Supplementation of Sulfur-Containing Amino Acids or Essential Amino Acids Does Not Reverse the Hepatic Lipid-Lowering Effect of a Protein-Rich Insect Meal in Obese Zucker Rats
Open accessAbstract
The present study tested the hypothesis that the liver lipid-lowering effect of insect meal (IM) is caused by its low methionine concentration. A total of fifty, male obese Zucker rats were randomly assigned to five groups of 10 rats each (casein (C), IM, IM + Met, IM + Cys, and IM + EAA). While group C received a diet with casein, the IM-fed groups received a diet with IM as the protein source. In groups IM + Met, IM + Cys and IM + EAA, the diets were additionally supplemented with methionine, cysteine and essential amino acids (EAA), respectively. Hepatic concentrations of triacylglycerols and cholesterol, and hepatic mRNA levels and activities of lipogenic and cholesterogenic enzymes were markedly lower in the IM-fed groups than in group C (p < 0.05). All of these parameters either did not differ across the IM-fed groups or were only slightly higher in groups IM + Met, IM + Cys and IM+EAA than in the group IM. In conclusion, the results indicate that a difference in the amino acid composition between IM and casein, a low concentration of methionine in IM and a reduced cysteine synthesis secondary to a decreased methionine availability resulting from feeding IM are not causative for the lipid-lowering effect of IM.
AI snapshot
Written from the paper’s full text.
TL;DR
In obese Zucker rats, replacing casein with *Tenebrio molitor* insect meal (IM) lowered hepatic triacylglycerol and cholesterol and inhibited lipogenic/cholesterogenic gene expression and enzyme activity. Supplementing the IM diet with methionine, cysteine, or essential amino acids did not reverse these effects, indicating that IM’s amino acid composition is not the cause of its lipid-lowering action.
Key findings
- IM feeding reduced hepatic triacylglycerol by up to 70% and cholesterol by up to 50% versus casein (p < 0.05).
- Hepatic mRNA levels of lipogenic and cholesterogenic genes were lower by 40% to 90% in all IM-fed groups than in the casein group; FASN and G6PD activities were 50% and 35% lower, respectively, in group IM versus casein (p < 0.05).
- Hepatic TG and cholesterol in IM + Met and IM + Cys did not differ from IM; IM + EAA had higher hepatic TG than IM but still clearly lower than casein.
- Hepatic methionine, SAM, and SAH did not differ between groups, while cysteine and total glutathione were reduced in IM versus casein (p < 0.05).
Methods
- Fifty male, 10-week-old obese Zucker rats were randomly assigned to five groups of 10: casein (C), insect meal (IM), IM + methionine, IM + cysteine, and IM + essential amino acids; diets were fed for 4 weeks.
- IM was from *Tenebrio molitor* L. and replaced casein isonitrogenously; diets were adjusted for methionine, cysteine, EAA, and major fatty acids as described.
- Hepatic lipids, mRNA expression by qPCR, enzyme activities (FASN, G6PD), methionine metabolites, and plasma amino acids were measured; data analyzed by one-way ANOVA with Fisher’s multiple comparison test (p < 0.05).
Limitations
- The paper does not include an explicit limitations section.
- Evident from the text: only male obese Zucker rats were studied, feeding lasted 4 weeks, and hepatic HMGCR activity was not determined in this experiment (the authors state this and cite prior work).
- The authors state that future studies are needed to test other IM components, such as chitin (approximately 3.4% of the IM diet), bioactive peptides, and ecdysteroids, as possible causes of the lipid-lowering effect.
Model-written summary. Check it against the paper before relying on it.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
0 of 10 cited sources checked · 0 supported · 0 flagged
- Findingown data
Hepatic TG concentration was still clearly lower in group IM+EAA than in group C.
“Nevertheless, the observation that the hepatic TG concentration was still clearly lower in group IM + EAA than in group C suggests that the hepatic lipid-lowering effect of IM cannot be substantially explained by a reduced availability of EAA from the IM.”
Quote in the paperSubstantial claim - Findingown data
Hepatic cholesterol concentration did not differ between group IM+EAA and group IM.
“While the hepatic concentration of cholesterol did not differ between groups IM + EAA and IM, the hepatic TG concentration was higher in group IM+EAA than in group IM (p < 0.05, Figure 1a).”
Quote in the paperSubstantial claim - Findingown data
Replacement of casein by insect meal (IM) as the dietary protein source caused a marked reduction of hepatic triacylglycerol (TG) concentration in obese Zucker rats (up to 70%, p < 0.05).
“Hepatic concentrations of triacylglycerols and cholesterol, and hepatic mRNA levels and activities of lipogenic and cholesterogenic enzymes were markedly lower in the IM-fed groups than in group C (p < 0.05).”
