Effect of Diets with the Addition of Edible Insects on the Development of Atherosclerotic Lesions in ApoE/LDLR−/− Mice
Abstract
:1. Introduction
2. Results
2.1. Nutritive Value and Fatty Acid Composition of Insects
2.2. Total Polyphenols Content and Antioxidant Activity of Insects’ Powder
2.3. Composition of Experimental Diets
2.4. Effect of Edible Insects on Body and Liver Weight and Biochemical Parameters in ApoE/LDLR−/− Mice
2.5. Effect of Edible Insects on Fatty Acids Composition of Adipose Tissue and Liver in ApoE/LDLR−/− Mice
2.6. Effect of Edible Insects on the Development of Atherosclerosis in ApoE/LDLR−/− Mice
3. Discussion
4. Materials and Methods
4.1. Insects
4.1.1. Nutritive Value and Fatty Acid Composition of Insects
4.1.2. Determination of Total Polyphenols Content of Insects
4.1.3. Determination of Antioxidant Activity of Insects
ABTS•+ Radical Scavenging
DPPH• Radical Scavenging
Ferric Reducing Antioxidant Power (FRAP)
4.2. Animals and Housing
4.3. Diets and Feeding
4.4. Blood Sampling, Glucose, and Biochemical Analyses of Plasma
4.5. Fatty Acids Profile of Adipose Tissue and Liver
4.6. Quantification of Atherosclerosis in Aorta (En Face Method)
4.7. Quantification of Atherosclerosis in Aortic Roots (Cross-Section Method)
4.8. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Insect | DM (g/100 g Insects’ Powder) | Ash (g/100 g DM) | Crude Protein (g/100 g DM) | Fat (g/100 g DM) | Chitin (g/100 g DM) |
---|---|---|---|---|---|
TM | 96.19 ± 0.11 | 3.39 a ± 0.06 | 57.06 a ± 0.14 | 28.67 a ± 0.02 | 9.36 a ± 0.07 |
GA | 96.10 ± 0.14 | 3.90 b ± 0.08 | 67.04 b ± 0.35 | 22.33 b ± 0.28 | 7.03 b ± 0.02 |
Systematic Name (IUPAC) | Number of Carbon Atoms: Number π Bonds | Insect | |
---|---|---|---|
TM | GA | ||
Dodecanoic acid | C12:0 | 0.46 a ± 0.02 | 0.19 b ± 0.08 |
Tetradecanoic acid | C14:0 | 5.58 a ± 0.27 | 1.81 b ± 0.89 |
Pentadecanoic acid | C15:0 | 0.21 ± 0.02 | 0.23 ± 0.05 |
Hexadecanoic acid | C16:0 | 18.84 a ± 0.30 | 22.16 b ± 1.53 |
cis-9-Hexadecenoic acid | C16:1 | 5.06 ± 0.22 | 4.65 ± 0.34 |
Heptadecanoic acid | C17:0 | 0.3 ± 0.05 | 0.27 ± 0.05 |
cis,cis-9,12-Hexadecadienoic acid | C16:2 | 0.89 a ± 0.02 | 0.41 b ± 0.25 |
Octadecanoic acid | C18:0 | 8.45 a ± 0.14 | 11.98 b ± 0.81 |
cis-9-Octadecenoic acid | C18:1 | 36.13 a ± 0.71 | 30.61 b ± 1.26 |
Octadecadienoic acid | C18:2 | 20.44 a ± 0.57 | 23.43 b ± 0.76 |
all cis-9,12,15-Octadecatrienoic acid | C18:3 (n − 3) | 2.58 a ± 0.05 | 3.27 b ± 0.19 |
