Cited by 7Insect Utilization and EffectsAquaculture Nutrition and GrowthAnimal Nutrition and Physiology

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 access
Meyer, Sandra, Schäfer, Lea, Röhrig, Julia, Maheshwari, Garima, Most, Erika, Zorn, Holger, Ringseis, Robert, Eder, Klaus +1 more·2020·Nutrients

Abstract

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

Crossref · 10.3390/nu12040987

Cites

35 of 35 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

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
  • 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
  • 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.

    Findingreasoning

    The 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 claim
  • May combine two claims.

    Findingown data

    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.

    “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 claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingreasoning

    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.

    “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 claim
  • May combine two claims.

    Findingreasoning

    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.

    “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 claim
  • May combine two claims.

    Findingown data

    The 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.

    Interpretationreasoning

    IM 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 given

    Five 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 claim
  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    The 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 claim
  • Classified as probably not a substantial claim.

    Premisecitation

    Cysteine 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.

    Premisecitation

    Methionine 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 conductcitation

    The 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 given

    The 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 claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    All 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
13 of 13
  • 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.”
3 of 3

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]”
  • 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].”

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

    Minor

    The 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.

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 3

  1. 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.
  2. National Research Council (1995). Nutrient Requirements of Laboratory Animals, National Academy Press. [4th ed.].
  3. 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

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)
OpenAlex
W3014858462
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
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

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