- Also stated in: § 3.3. The Effect of IM, without and with Adjustment of Dietary Amino Acids, on Hepatic Lipid Concentrations and the Expression and Activities of Lipogenic and Cholesterogenic Enzymes · plain
“As shown in Figure 1a, the replacement of casein by IM as the dietary protein source caused a marked reduction of hepatic TG (up to 70%) and cholesterol (up to 50%) concentrations in obese Zucker rats (p < 0.05).”
Quote in the paperSubstantial claim - Also stated in: § 3.3. The Effect of IM, without and with Adjustment of Dietary Amino Acids, on Hepatic Lipid Concentrations and the Expression and Activities of Lipogenic and Cholesterogenic Enzymes · plain
- Findingown data
Hepatic mRNA levels of lipogenic and cholesterogenic genes (Acaca, Elovl5, Elovl6, Fads1, Fads2, Fasn, G6pd, Scd, Hmgcr and Sqle) were markedly lower (from 40% up to 90%) in IM-fed groups than in group C.
“As shown in Figure 1b, the mRNA levels of lipogenic (Acaca, Elovl5, Elovl6, Fads1, Fads2, Fasn, G6pd and Scd) and cholesterogenic genes (Hmgcr and Sqle) in the liver were markedly lower (from 40% up to 90%) in group IM and the other IM-fed groups (IM + Met, IM + Cys, and IM + EAA) than in group C.”
Quote in the paperSubstantial claim - Findingown data
Hepatic mRNA levels of Fads1, Fads2, G6pd and Sqle in groups IM+Met, IM+Cys and IM+EAA were still clearly below those in group C.
“whereas the mRNA levels of Fads1, Fads2, G6pd and Sqle in the liver were higher in groups IM + Met, IM + Cys and IM + EAA than in group IM (p < 0.05, Figure 1b), but were still clearly below those in group C.”
Quote in the paperSubstantial claim
- Findingown data
Hepatic TG concentration did not differ between group IM+Cys and group IM.
“In contrast to our hypothesis, hepatic concentrations of TG and cholesterol in groups IM + Met and IM + Cys did not differ from those in group IM.”
Quote in the paperSubstantial claim - Findingown data
Hepatic total glutathione concentration was reduced in group IM compared to group C (p < 0.05).
“In contrast, the hepatic concentrations of cysteine and total glutathione, but not homocysteine, were reduced in group IM compared to in group C (p < 0.05, Figure 2)”
Quote in the paperSubstantial claim - Findingown data
Hepatic cholesterol concentration did not differ between group IM+Met and group IM.
“In contrast to our hypothesis, hepatic concentrations of TG and cholesterol in groups IM + Met and IM + Cys did not differ from those in group IM.”
Quote in the paperSubstantial claim - Findingown data
Hepatic mRNA levels of Acaca, Elovl5, Elovl6, Fasn, Hmgcr and Scd did not differ across the IM-fed groups (IM, IM+Met, IM+Cys, IM+EAA).
“The mRNA levels of most of these genes (Acaca, Elovl5, Elovl6, Fasn, Hmgcr and Scd) did not differ across the groups fed IM, without or with adjustment of dietary amino acids (groups IM, IM + Met, IM + Cys, and IM + EAA)”
Quote in the paperSubstantial claim - Findingown data
Hepatic TG concentration did not differ between group IM+Met and group IM.
“In contrast to our hypothesis, hepatic concentrations of TG and cholesterol in groups IM + Met and IM + Cys did not differ from those in group IM.”
Quote in the paperSubstantial claim - Findingown data
Hepatic glucose-6-phosphate dehydrogenase (G6PD) activity was lower in group IM than in group C by 35% (p < 0.05).
“The hepatic activities of two lipogenic enzymes (FASN and G6PD) were also markedly lower in group IM than in group C (50% and 35%, respectively; p < 0.05, Figure 1c)”
Quote in the paperSubstantial claim - Findingown data
Hepatic cysteine concentration was reduced in group IM compared to group C (p < 0.05).
“In contrast, the hepatic concentrations of cysteine and total glutathione, but not homocysteine, were reduced in group IM compared to in group C (p < 0.05, Figure 2)”
Quote in the paperSubstantial claim - Findingown data
Hepatic TG concentration was higher in group IM+EAA than in group IM (p < 0.05).
“While the hepatic concentration of cholesterol did not differ between groups IM + EAA and IM, the hepatic TG concentration was higher in group IM+EAA than in group IM (p < 0.05, Figure 1a).”
Quote in the paperSubstantial claim - Findingown data
Hepatic fatty acid synthase (FASN) activity was lower in group IM than in group C by 50% (p < 0.05).
“The hepatic activities of two lipogenic enzymes (FASN and G6PD) were also markedly lower in group IM than in group C (50% and 35%, respectively; p < 0.05, Figure 1c)”
Quote in the paperSubstantial claim - Findingown data
Hepatic homocysteine concentration did not differ between group IM and group C.