Other fatty acids | 1.07 ± 0.17 | 0.98 ± 0.53 | |
MUFA | 41.19 a ± 0.92 | 35.27 b ± 1.51 | |
PUFA | 23.91 a ± 0.52 | 27.11 b ± 0.40 | |
SFA | 33.84 a ± 0.49 | 36.64 b ± 0.87 |
Parameters | Insect | |
---|---|---|
TM | GA | |
Polyphenols (mg GAE/100 g DM) | 567.92 ± 34.05 | 568.85 ± 31.15 |
TEAC ABTS •+ (μΜTrolox/1 g DM) | 47.3 a ± 0.42 | 89.94 b ± 0.7 |
RSA ABTS •+ (%) | 77.3 ± 0.42 | 71.2 ± 0.28 |
TEAC DPPH• (μΜTrolox/1 g DM) | 81.52 a ± 0.92 | 178.63 b ± 1.46 |
RSA DPPH• (%) | 76.15 ± 0.49 | 75.75 ± 0.35 |
TEAC TPTZ (FRAP) (μmolTrolox/1 g DM) | 65.27 ± 10.28 | 54.36 ± 7.18 |
Ingredient (g/kg) | AIN-93G (Control) | AIN-93G + 10% TM (TM) | AIN-93G + 10% GA (GA) |
---|---|---|---|
Casein | 200 | 146 | 144 |
Protein from insect | - | 54 | 56 |
Cornstarch | 533 | 533 | 533 |
Sucrose | 100 | 100 | 100 |
Cellulose | 50 | 44 | 43 |
Chitin from insect | - | 6 | 7 |
Soybean oil | 70 | 34 | 53 |
Fat from insect | - | 36 | 17 |
Vitamin mixture | 10 | 10 | 10 |
Mineral mixture | 35 | 35 | 35 |
Choline bitartrate | 2.5 | 2.5 | 2.5 |
t-butylhydroquinone | 0.014 | 0.014 | 0.014 |
TM | - | 100 | - |
GA | - | - | 100 |
Parameters | Experimental Groups | ||
---|---|---|---|
Control | TM | GA | |
Body weight (g) | 20.96 ± 1.37 | 20.39 ± 1.24 | 19.87 ± 1.99 |
Liver weight (g/100 g) | 4.18 ab ± 0.32 | 3.86 a ± 0.44 | 4.39 b ± 0.48 |
Blood glucose (mg/dL) | 132.30 ± 14.31 | 118.50 ± 22.01 | 132.82 ± 22.54 |
TC (mmol/L) | 20.58 ± 2.20 | 22.75 ± 2.51 | 21.92 ± 2.74 |
LDL (mmol/L) | 8.86 ± 1.01 | 9.14 ± 1.42 | 8.01 ± 2.21 |
HDL (mmol/L) | 1.00 ± 0.13 | 0.85 ± 0.45 | 0.85 ± 0.18 |
TAG (mmol/L) | 2.34 ± 0.58 | 1.85 ± 0.39 | 2.13 ± 0.47 |
Systematic Name (IUPAC) | Number of Carbon Atoms: Number π Bonds | Experimental Groups | ||
---|---|---|---|---|
Control | TM | GA | ||
Dodecanoic acid | C12:0 | 0.15 a ± 0.02 | 0.20 b ± 0.01 | 0.14 a ± 0.03 |
Tetradecanoic acid | C14:0 | 2.45 b ± 0.21 | 2.85 c ± 0.20 | 2.16 a ± 0.26 |
Pentadecanoic acid | C15:0 | 0.15 a ± 0.03 | 0.22 b ± 0.05 | 0.13 a ± 0.02 |
14-Methylpentadecanoic acid | C16:0 iso | 0.15 a ± 0.03 | 0.15 a ± 0.02 | 0.13 a ± 0.02 |
Hexadecanoic acid | C16:0 | 21.48 a ± 1.59 | 19.80 b ± 0.46 | 20.58 a,b ± 0.77 |
cis-9-Hexadecenoic acid | C16:1 | 3.30 a ± 0.68 | 4.43 b ± 0.61 | 3.21 a ± 0.56 |
Heptadecanoic acid | C17:0 | 0.37 a ± 0.08 | 0.51 b ± 0.07 | 0.44 a,b ± 0.08 |
cis-10-Heptadecanoic acid | C17:1 | 0.42 a ± 0.07 | 0.62 b ± 0.05 | 0.55 a ± 0.06 |
