Comparison of the In Vitro Iron Bioavailability of Tempeh Made with Tenebrio molitor to Beef and Plant-Based Meat Alternatives
Abstract
:1. Introduction
2. Materials and Methods
2.1. Mealworm Sourcing
2.2. Tempeh Production
2.3. Sample Cooking and Homogenization
2.4. Gastrointestinal Digestion
2.5. Microwave Digestion
2.6. Inductively Coupled Plasma and Mass Spectrometry (ICP-MS) Analysis
2.7. Caco-2 Cell Assay
2.8. Ferritin Analysis
2.9. Statistical Analysis
3. Results
3.1. Comparison of Total Iron, Soluble Iron, and Iron Bioavailability of Insect-Based Tempeh Compared to Soybean-Based Controls
3.2. Comparison of Soluble and Bioavailable Iron from Meat with Plant- or Insect-Based Meat Alternatives
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- National Institutes of Health. What Is Iron and What Does It Do? Available online: http://ods.od.nih.gov (accessed on 12 June 2023).
- Kabir, A.; Rahman, M.; Khan, N. Maternal anemia and risk of adverse maternal health and birth outcomes in Bangladesh: A nationwide population-based survey. PLoS ONE 2022, 17, e0277654. [Google Scholar] [CrossRef]
- Piskin, E.; Cianciosi, D.; Gulec, S.; Tomas, M.; Capanoglu, E. Iron Absorption: Factors, Limitations, and Improvement Methods. ACS Omega 2022, 7, 20441–20456. [Google Scholar] [CrossRef] [PubMed]
- WHO. Anaemia. Available online: https://www.Who.Int/Health-Topics/Anaemia#tab=tab_1 (accessed on 23 July 2024).
- National Institutes of Health: Office of Dietary Supplements. Iron: Fact Sheet for Health Professionals. Available online: https://Ods.Od.Nih.Gov/Factsheets/Iron-HealthProfessional/ (accessed on 15 June 2023).
- Carpenter, C.E.; Mahoney, A.W. Contributions of heme and nonheme iron to human nutrition. Crit. Rev. Food Sci. Nutr. 1992, 31, 333–367. [Google Scholar] [CrossRef]
- Lane, D.J.R.; Bae, D.-H.; Merlot, A.M.; Sahni, S.; Richardson, D.R. Duodenal Cytochrome b (DCYTB) in Iron Metabolism: An Update on Function and Regulation. Nutrients 2015, 7, 2274–2296. [Google Scholar] [CrossRef]
- Laftah, A.H.; Latunde-Dada, G.O.; Fakih, S.; Hider, R.C.; Simpson, R.J.; McKie, A.T. Haem and folate transport by proton-coupled folate transporter/haem carrier protein 1 (SLC46A1). Br. J. Nutr. 2008, 101, 1150–1156. [Google Scholar] [CrossRef]
- Milman, N.T. A Review of Nutrients and Compounds, Which Promote or Inhibit Intestinal Iron Absorption: Making a Platform for Dietary Measures That Can Reduce Iron Uptake in Patients with Genetic Haemochromatosis. J. Nutr. Metab. 2020, 2020, 1–15. [Google Scholar] [CrossRef]
- Hurrell, R.; Egli, I. Iron bioavailability and dietary reference values. Am. J. Clin. Nutr. 2010, 91, 1461S–1467S. [Google Scholar] [CrossRef]
- Scheers, N.; Rossander-Hulthen, L.; Torsdottir, I.; Sandberg, A.-S. Increased iron bioavailability from lactic-fermented vegetables is likely an effect of promoting the formation of ferric iron (Fe3+). Eur. J. Nutr. 2015, 55, 373–382. [Google Scholar] [CrossRef]
- Chawla, P.; Bhandari, L.; Sadh, P.K.; Kaushik, R. Impact of solid-state fermentation (Aspergillus oryzae) on functional properties and mineral bioavailability of black-eyed pea (Vigna unguiculata) seed flour. Cereal Chem. 2017, 94, 437–442. [Google Scholar] [CrossRef]
- Gibson, R.S.; Yeudall, F.; Drost, N.; Mtitimuni, B.M.; Cullinan, T.R. Experiences of a Community-Based Dietary Intervention to Enhance Micronutrient Adequacy of Diets Low in Animal Source Foods and High in Phytate: A Case Study in Rural Malawian Children 1. In. J. Nutr. 2003, 133 (11 Suppl. 2), 3875S–4061S. [Google Scholar] [CrossRef] [PubMed]
- Hilaj, N.; Galetti, V.; Lima, R.M.; Krzystek, A.; Andlauer, W.; Zeder, C.; Zimmermann, M.; Moretti, D. Measuring Dietary Iron Absorption From Edible Tenebrio molitor and Assessing the Effect of Chitin on Iron Bioavailability: A Stable Iron Isotope Study in Young Women. Curr. Dev. Nutr. 2021, 5, 587. [Google Scholar] [CrossRef]
- Latunde-Dada, G.O.; Yang, W.; Aviles, M.V. In Vitro Iron Availability from Insects and Sirloin Beef. J. Agric. Food Chem. 2016, 64, 8420–8424. [Google Scholar] [CrossRef] [PubMed]
- Sridhar, K.; Bouhallab, S.; Croguennec, T.; Renard, D.; Lechevalier, V. Recent trends in design of healthier plant-based alternatives: Nutritional profile, gastrointestinal digestion, and consumer perception. Crit. Rev. Food Sci. Nutr. 2022, 63, 10483–10498. [Google Scholar] [CrossRef]