“In contrast, the hepatic concentrations of cysteine and total glutathione, but not homocysteine, were reduced in group IM compared to in group C (p < 0.05, Figure 2)”
Quote in the paperNot a substantial claim - Findingown data
Hepatic concentrations of methionine, SAM and SAH did not differ between rats of all groups, including group C and group IM, despite dietary methionine supply being 40% lower in group IM than in group C.
“The present study shows that the hepatic concentrations of methionine and its demethylation metabolites SAM and SAH did not differ between rats of all groups, and even not between rats of group C and group IM (Table S2), despite the dietary methionine supply being 40% lower in group IM than in group C (Figure 2).”
Quote in the paperSubstantial claim - Findingown data
Hepatic mRNA levels of Fads1, Fads2, G6pd and Sqle were higher in groups IM+Met, IM+Cys and IM+EAA than in group IM (p < 0.05).
“whereas the mRNA levels of Fads1, Fads2, G6pd and Sqle in the liver were higher in groups IM + Met, IM + Cys and IM + EAA than in group IM (p < 0.05, Figure 1b), but were still clearly below those in group C.”
Quote in the paperSubstantial claim - Findingown data
Replacement of casein by insect meal (IM) as the dietary protein source caused a marked reduction of hepatic cholesterol concentration in obese Zucker rats (up to 50%, p < 0.05).
“Hepatic concentrations of triacylglycerols and cholesterol, and hepatic mRNA levels and activities of lipogenic and cholesterogenic enzymes were markedly lower in the IM-fed groups than in group C (p < 0.05).”
- Also stated in: § 3.3. The Effect of IM, without and with Adjustment of Dietary Amino Acids, on Hepatic Lipid Concentrations and the Expression and Activities of Lipogenic and Cholesterogenic Enzymes · plain
“As shown in Figure 1a, the replacement of casein by IM as the dietary protein source caused a marked reduction of hepatic TG (up to 70%) and cholesterol (up to 50%) concentrations in obese Zucker rats (p < 0.05).”
Quote in the paperSubstantial claim - Also stated in: § 3.3. The Effect of IM, without and with Adjustment of Dietary Amino Acids, on Hepatic Lipid Concentrations and the Expression and Activities of Lipogenic and Cholesterogenic Enzymes · plain
- Findingown data
Hepatic cholesterol concentration did not differ between group IM+Cys and group IM.
“In contrast to our hypothesis, hepatic concentrations of TG and cholesterol in groups IM + Met and IM + Cys did not differ from those in group IM.”
Quote in the paperSubstantial claim - Findingown data
Relative liver weights did not differ between groups.
“In addition, relative liver weights did not differ between groups (Table 4).”
Quote in the paperNot a substantial claim - Findingown data
The replacement of casein by IM as a dietary protein source caused a different amino acid composition between the diet of group C and the IM-containing diets.
“As expected, the replacement of casein by IM as a dietary protein source caused a different amino acid composition between the diet of group C and the IM-containing diets (IM, IM + Met, IM + Cys, and IM + EAA; Table 3).”
Quote in the paperNot a substantial claim - Findingnone given
IM has a low methionine concentration when compared to other animal proteins.
“One typical characteristic of IM is its low methionine concentration when compared to other animal proteins.”
Quote in the paperSubstantial claim - Findingown data
Growth performance parameters (final BW, daily BW gain, feed intake and feed to gain ratio) did not differ between group C and the groups fed the IM-containing diets.
“growth performance parameters (final BW, daily BW gain, feed intake and feed to gain ratio) did not differ between group C and the groups fed the IM-containing diets (Table 4).”
Quote in the paperNot a substantial claim - Interpretationown data
The strong liver lipid-lowering effect of IM cannot be substantially reversed by the increased supply of cysteine to the IM diet.
“the increased supply of cysteine to the IM diet”
Quote in the paperSubstantial claim - Study design and conductreasoning
The metabolic effects induced by the IM-containing diets were not confounded by different levels of specific fatty acids between the diet of group C and the IM-containing diets.
“Thus, it is highly unlikely that the metabolic effects induced by the IM-containing diets were confounded by different levels of specific fatty acids between the diet of group C and the IM-containing diets.”
Quote in the paperSubstantial claim - Interpretationreasoning
The α-linolenic acid content is not relevant for the lipid-lowering action of IM.
“we exclude the possibility that the α-linolenic acid content is of relevance for the lipid-lowering action of IM.”
Quote in the paperSubstantial claim - Interpretationreasoning
The inhibitory effect of IM on hepatic lipid synthesis likely does not disappear by the combined ingestion of IM and other dietary proteins rich in sulfur-containing amino acids or EAA.
“A practical consequence of our findings is that the inhibitory effect of IM on hepatic lipid synthesis likely does not disappear by the combined ingestion of IM and other dietary proteins rich in sulfur-containing amino acids or EAA.”
Quote in the paperSubstantial claim - Interpretationown data
A low concentration of methionine in IM is not causative for the lipid-lowering effect of IM.