Octadecanoic acid | C18:0 | 12.42 a ± 1.60 | 11.70 a ± 1.61 | 13.25 a ± 1.67 |
cis-9-Octadecenoic acid | C18:1 | 29.03 a ± 0.84 | 32.96 c ± 0.46 | 30.41 b ± 1.09 |
Nonadecanoic acid | C19:0 | 0.13 a ± 0.09 | 0.20 a ± 0.06 | 0.21 a ± 0.08 |
cis,cis-9,12-Octadecadienoic acid | C18:2 (n − 6) | 23.96 a ± 1.09 | 21.07 b ± 1.20 | 23.26 a ± 1.33 |
all cis-6,9,12-Octadecatrienoic acid | C18:3 (n − 6) | 0.36 a ± 0.12 | 0.29 a ± 0.06 | 0.36 a ± 0.11 |
all cis-9,12,15-Octadecatrienoic acid | C18:3 (n−3) | 4.72 a ± 1.46 | 4.32 a ± 0.43 | 4.53 a ± 0.56 |
cis,cis-11,14-Eicosadienoic acid | C20:2 (n − 6) | 0.32 b ± 0.32 | 0.15 a,b ± 0.05 | 0.12 a ± 0.03 |
all cis-5,8,11,14-Eicosatetraenoic acid | C20:4 (n − 6) | 0.13 a ± 0.06 | 0.14 a ± 0.03 | 0.11 a ± 0.03 |
Other fatty acids | 0.33 a ± 0.17 | 0.29 a ± 0.17 | 0.37 a ± 0.08 | |
Total SFA | 37.30 a ± 1.42 | 35.64 a ± 1.41 | 37.04 a ± 1.75 | |
Total MUFA | 32.74 a ± 1.08 | 38.01 b ± 0.51 | 34.17 a ± 1.55 | |
Total PUFA | 29.63 a ± 1.37 | 26.06 b ± 1.17 | 28.43 a ±1.56 | |
18:2/18:3 (n−6/n−3) | 5.66 a ± 2.13 | 4.93 a ± 0.65 | 5.20 a ± 0.65 | |
18:1/18:0 | 2.37 a ± 0.30 | 2.86 b ± 0.39 | 2.33 a ± 0.35 | |
16:1/16:0 | 0.15 a ± 0.03 | 0.22 b ± 0.03 | 0.16 a ± 0.03 | |
16:0/14:0 | 8.84 a ± 0.96 | 6.97 b ± 0.51 | 9.69 a ± 1.45 | |
18:0/16:0 | 0.58 a ± 0.11 | 0.59 a ± 0.09 | 0.64 a ± 0.09 | |
16:0/18:2 | 0.90 a,b ± 0.05 | 0.94 b ± 0.05 | 0.89 a ± 0.05 |
Systematic Name (IUPAC) | Number of Carbon Atoms: Number π Bonds | Experimental Groups | ||
---|---|---|---|---|
Control | TM | GA | ||
Dodecanoic acid | C12:0 | 0.06 a ± 0.03 | 0.05 a ± 0.03 | 0.06 a ± 0.03 |
Tetradecanoic acid | C14:0 | 1.05 a ± 0.43 | 0.90 a ± 0.22 | 0.91 a ± 0.13 |
Pentadecanoic acid | C15:0 | 0.15 a ± 0.03 | 0.17 a ± 0.06 | 0.15 a ± 0.03 |
12-Methylpentadecanoic acid | C16:0 iso | 0.05 a ± 0.02 | 0.06 a ± 0.02 | 0.05 a ± 0.01 |
Hexadecanoic acid | C16:0 | 21.81 a ± 0.86 | 23.17 a ± 2.55 | 22.73 a ± 1.05 |
cis-9-Hexadecenoic acid | C16:1 | 3.84 b ± 1.33 | 3.19 a,b ± 1.03 | 2.69 a ± 0.60 |
cis,cis-9,12-Hexadecadienoic acid | C16:2 | 0.32 a ± 0.11 | 0.36 a ± 0.10 | 0.41 a ± 0.13 |
Heptadecanoic acid | C17:0 | 0.36 a ± 0.05 | 0.65 a ± 0.73 | 0.48 a ± 0.08 |
Octadecanoic acid | C18:0 | 9.81 a,b ± 0.89 | 9.42 a ± 1.25 | 10.77 b ± 1.02 |
cis-9-Octadecenoic acid | C18:1 | 28.80 a ± 1.16 | 31.76 b ± 0.77 | 28.58 a ± 1.05 |
cis,cis-9,12-Octadecadienoic acid | C18:2(n − 6) | 23.16 b ± 1.99 | 21.28 a ± 1.13 | 22.92 a,b ± 1.40 |
