Targeted Phenolic Characterization and Antioxidant Bioactivity of Extracts from Edible Acheta domesticus

Maria Catalina Nino, Lavanya Reddivari, Mario G Ferruzzi, Andrea M Liceaga, Maria Catalina Nino, Lavanya Reddivari, Mario G Ferruzzi, Andrea M Liceaga

Abstract

With entomophagy gaining popularity in the Western hemisphere as a solution for future food insecurity, research on alternative protein sources, such as edible insects, has become relevant. Most of the research performed on insects has been on their nutritional qualities; however, little is known regarding bioactive compounds, such as polyphenols, that, if present in the insect, could provide additional benefits when the insect is consumed. In this study, methanolic extracts of Acheta domesticus from two farms and their corresponding feeds were obtained using a microwave-assisted extraction. Targeted phenolic characterization was accomplished through LC-MS/MS leading to the identification of 4-hydroxybenzoic acid, p-coumaric acid, ferulic acid, and syringic acid as major phenolic compounds in both A. domesticus extracts. Furthermore, the in vitro antioxidant activity was evaluated using 2,2-diphenyl-1-picrylhydrazyl radical cation (DPPH) and 2,2'-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) radical assays demonstrating the superior quenching activity of the A. domesticus extracts compared to the feeds. The discovery of phenolic compounds in A. domesticus implies the ability of this insect species to sequester and absorb dietary phenolics leading to possible added health benefits when consumed.

Keywords: antioxidant activity; bioactive compounds; edible insects; phenolic compounds.

Conflict of interest statement

All authors declare no competing interests.

Figures

Figure 1
Figure 1
Antioxidant activity assays of extracts of A. domesticus (organic Acheta and commercial Acheta) and feed (organic feed and commercial feed): (a) DPPH radical scavenging activity (IC50 value, mg extract/mL); (b) ABTS radical scavenging activity (IC50 value, mg extract/mL). Asterisk (*) indicates significant difference (p < 0.05) between A. domesticus and feed extracts, respectively.