“This indicates that a difference in the amino acid composition between IM and casein, a low concentration of methionine in IM and a reduced cysteine synthesis secondary to a decreased methionine availability resulting from feeding IM are not causative for the lipid-lowering effect of IM.”
Quote in the paperSubstantial claim - Study design and conductown data
The metabolic effects induced by feeding the IM-containing diets were not biased by differences in the final BWs and BW gain of the rats.
“Thus, these findings suggest that the metabolic effects induced by feeding the IM-containing diets in the present study were not biased by differences in the final BWs and BW gain of the rats.”
Quote in the paperSubstantial claim - Premisecitation
Feeding IM from Tenebrio molitor instead of casein causes a marked attenuation of liver steatosis and hyperlipidemia due to the inhibition of hepatic TG and cholesterol synthesis in obese Zucker rats.
“Interestingly, we have recently demonstrated in two studies with obese Zucker rats that feeding IM from Yellow mealworm (Tenebrio molitor L.) instead of casein as a protein source also causes a marked attenuation of liver steatosis and hyperlipidemia due to the inhibition of hepatic triacylglycerol (TG) and cholesterol synthesis [14,15].”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [14] Gessner, 2019, Insect Meal as Alternative Protein Source Exerts Pronounced Lipid-Lowering Effects in Hyperlipidemic Obese Zucker Rats, J. Nutr. source
Not checked in the free run.
- cites [15] Meyer, 2019, The Antisteatotic and Hypolipidemic Effect of Insect Meal in Obese Zucker Rats is Accompanied by Profound Changes in Hepatic Phospholipid and 1-Carbon Metabolism, Mol. Nutr. Food Res. source
Not checked in the free run.
- Interpretationown data
The strong liver lipid-lowering effect of IM cannot be substantially reversed by adjustment of the dietary methionine concentration between the IM diet and the casein diet.
“The present study clearly shows that the strong liver lipid-lowering effect of IM cannot be substantially reversed by either the adjustment of the dietary methionine concentration between the IM diet and the casein diet”
Quote in the paperSubstantial claim - Premisecitation
Feeding low levels of methionine (methionine restriction) causes a strong inhibition of hepatic lipid synthesis and a lowering of blood lipid levels in laboratory animals.
“Noteworthily, studies in laboratory animals showed that feeding low levels of methionine (“methionine restriction”) causes a strong inhibition of hepatic lipid synthesis and a lowering of blood lipid levels [16,17,18]”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [16] Orentreich, 1993, Low methionine ingestion by rats extends life span, J. Nutr.
Not checked in the free run.
- cites [17] Richie, 1994, Methionine restriction increases blood glutathione and longevity in F344 rats, FASEB J. source
Not checked in the free run.
- cites [18] Perrone, 2010, Methionine restriction effects on mitochondrial biogenesis and aerobic capacity in white adipose tissue, liver, and skeletal muscle of F344 rats, Metabolism source
Not checked in the free run.
- Interpretationreasoning
A difference in the amino acid composition between IM and casein is not causative for the lipid-lowering effect of IM.
“This indicates that a difference in the amino acid composition between IM and casein, a low concentration of methionine in IM and a reduced cysteine synthesis secondary to a decreased methionine availability resulting from feeding IM are not causative for the lipid-lowering effect of IM.”
Quote in the paperSubstantial claim - Interpretationown data
A reduced availability of sulfur-containing amino acids or EAA from IM does not significantly contribute to the marked lipid-lowering effect of IM.
“In line with the effects on hepatic TG and cholesterol concentrations, these results strongly suggest that a reduced availability of sulfur-containing amino acids or EAA from IM does not significantly contribute to the marked lipid-lowering effect of IM.”
Quote in the paperSubstantial claim - Interpretationown data
A reduced cysteine synthesis secondary to a decreased methionine availability resulting from feeding IM is not causative for the lipid-lowering effect of IM.
“This indicates that a difference in the amino acid composition between IM and casein, a low concentration of methionine in IM and a reduced cysteine synthesis secondary to a decreased methionine availability resulting from feeding IM are not causative for the lipid-lowering effect of IM.”
Quote in the paperSubstantial claim - Interpretationown data
The strong liver lipid-lowering effect of IM cannot be substantially reversed by the adjustment of the dietary concentrations of EAA between the IM diet and the casein diet.
“or the adjustment of the dietary concentrations of EAA between the IM diet and the casein diet.”
Quote in the paperSubstantial claim
- Classified as probably not a substantial claim. 9
- May combine two claims. 6
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
FindingreasoningThe concentrations of most EAA (histidine, leucine, lysine, methionine, phenylalanine, threonine and tryptophan) were similar between the diets of group C and group IM+EAA, except for isoleucine and valine, which were slightly lower in the diet of group IM+EAA than in the diet of group C.
