In Vitro Antioxidant and Antihypertensive Activity of Edible Insects Flours (Mealworm and Grasshopper) Fermented with Lactococcus lactis Strains

The objective of the present study was to evaluate the potential antioxidant and angiotensin converting enzyme inhibition (ACEI) activity of edible insect flours fermented with Lactococcus lactis strains. For the fermentation, mealworm and grasshoppers flours were dissolved (0.5% w/v) in buffer solution (pH 7.0) and individually inoculated (3%) with Lactococcus lactis strains (NRRL B-50571, NRRL B-50572). The samples were incubated for 72 h at 30 °C, and the pH was recorded. The degree of hydrolysis (DH) and protein content were determined. The total polyphenol compounds, antioxidant activity (ABTS, DPPH, ORAC, and FRAP), and ACEI of the <3 kDa fractions were analyzed. The pH of the fermented samples decreased to 3.5–3.9 (p < 0.05). The fermented grasshopper flour showed an increased DH (0.42%) and overall higher total polyphenol content (8.23 mg Gallic Acid Equivalent/mL). In general, the highest antioxidant activity was for the grasshopper fractions fermented for 24 h by Lactococcus lactis NRRL B-50572, which also showed 23.47% ACEI inhibition with an IC50 of 0.97 mg/mL. The peptide profile obtained increased after fermentation, being higher for the mealworm flour fermented sample. This study presents, for the first time, the use of specific strains of Lactococus lactis for fermenting edible insect-derived products in the production of bioactive compounds with potential antioxidant and antihypertensive activity.

[1]  L. Reddivari,et al.  Insects as a source of phenolic compounds and potential health benefits , 2021 .

[2]  L. Reddivari,et al.  Identification and Characterization of Edible Cricket Peptides on Hypertensive and Glycemic In Vitro Inhibition and Their Anti-Inflammatory Activity on RAW 264.7 Macrophage Cells , 2020, Nutrients.

[3]  H. García,et al.  An insight to fermented edible insects: A global perspective and prospective. , 2020, Food research international.

[4]  M. Sharifi-Rad,et al.  Lifestyle, Oxidative Stress, and Antioxidants: Back and Forth in the Pathophysiology of Chronic Diseases , 2020, Frontiers in Physiology.

[5]  M. Karaś,et al.  Current Trends of Bioactive Peptides—New Sources and Therapeutic Effect , 2020, Foods.

[6]  K. Takács,et al.  STUDY OF CHITINASE AND CHITINOLYTIC ACTIVITY OF LACTOBACILLUS STRAINS , 2020 .

[7]  Yusuf Olamide Kewuyemi,et al.  Fermented Edible Insects for Promoting Food Security in Africa , 2020, Insects.

[8]  S. Imathiu,et al.  Benefits and food safety concerns associated with consumption of edible insects , 2020 .

[9]  -S E.H.  STUDY OF CHITINASE AND CHITINOLYTIC ACTIVITY OF LACTOBACILLUS STRAINS , 2020 .

[10]  C. Prentice,et al.  Edible insects: An alternative of nutritional, functional and bioactive compounds. , 2019, Food chemistry.

[11]  H. García,et al.  Cooperation between Lactococcus lactis NRRL B-50571 and NRRL B-50572 for Aroma Formation in Fermented Milk , 2019, Foods.

[12]  Ding Yang,et al.  Edible insects as a food source: a review , 2019 .

[13]  V. Dries,et al.  Comparison of Six Commercial Meat Starter Cultures for the Fermentation of Yellow Mealworm (Tenebrio molitor) Paste , 2019, Microorganisms.

[14]  G. Reglero,et al.  Characterization, antioxidant activity, and inhibitory effect on pancreatic lipase of extracts from the edible insects Acheta domesticus and Tenebrio molitor. , 2019, Food chemistry.

[15]  A. González-Córdova,et al.  In Vitro Antithrombotic and Hypocholesterolemic Activities of Milk Fermented with Specific Strains of Lactococcus lactis , 2019, Nutrients.

[16]  S. Govorushko.  Global status of insects as food and feed source: A review , 2019, Trends in Food Science & Technology.

[17]  M. Serafini,et al.  Antioxidant Activities in vitro of Water and Liposoluble Extracts Obtained by Different Species of Edible Insects and Invertebrates , 2019, Front. Nutr..

[18]  Jianshe Chen,et al.  Extraction, characterization and functional properties of soluble proteins from edible grasshopper (Schistocerca gregaria) and honey bee (Apis mellifera). , 2019, Food research international.

[19]  Philip E. Johnson,et al.  Effect of enzymatic hydrolysis on bioactive properties and allergenicity of cricket (Gryllodes sigillatus) protein. , 2018, Food chemistry.

[20]  J. Patz,et al.  Impact of Edible Cricket Consumption on Gut Microbiota in Healthy Adults, a Double-blind, Randomized Crossover Trial , 2018, Scientific Reports.

[21]  Maria Aliciane Fontenele Domingues,et al.  Nutritional, functional and biological properties of insect proteins: Processes for obtaining, consumption and future challenges , 2018, Trends in Food Science & Technology.

[22]  H. Astiazarán-García,et al.  Randomized double-blind controlled clinical trial of the blood pressure-lowering effect of fermented milk with Lactococcus lactis: A pilot study. , 2018, Journal of dairy science.