References

    1. Payne C., Megido R.C., Dobermann D., Frédéric F., Shockley M., Sogari G. Edible Insects in the Food Sector. Springer; Berlin/Heidelberg, Germany: 2019. Insects as Food in the Global North—The Evolution of the Entomophagy Movement; pp. 11–26.
    1. Sosa D.A.T., Fogliano V. Insect Physiology and Ecology. InTech; Rijeka, Croatia: 2017. Potential of insect-derived ingredients for food applications; pp. 215–231.
    1. Van Huis A. Potential of insects as food and feed in assuring food security. Annu. Rev. Entomol. 2013;58:563–583. doi: 10.1146/annurev-ento-120811-153704.
    1. Roos N., van Huis A. Consuming insects: Are there health benefits? J. Insects Food Feed. 2017;3:225–229. doi: 10.3920/JIFF2017.x007.
    1. Yi L., Lakemond C.M.M., Sagis L.M.C., Eisner-Schadler V., van Huis A., van Boekel M.A.J.S. Extraction and characterisation of protein fractions from five insect species. Food Chem. 2013;141:3341–3348. doi: 10.1016/j.foodchem.2013.05.115.
    1. Halloran A., Roos N., Eilenberg J., Cerutti A., Bruun S. Life cycle assessment of edible insects for food protein: A review. Agron. Sustain. Dev. 2016;36:57. doi: 10.1007/s13593-016-0392-8.
    1. Nakagaki B.J., Defoliart G.R. Comparison of diets for mass-rearing Acheta domesticus (Orthoptera: Gryllidae) as a novelty food, and comparison of food conversion efficiency with values reported for livestock. J. Econ. Entomol. 1991;84:891–896. doi: 10.1093/jee/84.3.891.
    1. Rumpold B.A., Schlüter O.K. Potential and challenges of insects as an innovative source for food and feed production. Innov. Food Sci. Emerg. Technol. 2013;17:1–11. doi: 10.1016/j.ifset.2012.11.005.
    1. Poma G., Cuykx M., Amato E., Calaprice C., Focant J.F., Covaci A. Evaluation of hazardous chemicals in edible insects and insect-based food intended for human consumption. Food Chem. Toxicol. 2017;100:70–79. doi: 10.1016/j.fct.2016.12.006.
    1. Oonincx D.G., van Itterbeeck J., Heetkamp M.J., van den Brand H., van Loon J.J., van Huis A. An exploration on greenhouse gas and ammonia production by insect species suitable for animal or human consumption. PLoS ONE. 2010;5:e14445. doi: 10.1371/journal.pone.0014445.
    1. Da Silva Lucas A.J., de Oliveira L.M., da Rocha M., Prentice C. Edible insects: An alternative of nutritional, functional and bioactive compounds. Food Chem. 2020;311:126022. doi: 10.1016/j.foodchem.2019.126022.
    1. Calzada-Luna G., San Martin-Gonzalez F., Mauer L., Liceaga A.M. Cricket (Acheta domesticus) Protein Hydrolysates Impact on the Physicochemical, Structural and Sensory properties of Tortillas and Tortilla chips. J. Insects Food Feed. 2021;7:109–120. doi: 10.3920/JIFF2020.0010.
    1. Del Hierro J.N., Gutiérrez-Docio A., Otero P., Reglero G., Martin D. Characterization, antioxidant activity, and inhibitory effect on pancreatic lipase of extracts from the edible insects Acheta domesticus and Tenebrio molitor. Food Chem. 2020;309:125742. doi: 10.1016/j.foodchem.2019.125742.
    1. Ignat I., Volf I., Popa V.I. A critical review of methods for characterisation of polyphenolic compounds in fruits and vegetables. Food Chem. 2011;126:1821–1835. doi: 10.1016/j.foodchem.2010.12.026.
    1. Carocho M., CFR Ferreira I. The role of phenolic compounds in the fight against cancer—A review. Anti-Cancer Agents Med. Chem. (Former. Curr. Med. Chem. -Anti-Cancer Agents) 2013;13:1236–1258. doi: 10.2174/18715206113139990301.
    1. Di Carlo G., Mascolo N., Izzo A.A., Capasso F. Flavonoids: Old and new aspects of a class of natural therapeutic drugs. Life Sci. 1999;65:337–353. doi: 10.1016/S0024-3205(99)00120-4.
    1. Farhadi F., Khameneh B., Iranshahi M., Iranshahy M. Antibacterial activity of flavonoids and their structure-activity relationship: An update review. Phytother. Res. 2019;33:13–40. doi: 10.1002/ptr.6208.
    1. Gomes A., Fernandes E., Lima J.L., Mira L., Corvo M.L. Molecular mechanisms of anti-inflammatory activity mediated by flavonoids. Curr. Med. Chem. 2008;15:1586–1605. doi: 10.2174/092986708784911579.
    1. Nino M., Reddivari L., Osorio C., Kaplan I., Liceaga A. Insects as a source of phenolic compounds and potential health benefits. J. Insects Food Feed. 2021:1–12. in press.
    1. Burghardt F., Proksch P., Fiedler K. Flavonoid sequestration by the common blue butterfly Polyommatus icarus: Quantitative intraspecific variation in relation to larval hostplant, sex and body size. Biochem. Syst. Ecol. 2001;29:875–889. doi: 10.1016/S0305-1978(01)00036-9.
    1. Hirayama C., Ono H., Meng Y., Shimada T., Daimon T. Flavonoids from the cocoon of Rondotia menciana. Phytochemistry. 2013;94:108–112. doi: 10.1016/j.phytochem.2013.05.023.
    1. Liu S., Sun J., Yu L., Zhang C., Bi J., Zhu F., Qu M., Yang Q. Antioxidant activity and phenolic compounds of Holotrichia parallela Motschulsky extracts. Food Chem. 2012;134:1885–1891. doi: 10.1016/j.foodchem.2012.03.091.
    1. Singleton V.L., Rossi J.A. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 1965;16:144–158.