“Due to adjustment of the concentrations of EAA between the diets of group C and group IM + EAA, the concentrations of most EAA (histidine, leucine, lysine, methionine, phenylalanine, threonine and tryptophan) were similar between the diets of these groups, except for isoleucine and valine, which were slightly lower in the diet of group IM + EAA than in the diet of group C.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataHepatic concentrations of cysteine, glutathione and homocysteine were either higher in groups IM+Met, IM+Cys and IM+EAA than in group C, or did not differ between these groups.
“In contrast, the hepatic concentrations of cysteine, glutathione and homocysteine were either higher in groups IM + Met, IM + Cys and IM + EAA than in group C, or did not differ between these groups”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
FindingreasoningThe concentration of cysteine was higher in the diet of group IM+Cys than in the diet of group C and in the other IM-containing diets.
“Owing to supplementation of cysteine, the concentration of cysteine was higher in the diet of group IM + Cys than in the diet of group C and in the other IM-containing diets.”
Quote in the paperNot a substantial claimMay combine two claims.
FindingreasoningThe concentration of methionine was lower in the diets of groups IM and IM+Cys than in the diet of group C, but was similar between the diets of groups IM+Met and C.
“The concentration of methionine was lower in the diets of groups IM and IM + Cys than in the diet of group C, but was similar between the diets of groups IM + Met and C due to the adjustment of the methionine concentration between these diets.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe concentration of α-linolenic acid slightly differed between the diet of group C and the IM-containing diets, and was lower in the IM-containing diets than in the diet of group C.
“Only the concentration of α-linolenic acid, which was reported to cause hypolipidemic effects in rats [32], slightly differed between the diet of group C and the IM-containing diets. However, since the dietary concentration of α-linolenic acid was even lower in the IM-containing diets than in diet of group C”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [32] Su, 2016, Hypolipidemic Activity of Peony Seed Oil Rich in α-Linolenic, is Mediated Through Inhibition of Lipogenesis and Upregulation of Fatty Acid β-Oxidation, J. Food Sci. source
Not checked in the free run.
May combine two claims.
InterpretationreasoningIM causes a profound inhibition of hepatic lipogenesis and cholesterogenesis.
“Thus, based on the current and our recent findings from gene expression and enzyme activity measurements in the liver, IM causes a profound inhibition of hepatic lipogenesis and cholesterogenesis.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [14] Gessner, 2019, Insect Meal as Alternative Protein Source Exerts Pronounced Lipid-Lowering Effects in Hyperlipidemic Obese Zucker Rats, J. Nutr. source
Not checked in the free run.
- Rests on an assumption: Hepatic mRNA levels and activities of lipogenic and cholesterogenic enzymes reflect the rates of hepatic lipogenesis and cholesterogenesis.
Classified as probably not a substantial claim.
Study design and conductnone givenFive semisynthetic diets with comparable levels of gross energy and crude nutrients were fed.
“Five semisynthetic diets with comparable levels of gross energy and crude nutrients were fed (Table 1).”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Study design and conductreasoningThe concentrations of crude fat and the main fatty acids were adjusted across the diet of group C and the IM-containing diets.
“In order to adjust the concentrations of crude fat and the main fatty acids across the diet of group C and the IM-containing diets, the diet of group C contained 5% soybean oil and the IM-containing diets 1.92% safflower oil and 0.38% linseed oil.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
PremisecitationCysteine supplementation reverses the effects of methionine restriction on the expression of genes involved in lipid synthesis.
“Cysteine supplementation was found to reverse the effects of methionine restriction on the expression of genes involved in lipid synthesis [25]”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [25] Elshorbagy, 2011, Cysteine supplementation reverses methionine restriction effects on rat adiposity: Significance of stearoyl-coenzyme A desaturase, J. Lipid Res. source
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
PremisecitationMethionine supplementation causes the opposite and exerts a marked hyperlipidemic action.
“whereas methionine supplementation causes the opposite and exerts a marked hyperlipidemic action [19].”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [19] Hirche, 2006, Effect of dietary methionine on plasma and liver cholesterol concentrations in rats and expression of hepatic genes involved in cholesterol metabolism, Br. J. Nutr. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductcitationThe three most stable reference genes (Actb, Canx and Mdh1) were used to calculate GeNorm normalization factors.
“The three most stable reference genes used to calculate GeNorm normalization factors according to [28] were: Actb, Canx and Mdh1.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [28] Vandesompele, 2002, Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes, Genome Biol. source
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe rats were randomly assigned to five groups of 10 rats each.
“The rats were randomly assigned to five groups of 10 rats each (casein (C), IM, IM + Met, IM + Cys, and IM + EAA).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenAll data were checked for normality of distribution by Anderson-Darling test.
“All data were checked for normality of distribution by Anderson-Darling test.”
Quote in the paperNot a substantial claim
The paper relies on this without support.
The study had sufficient statistical power to detect a reversal of the lipid-lowering effect of IM by methionine, cysteine or EAA supplementation.
“Data were analyzed by one-way ANOVA followed by Fisher´s multiple comparison test. Differences were considered significant at p < 0.05.”
