (2017) Pesticide exposure assessed through agricultural crop proximity and risk of amyotrophic lateral sclerosis. Environ Health 16(1):91

    Article  Google Scholar 

  • Viuda-Martos M, Ruiz-Navajas Y, Fernández-López J, Pérez-Álvarez J (2008) Antifungal activity of lemon (Citrus lemon L.), mandarin (Citrus reticulata L.), grapefruit (Citrus paradisi L.) and orange (Citrus sinensis L.) essential oils. Food Control 19:1130–1138. https://doi.org/10.1016/j.foodcont.2007.12.003

    Article  CAS  Google Scholar 

  • Zuccarello P, Ferrante M, Cristaldi A, Copat C, Grasso A, Sangregorio D, Fiore M, Oliveri Conti G (2019) Exposure to microplastics (<10 μm) associated to plastic bottles mineral water consumption: the first quantitative study. Water Res 15(157):365–371. https://doi.org/10.1016/j.watres.2019.03.091

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Dipartimento di Agricoltura, Alimentazione e Ambiente (Di3A), University of Catania, via Santa Sofia 100, 95123, Catania, Italy

    Cristina Restuccia & Lucia Parafati

  2. Environmental and Food Hygiene Laboratories (LIAA), Department of Medical, Surgical Sciences and Advanced Technologies “G.F. Ingrassia”, University of Catania, via Santa Sofia 87, 95123, Catania, Italy

    Gea Oliveri Conti, Pietro Zuccarello, Antonio Cristaldi & Margherita Ferrante

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  1. Cristina Restuccia
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  2. Gea Oliveri Conti
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Correspondence to Gea Oliveri Conti.

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Highlights

1. The study provides first data about citrus EOs’ efficacy in Aspergillus spp.

2. This study is the first that evaluates five EOs efficacy in mycelium growth and AFB1 synthesis control.

3. Lemon, bergamot, and bitter orange EOs were the most effective in mycelium growth reduction.

4. Citrus EOs showed different capacity of AFB1 inhibition (lemon > bitter orange > bergamot > sweet orange > mandarin)

5. Our results show that EOs’ use can be used as eco-friendly fungicides for improvement of food safety

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Restuccia, C., Oliveri Conti, G., Zuccarello, P. et al. Efficacy of different citrus essential oils to inhibit the growth and B1 aflatoxin biosynthesis of Aspergillus flavus. Environ Sci Pollut Res 26, 31263–31272 (2019). https://doi.org/10.1007/s11356-019-06169-9

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