    1. Cuadrado-Silva C., Pozo-Bayón M., Osorio C. Targeted metabolomic analysis of polyphenols with antioxidant activity in sour guava (Psidium friedrichsthalianum Nied.) fruit. Molecules. 2017;22:11. doi: 10.3390/molecules22010011.
    1. Reddivari L., Hale A.L., Miller J.C. Determination of phenolic content, composition and their contribution to antioxidant activity in specialty potato selections. Am. J. Potato Res. 2007;84:275–282. doi: 10.1007/BF02986239.
    1. Ketnawa S., Liceaga A.M. Effect of microwave treatments on antioxidant activity and antigenicity of fish frame protein hydrolysates. Food Bioprocess Technol. 2017;10:582–591. doi: 10.1007/s11947-016-1841-8.
    1. Suh H.-J., Kim S.-R., Lee K.-S., Park S., Kang S.C. Antioxidant activity of various solvent extracts from Allomyrina dichotoma (Arthropoda: Insecta) larvae. J. Photochem. Photobiol. B Biol. 2010;99:67–73. doi: 10.1016/j.jphotobiol.2010.02.005.
    1. Musundire R., Zvidzai C., Chidewe C. Bio-Active Compounds Composition in Edible Stinkbugs Consumed in South-Eastern Districts of Zimbabwe. Int. J. Biol. 2014;6:36–45. doi: 10.5539/ijb.v6n3p36.
    1. Musundire R., Zvidzai C., Chidewe C., Ngadze R., Macheka L., Manditsera F., Mubaiwa J., Masheka A. Nutritional and bioactive compounds composition of Eulepida mashona, an edible beetle in Zimbabwe. J. Insects Food Feed. 2016;2:179–187. doi: 10.3920/JIFF2015.0050.
    1. Musundire R., Zvidzai C., Chidewe C., Samende B., Manditsera F. Nutrient and anti-nutrient composition of Henicus whellani (Orthoptera: Stenopelmatidae), an edible ground cricket, in south-eastern Zimbabwe. Int. J. Trop. Insect Sci. 2014;34:223–231. doi: 10.1017/S1742758414000484.
    1. Everette J.D., Bryant Q.M., Green A.M., Abbey Y.A., Wangila G.W., Walker R.B. Thorough study of reactivity of various compound classes toward the Folin-Ciocalteu reagent. J. Agric. Food Chem. 2010;58:8139–8144. doi: 10.1021/jf1005935.
    1. Magalhães L.M., Santos F., Segundo M.A., Reis S., Lima J.L. Rapid microplate high-throughput methodology for assessment of Folin-Ciocalteu reducing capacity. Talanta. 2010;83:441–447. doi: 10.1016/j.talanta.2010.09.042.
    1. Burghardt F., Fiedlert K., Proksch P. Uptake of flavonoids from Vicia villosa (Fabaceae) by the lycaenid butterfly, Polyommatus icarus (Lepidoptera: Lycaenidae) Biochem. Syst. Ecol. 1997;25:527–536. doi: 10.1016/S0305-1978(97)00057-4.
    1. Wiesen B., Krug E., Fiedler K., Wray V., Proksch P. Sequestration of host-plant-derived flavonoids by lycaenid butterfly Polyommatus icarus. J. Chem. Ecol. 1994;20:2523–2538. doi: 10.1007/BF02036189.
    1. Schittko U., Burghardt F., Fiedler K., Wray V., Proksch P. Sequestration and distribution of flavonoids in the common blue butterfly Polyommatus icarus reared on Trifolium repens. Phytochemistry. 1999;51:609–614. doi: 10.1016/S0031-9422(98)00746-8.
    1. Geuder M., Wray V., Fiedler K., Proksch P. Sequestration and metabolism of host-plant flavonoids by the lycaenid butterfly Polyommatus bellargus. J. Chem. Ecol. 1997;23:1361–1372. doi: 10.1023/B:JOEC.0000006469.00557.69.
    1. Ferreres F., Valentão P., Pereira J.A., Bento A., Noites A., Seabra R.M., Andrade P.B. HPLC-DAD-MS/MS-ESI screening of phenolic compounds in Pieris brassicae L. reared on Brassica rapa var. rapa L. J. Agric. Food Chem. 2008;56:844–853. doi: 10.1021/jf072657a.
    1. Ferreres F., Fernandes F., Pereira D.M., Pereira J.A., Valentao P., Andrade P.B. Phenolics metabolism in insects: Pieris brassicae—Brassica oleracea var. costata ecological duo. J. Agric. Food Chem. 2009;57:9035–9043. doi: 10.1021/jf901538j.
    1. Cheynier V. Phenolic compounds: From plants to foods. Phytochem. Rev. 2012;11:153–177. doi: 10.1007/s11101-012-9242-8.
    1. Ifie I., Marshall L.J. Food processing and its impact on phenolic constituents in food. Cogent Food Agric. 2018;4:1507782. doi: 10.1080/23311932.2018.1507782.
    1. Shahidi F., Zhong Y. Measurement of antioxidant activity. J. Funct. Foods. 2015;18:757–781. doi: 10.1016/j.jff.2015.01.047.
    1. Craft B.D., Kerrihard A.L., Amarowicz R., Pegg R.B. Phenol-based antioxidants and the in vitro methods used for their assessment. Compr. Rev. Food Sci. Food Saf. 2012;11:148–173. doi: 10.1111/j.1541-4337.2011.00173.x.
    1. Sang S., Lapsley K., Jeong W.-S., Lachance P.A., Ho C.-T., Rosen R.T. Antioxidative phenolic compounds isolated from almond skins (Prunus amygdalus Batsch) J. Agric. Food Chem. 2002;50:2459–2463. doi: 10.1021/jf011533+.
    1. Santos D.I., Saraiva J.M.A., Vicente A.A., Moldão-Martins M. Innovative Thermal and Non-Thermal Processing, Bioaccessibility and Bioavailability of Nutrients and Bioactive Compounds. Elsevier; Amsterdam, The Netherlands: 2019. Methods for determining bioavailability and bioaccessibility of bioactive compounds and nutrients; pp. 23–54.
    1. Ferreira I.C., Martins N., Barros L. Advances in Food and Nutrition Research. Volume 82. Elsevier; Amsterdam, The Netherlands: 2017. Phenolic compounds and its bioavailability: In vitro bioactive compounds or health promoters? pp. 1–44.

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