The paper relies on this without support.
The supplemented methionine, cysteine and EAA were bioavailable and reached the liver at levels sufficient to reverse the lipid-lowering effect if these amino acids were causative.
“In groups IM + Met, IM + Cys and IM + EAA, the diets were additionally supplemented with methionine, cysteine and essential amino acids (EAA), respectively.”
The paper relies on this without support.
Hepatic mRNA levels and activities of lipogenic and cholesterogenic enzymes reflect the rates of hepatic lipogenesis and cholesterogenesis.
“Thus, based on the current and our recent findings from gene expression and enzyme activity measurements in the liver, IM causes a profound inhibition of hepatic lipogenesis and cholesterogenesis.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The characteristically low methionine concentration of insect meal or a decreased cysteine synthesis secondary to a reduced methionine availability are not causative for the lipid-lowering effects of insect meal in obese Zucker rats.
“we have shown recently that the characteristically low methionine concentration of insect meal or a decreased cysteine synthesis secondary to a reduced methionine availability are not causative [30]”
From Effect of Ecdysterone on the Hepatic Transcriptome and Lipid Metabolism in Lean and Obese Zucker Rats (2021) · cites this paper as [30]
Feeding of protein-rich insect meal produced from Tenebrio molitor markedly decreases liver and/or plasma lipids in obese Zucker rats.
“recent reports showed that feeding of protein-rich insect meal produced from industrialised mass-rearing of the edible species Tenebrio molitor markedly decreases liver and/or plasma lipids in obese Zucker rats [17,18,30].”
From Effect of Ecdysterone on the Hepatic Transcriptome and Lipid Metabolism in Lean and Obese Zucker Rats (2021) · cites this paper as [30]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Abstract implies cholesterogenic enzyme activity was measured
MinorThe abstract reports lower activities of lipogenic and cholesterogenic enzymes, but the results explicitly say that activity of the cholesterogenic enzyme HMGCR was not determined in this study.
“Hepatic concentrations of triacylglycerols and cholesterol, and hepatic mRNA levels and activities of lipogenic and cholesterogenic enzymes were markedly lower in the IM-fed groups than in group C (p < 0.05).”
“In the present study, the hepatic activity of the cholesterogenic enzyme HMGCR was not determined”
Cites
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., & Speleman, F. (2002) · Genome Biology · doi:10.1186/gb-2002-3-7-research0034 · Cited by 20,038 · see citing works
The environmental sustainability of insects as food and feed. A review
van Huis, A., & Oonincx, D. G. A. B. (2017) · Agronomy for Sustainable Development · doi:10.1007/s13593-017-0452-8 · Cited by 1,043 · see citing works
Oonincx, D. G. A. B., & de Boer, I. J. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051145 · Cited by 959 · see citing works
Werstuck, G. H., Lentz, S. R., Dayal, S., Hossain, G. S., Sood, S. K., Shi, Y., Zhou, J., Maeda, N., Krisans, S. K., Malinow, M. R., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci11596 · Cited by 702 · see citing works
Low methionine ingestion by rats extends life span.
Orentreich, N., Matias, J. R., Felice, A. D., & Zimmerman, J. (1993) · Journal of NutriLife · doi:10.1093/jn/123.2.269 · Cited by 608 · see citing works
Methionine restriction increases blood glutathione and longevity in F344 rats
Richie, J. P., Leutzinger, Y., Parthasarathy, S., Maixoy, V., Orentreich, N., & Zimmerman, J. A. (1994) · The FASEB Journal · doi:10.1096/fasebj.8.15.8001743 · Cited by 363 · see citing works
Wu, G., Fanzo, J., Miller, D. D., Pingali, P., Post, M. J., Steiner, J. L., & Thalacker‐Mercer, A. E. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12500 · Cited by 342 · see citing works
[6] Fatty acid synthase from rat liver
Nepokroeff, C. M., Lakshmanan, M. R., & Porter, J. W. (1975) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(75)35136-7 · Cited by 270 · see citing works
Soy Protein Affects Serum Insulin and Hepatic SREBP-1 mRNA and Reduces Fatty Liver in Rats
Ascencio, C., Torres, N., Isoard, F., Tovar, A. R., Gomez-Perez, F. J., & Hernández‐Pando, R. (2004) · Journal of Nutrition · doi:10.1093/jn/134.3.522 · Cited by 260 · see citing works
Biasato, I., Renna, M., Gai, F., Dabbou, S., Meneguz, M., Perona, G. E., Martínez-Miró, S., Barroeta, A. C., Bergagna, S., Sardi, L., et al. (2019) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-019-0325-x · Cited by 211 · see citing works
Elshorbagy, A. K., Valdivia-Garcia, M., Mattocks, D. A. L., Plummer, J. D., Smith, A. D., Drevon, C. A., Refsum, H., & Perrone, C. E. (2011) · Journal of Lipid Research · doi:10.1194/jlr.m010215 · Cited by 177 · see citing works
Perrone, C. E., Mattocks, D. A. L., Jarvis-Morar, M., Plummer, J. D., & Orentreich, N. (2010) · Metabolism · doi:10.1016/j.metabol.2009.10.023 · Cited by 136 · see citing works