all cis-6,9,12-Octadecatrienoic acid | C18:3 (n − 6) | 1.07 a ± 0.28 | 0.84 a ± 0.25 | 0.95 a ± 0.18 |
all cis-9,12,15-Octadecatrienoic acid | C18:3 (n−3) | 3.22 b ± 0.47 | 2.55 a ± 0.79 | 3.09 a,b ± 0.45 |
cis,cis-11,14-Eicosadienoic acid | C20:2 (n − 6) | 0.74 a ±0.26 | 0.60 a ± 0.17 | 0.66 a ± 0.16 |
all cis-5,8,11,14-Eicosatetraenoic acid | C20:4 (n − 6) | 3.07 a ± 0.64 | 3.00 a ± 0.62 | 3.18 a ± 0.94 |
all cis-4,7,10,13,16-Docosapentaenoic acid (DPA) | C22:5 (n − 6) | 0.21 b ± 0.10 | 0.15 a,b ± 0.08 | 0.10 a ± 0.04 |
all cis-4,7,10,13,16,19-Docosahexaenoic acid (DHA) | C22:6 (n − 3) | 1.48 a ± 0.33 | 1.28 a ± 0.35 | 1.49 a ± 0.54 |
Other fatty acids | 0.49 a,b ± 0.14 | 0.37 a ± 0.15 | 0.55 b ± 0.17 | |
Total SFA | 33.29 a ± 1.62 | 34.40 a,b ± 1.77 | 35.14 b ± 1.28 | |
Total MUFA | 32.64 a ± 1.89 | 34.95 b ± 1.37 | 31.27 a ± 1.18 | |
Total PUFA | 33.58 a ± 2.27 | 30.28 b ± 1.70 | 33.04 a ± 1.92 | |
18:2/18:3 (n-6/n-3) | 7.35 a ± 1.41 | 11.44 a ± 11.91 | 7.55 a ± 1.14 | |
18:1/18:0 | 2.96 a ± 0.33 | 3.44 b ± 0.56 | 2.68 a ± 0.31 | |
16:1/16:0 | 0.18 b ± 0.06 | 0.14 a,b ± 0.05 | 0.12 a ± 0.02 | |
16:0/14:0 | 23.98 a ± 10.11 | 28.68 a ± 15.16 | 25.28 a ± 2.43 | |
18:0/16:0 | 0.45 a ± 0.04 | 0.41 a ± 0.09 | 0.48 a ± 0.05 | |
16:0/18:2 | 0.95 a ± 0.09 | 1.09 b ± 0.14 | 0.99 a,b ± 0.07 |
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Hassen, H.; Škvorová, P.; Pokhrel, K.; Kulma, M.; Piątkowska, E.; Kostogrys, R.B.; Kouřimská, L.; Tarko, T.; Franczyk-Żarów, M. Effect of Diets with the Addition of Edible Insects on the Development of Atherosclerotic Lesions in ApoE/LDLR−/− Mice. Int. J. Mol. Sci. 2024, 25, 7256. https://doi.org/10.3390/ijms25137256
Hassen H, Škvorová P, Pokhrel K, Kulma M, Piątkowska E, Kostogrys RB, Kouřimská L, Tarko T, Franczyk-Żarów M. Effect of Diets with the Addition of Edible Insects on the Development of Atherosclerotic Lesions in ApoE/LDLR−/− Mice. International Journal of Molecular Sciences. 2024; 25(13):7256. https://doi.org/10.3390/ijms25137256
Chicago/Turabian StyleHassen, Hayat, Petra Škvorová, Kshitiz Pokhrel, Martin Kulma, Ewa Piątkowska, Renata B. Kostogrys, Lenka Kouřimská, Tomasz Tarko, and Magdalena Franczyk-Żarów. 2024. "Effect of Diets with the Addition of Edible Insects on the Development of Atherosclerotic Lesions in ApoE/LDLR−/− Mice" International Journal of Molecular Sciences 25, no. 13: 7256. https://doi.org/10.3390/ijms25137256