[23]  Ji-Su Kim,et al.  Characteristics of fermented seasoning sauces using Tenebrio molitor larvae , 2018 .

[24]  M. Karaś,et al.  Edible Insects as Source of Proteins , 2018 .

[25]  Ole G. Mouritsen,et al.  Flavour of fermented fish, insect, game, and pea sauces: Garum revisited , 2017 .

[26]  A. Huis,et al.  The environmental sustainability of insects as food and feed. A review , 2017, Agronomy for Sustainable Development.

[27]  Ceren Daşkaya-Dikmen,et al.  Angiotensin-I-Converting Enzyme (ACE)-Inhibitory Peptides from Plants , 2017, Nutrients.

[28]  A. Sanchez,et al.  Bioactive peptides: A review , 2017 .

[29]  Zhongxing Zhao,et al.  Purification, modification and inhibition mechanism of angiotensin I-converting enzyme inhibitory peptide from silkworm pupa (Bombyx mori) protein hydrolysate , 2017 .

[30]  M. Karaś,et al.  Antioxidant activity of predigested protein obtained from a range of farmed edible insects , 2017 .

[31]  M. Boekel,et al.  Protein identification and in vitro digestion of fractions from Tenebrio molitor , 2016, European Food Research and Technology.

[32]  N. Shah,et al.  Lactic acid bacterial fermentation modified phenolic composition in tea extracts and enhanced their antioxidant activity and cellular uptake of phenolic compounds following in vitro digestion , 2016 .

[33]  Jun-qiang Jia,et al.  A novel angiotensin-І converting enzyme (ACE) inhibitory peptide from gastrointestinal protease hydrolysate of silkworm pupa (Bombyx mori) protein: Biochemical characterization and molecular docking study , 2015, Peptides.

[34]  Jun-qiang Jia,et al.  Purification and molecular docking study of a novel angiotensin-I converting enzyme (ACE) inhibitory peptide from alcalase hydrolysate of ultrasonic-pretreated silkworm pupa (Bombyx mori) protein , 2015 .

[35]  M. Kaya,et al.  Extraction and characterization of chitin and chitosan with antimicrobial and antioxidant activities from cosmopolitan Orthoptera species (Insecta) , 2015, Biotechnology and Bioprocess Engineering.

[36]  Yantyati Widyastuti,et al.  The Role of Lactic Acid Bacteria in Milk Fermentation , 2014 .

[37]  S. Parkar,et al.  Fecal microbial metabolism of polyphenols and its effects on human gut microbiota. , 2013, Anaerobe.

[38]  Haile Ma,et al.  Angiotensin I-converting enzyme (ACE) inhibitory peptide derived from Tenebrio molitor (L.) larva protein hydrolysate , 2013, European Food Research and Technology.

[39]  M. Griffiths,et al.  Lactobacillus helveticus: the proteolytic system , 2012, Front. Microbiol..

[40]  J. Regenstein,et al.  Effect of thermal treatment on the characteristic properties of loach peptide , 2012 .

[41]  T. Herald,et al.  High-throughput micro plate assays for screening flavonoid content and DPPH-scavenging activity in sorghum bran and flour. , 2012, Journal of the science of food and agriculture.

[42]  J. V. van Loon,et al.  An Exploration on Greenhouse Gas and Ammonia Production by Insect Species Suitable for Animal or Human Consumption , 2010, PloS one.

[43]  Jace D Everette,et al.  Thorough study of reactivity of various compound classes toward the Folin-Ciocalteu reagent. , 2010, Journal of agricultural and food chemistry.

[44]  R. Siezen,et al.  The proteolytic system of lactic acid bacteria revisited: a genomic comparison , 2010, BMC Genomics.

[45]  J. Camp,et al.  Antioxidative and ACE inhibitory activities in enzymatic hydrolysates of the cotton leafworm, Spodoptera littoralis. , 2009 .

[46]  A. Zulueta,et al.  ORAC and TEAC assays comparison to measure the antioxidant capacity of food products. , 2009 .

[47]  R. Chakraborty,et al.  Validity of modified Gompertz and Logistic models in predicting cell growth of Pediococcus acidilactici H during the production of bacteriocin pediocin AcH , 2007 .

[48]  P. Proksch,et al.  Sequestration of host-plant-derived flavonoids by lycaenid butterflyPolyommatus icarus , 1994, Journal of Chemical Ecology.

[49]  M. Ikawa,et al.  Utilization of Folin-Ciocalteu phenol reagent for the detection of certain nitrogen compounds. , 2003, Journal of agricultural and food chemistry.

[50]  Jianping Wu,et al.  Improved method for direct high-performance liquid chromatography assay of angiotensin-converting enzyme-catalyzed reactions. , 2002, Journal of chromatography. A.

[51]  C. Dambmann,et al.  Improved Method for Determining Food Protein Degree of Hydrolysis , 2001 .

[52]  R. Lamuela-Raventós,et al.  Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent , 1999 .

[53]  P. Proksch,et al.  Uptake of flavonoids from Vicia villosa (Fabaceae) by the lycaenid butterfly, Polyommatus icarus (Lepidoptera: Lycaenidae) , 1997 .

[54]  J J Strain,et al.  The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. , 1996, Analytical biochemistry.