Martinez‐Uña, M., Varela‐Rey, M., Cano, A., Fernández-Ares, L., Beraza, N., Aurrekoetxea, I., Martínez‐Arranz, I., García‐Rodríguez, J. L., Buqué, X., Mestre, D., et al. (2013) · Hepatology · doi:10.1002/hep.26399 · Cited by 126 · see citing works
Jin, X. H., Heo, P. S., Hong, J., Kim, N. J., & Kim, Y.-E. (2016) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.15.0535 · Cited by 126 · see citing works
Dietary chitosan improves hypercholesterolemia in rats fed high-fat diets
Zhang, J., Liu, J., Li, L., & Xia, W. (2008) · Nutrition Research · doi:10.1016/j.nutres.2007.12.013 · Cited by 125 · see citing works
Chitosan Supplementation and Fecal Fat Excretion in Men
Gades, M. D., & Stern, J. S. (2003) · Obesity Research · doi:10.1038/oby.2003.97 · Cited by 117 · see citing works
20-Hydroxyecdysone decreases weight and hyperglycemia in a diet-induced obesity mice model
Kizelsztein, P., Govorko, D., Komarnytsky, S., Evans, A., Wang, Z., Cefalu, W. T., & Raskin, I. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90772.2008 · Cited by 117 · see citing works
Parr, M. K., Zhao, P., Haupt, O., Ngueu, S. T., Hengevoss, J., Fritzemeier, K. H., Piechotta, M., Schlörer, N., Muhn, P., Zheng, W., et al. (2014) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201300806 · Cited by 106 · see citing works
Multi-Functional Roles of Chitosan as a Potential Protective Agent against Obesity
Walsh, A. M., Sweeney, T., Bahar, B., & O’Doherty, J. V. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053828 · Cited by 104 · see citing works
Sulfur amino acids in methionine-restricted rats: Hyperhomocysteinemia
Elshorbagy, A. K., Valdivia‐Garcia, M., Refsum, H., Smith, A. D., Mattocks, D. A. L., & Perrone, C. E. (2010) · Nutrition · doi:10.1016/j.nut.2009.09.017 · Cited by 96 · see citing works
Onomi, S., Okazaki, Y., & Katayama, T. (2004) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.68.1379 · Cited by 94 · see citing works
The Membrane Lipid Phosphatidylcholine Is an Unexpected Source of Triacylglycerol in the Liver
van der Veen, J. N., Lingrell, S., & Vance, D. E. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.381723 · Cited by 84 · see citing works
Manzoni, C., Duranti, M. M., Eberini, I., Scharnag, H., März, W., Castiglioni, S., & Lovati, M. R. (2003) · Journal of Nutrition · doi:10.1093/jn/133.7.2149 · Cited by 82 · see citing works
Shukla, A., Brandsch, C., Bettzieche, A., Hirche, F., Stangl, G. I., & Eder, K. (2006) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2006.05.007 · Cited by 80 · see citing works
Self-citationMeyer, S., Geßner, D. K., Braune, M. S., Friedhoff, T., Most, E., Höring, M., Liebisch, G., Zorn, H., Eder, K., & Ringseis, R. (2020) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-020-0425-7 · Cited by 77 · see citing works
Self-citationHirche, F., Schröder, A., Knoth, B., Stangl, G. I., & Eder, K. (2006) · British Journal Of Nutrition · doi:10.1079/bjn20061729 · Cited by 68 · see citing works
Self-citationFoucault, A.-S., Even, P., Lafont, R., Dioh, W., Veillet, S., Tomé, D., Huneau, J.-F., Hermier, D., & Quignard-Boulangé, A. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.02.002 · Cited by 68 · see citing works
Su, J., Ma, C., Liu, C., Gao, C., Nie, R., & Wang, H. (2016) · Journal of Food Science · doi:10.1111/1750-3841.13252 · Cited by 62 · see citing works
Gessner, D. K., Schwarz, A., Meyer, S., Wen, G., Most, E., Zorn, H., Ringseis, R., & Eder, K. (2019) · The Journal of Nutrition · doi:10.1093/jn/nxy256 · Cited by 53 · see citing works
Self-citationBettzieche, A., Brandsch, C., Weiße, K., Hirche, F., Eder, K., & Stangl, G. I. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507857266 · Cited by 51 · see citing works
Self-citationBurren, K. A., Mills, K. A., Copp, A. J., & Greene, N. D. E. (2006) · Journal of Chromatography B · doi:10.1016/j.jchromb.2006.07.012 · Cited by 47 · see citing works
Spielmann, J., Stangl, G. I., & Eder, K. (2008) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/j.1439-0396.2007.00766.x · Cited by 46 · see citing works
Self-citationGhosh, S., Forney, L. A., Wanders, D., Stone, K. P., & Gettys, T. W. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177513 · Cited by 44 · see citing works
Meyer, S., Gessner, D. K., Wen, G., Most, E., Liebisch, G., Zorn, H., Ringseis, R., & Eder, K. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201801305 · Cited by 23 · see citing works
Self-citationAutomatic amino acid analysis of blood serum and plasma
DeWolfe, M. S., Baskurt, S., & Cochrane, W. A. (1967) · Clinical Biochemistry · doi:10.1016/s0009-9120(67)80009-2 · Cited by 20 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- VDLUFA (Verband Deutscher Landwirtschaftlicher Untersuchungs- und Forschungsanstalten) (2007). Die chemische Untersuchung von Futtermitteln. VDLUFA-Methodenbuch. Band III, Ergänzungslieferungen von 1983, 1988, 1992, 1997, 2004, 2006, 2007, VDLUFA-Verlag.
- National Research Council (1995). Nutrient Requirements of Laboratory Animals, National Academy Press. [4th ed.].
- Delbecque, 1975, Dosage de la β-ecdysone par fragmentographie de masse au cours du dernier stade larvaire de Tenebrio molitor L (Insecte, Coléoptère), C. R. Acad. Sci. Paris, 281, 309
Cited by
Sorted by citations
Saeb, A., Grundmann, S. M., Geßner, D. K., Schuchardt, S., Most, E., Wen, G., Eder, K., & Ringseis, R. (2022) · Food & Function · doi:10.1039/d1fo03920b · Cited by 29 · see citing works
Self-citationMeyer, S., Gessner, D. K., Wen, G., Most, E., Liebisch, G., Zorn, H., Ringseis, R., & Eder, K. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201801305 · Cited by 23 · see citing works
Self-citationMarschall, M. J. M., Ringseis, R., Gessner, D. K., Grundmann, S. M., Most, E., Wen, G., Maheshwari, G., Zorn, H., & Eder, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105241 · Cited by 13 · see citing works
Self-citationMarschall, M. J. M., Grundmann, S. M., Geßner, D. K., Wen, G., Most, E., Eder, K., & Ringseis, R. (2023) · Nutrients · doi:10.3390/nu15020287 · Cited by 9 · see citing works
Self-citationTenebrio molitor-derived ingredients in obesity management: The new frontier of nutrition and health
Paulino, P. R., Cocato, M. L., & Sarkis, J. E. D. S. (2025) · Dietary Supplements and Nutraceuticals · doi:10.31989/dsn.v4i10.1751 · Cited by 3 · see citing works
A systematic review of the health effects of edible insects in human and mammalian nutrition
da Silva, C. B., Troyer, T. D., Paepe, E. D., Hesta, M., Vanhaecke, L., & Hemeryck, L. Y. (2026) · Journal of Insects as Food and Feed · doi:10.1163/23524588-bja10384 · Cited by 1 · see citing works
Zhao, Y., Zhao, J., Xie, C., Yang, X., & 李建英 (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1931736
- Authors
- Meyer, S., Schäfer, L., Röhrig, J., Maheshwari, G., Most, E., Zorn, H., Ringseis, R., Eder, K., & Gessner, D. K.
- Affiliations
- Justus-Liebig-Universität Gießen (DE)
- Corresponding author
- Ringseis, Robert
- Venue
- Nutrients
- Publisher
- MDPI AG
- Published
- 2020-04-02
- Volume
- 12
- Issue
- 4
- Pages
- 987
- ISSN
- 2072-6643 (ISSN-L)
- PMC
- PMC7230462
- OpenAlex
- W3014858462
- Semantic Scholar
- a62b81a8f85d3dad35f342bf8737f69a3b6bfefd
- Cited by
- 5
- References
- 35
- Citations by year
- 2026: 1 · 2023: 1 · 2022: 1 · 2021: 1 · 2019: 1
- FWCI
- 0.53
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- Nutrients (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Publikationsdatenbank der Fraunhofer-Gesellschaft (Fraunhofer-Gesellschaft) (submittedVersion, other-oa)
- Fraunhofer-Publica (Fraunhofer-Gesellschaft) (submittedVersion)
- Universitätsbibliothek Gießen (cc-by)
- Funders
- Hessisches Ministerium für Wissenschaft und Kunst (no grant number)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect Utilization and Effects
- Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Aquaculture Nutrition and Growth
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Keywords
- insect meal, high-protein diet, hepatic lipid metabolism, methionine, cysteine, essential amino acids, amino acid supplementation, triglycerides, liver cholesterol, lipogenic enzymes, obesity, casein, Zucker fatty rats
- MeSH terms
- Amino Acids, Essential, Amino Acids, Sulfur, Animals, Caseins, Cysteine, Dietary Proteins, Insecta, Lipids, Liver, Male, Obesity, Rats, Zucker, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review