- Broccardo, C.J.; Schauer, K.L.; Kohrt, W.M.; Schwartz, R.S.; Murphy, J.P.; Prenni, J.E. Multiplexed analysis of steroid hormones in human serum using novel microflow tile technology and LC–MS/MS. J. Chromatogr. B 2013, 934, 16–21. [Google Scholar] [CrossRef] [PubMed]
- Shrivastava, G.V. Methods for the determination of limit of detection and limit of quantitation of the analytiical methods. Chron. Young Sci. 2011, 2, 21–25. [Google Scholar] [CrossRef]
- Glahn, R.P. The Caco-2 Cell Bioassay for Measurement of Food Iron Bioavailability. J. Vis. Exp. 2022, e63859. [Google Scholar] [CrossRef]
- Yiannikourides, A.; Latunde-Dada, G.O. A Short Review of Iron Metabolism and Pathophysiology of Iron Disorders. Medicines 2019, 6, 85. [Google Scholar] [CrossRef]
- Ventura, M.; Holland, M.E.; Smith, M.B.; Chaparro, J.M.; Prenni, J.; Patz, J.A.; Paskewitz, S.; Weir, T.L.; Stull, V.J. Suitability of maize crop residue fermented by Pleurotus ostreatus as feed for edible crickets: Growth performance, micronutrient content, and iron bioavailability. Front. Nutr. 2023, 10, 1157811. [Google Scholar] [CrossRef]
- Clark, A.J.; Soni, B.K.; Sharkey, B.; Acree, T.; Lavin, E.; Bailey, H.M.; Stein, H.H.; Han, A.; Elie, M.; Nadal, M. Shiitake mycelium fermentation improves digestibility, nutritional value, flavor and functionality of plant proteins. LWT 2022, 156, 113065. [Google Scholar] [CrossRef]
- Mullaney, E.; Daly, C.; Ullah, A. Advances in phytase research. Adv. Appl. Microbiol. 2000, 10, 157–199. [Google Scholar]
- Ibrahim, A.S.; Spellberg, B.; Walsh, T.J.; Kontoyiannis, D.P. Pathogenesis of Mucormycosis. Clin. Infect. Dis. 2012, 54, S16–S22. [Google Scholar] [CrossRef] [PubMed]
- Misslinger, M.; Hortschansky, P.; Brakhage, A.A.; Haas, H. Fungal iron homeostasis with a focus on Aspergillus fumigatus. Biochim. Biophys. Acta (BBA) Mol. Cell Res. 2020, 1868, 118885. [Google Scholar] [CrossRef] [PubMed]
- Wilson, J.W. Edible Mealworms: Can Fermentation Improve Consumer Acceptability and Nutritional Properties? Unpublished dissertation, Colorado State University, Fort Collins, CO, USA, 2023. [Google Scholar]
- Sandburg, A.J. The Use of Caco-2 Cells to Estimate Fe Absorption in Humans: A Critical Analysis. Int. J. Vitam. Nutr. Res. 2010, 80, 307–313. [Google Scholar] [CrossRef]
- Sutardi; Buckle, K. Phytic acid changes in soybeans fermented by traditional inoculum and six strains of Rhizopus oligosporus. J. Appl. Bacteriol. 1985, 58, 539–543. [Google Scholar] [CrossRef]
- Gemede, H.F.; Ratta, N. Antinutritional factors in plant foods: Potential health benefits and adverse effects. Glob. Adv. Res. Food Sci. Technol. 2014, 3, 103–117. [Google Scholar] [CrossRef]
- Labba, I.-C.M.; Steinhausen, H.; Almius, L.; Knudsen, K.E.B.; Sandberg, A.-S. Nutritional Composition and Estimated Iron and Zinc Bioavailability of Meat Substitutes Available on the Swedish Market. Nutrients 2022, 14, 3903. [Google Scholar] [CrossRef] [PubMed]
- First, T.; Fogliano, V.; Mishyna, M. Entoferritin: An innovative iron source for human consumption. J. Funct. Foods 2023, 108, 105711. [Google Scholar] [CrossRef]
- Mwangi, M.N.; Oonincx, D.G.A.B.; Hummel, M.; A Utami, D.; Gunawan, L.; Veenenbos, M.; Zeder, C.; I Cercamondi, C.; Zimmermann, M.B.; van Loon, J.J.; et al. Absorption of iron from edible house crickets: A randomized crossover stable-isotope study in humans. Am. J. Clin. Nutr. 2022, 116, 1146–1156. [Google Scholar] [CrossRef]
- Beyond Meat. Beyond Burger. Available online: https://www.beyondmeat.com/en-CA/products/the-beyond-burger (accessed on 6 July 2024).
- Impossible. Heme + The Science Behind Impossible. Available online: https://impossiblefoods.com/heme (accessed on 6 July 2024).
- Zhao, S.; Wang, L.; Hu, W.; Zheng, Y. Meet the meatless: Demand for new generation plant-based meat alternatives. Appl. Econ. Perspect. Policy 2022, 45, 4–21. [Google Scholar] [CrossRef]
Life Stage | Iron RDA |
---|---|
Birth to 6 months | 0.27 mg/day |
Children 6 months to 13 years | 7–11 mg/day |
Teenage boys 14–18 years | 11 mg/day |
Teenage girls 14–18 | 15 mg/day |
Adult men 19–50 | 8 mg/day |
Adult women 19–50 | 18 mg/day |
Adults 51 years and older | 8 mg/day |
Pregnant women | 27 mg/day |
Breastfeeding women | 10 mg/day |
Sample Comparison | Mean Diff. | 99% CI | Adjusted p |
---|---|---|---|
Sirloin vs. Ground Beef | 38.87 | −138 to 216 | 0.962 |
Beyond Burger vs. Ground Beef | 599.50 | 431 to 768 | <0.0001 |
Impossible Burger vs. Ground Beef | 274.70 | 106 to 443 | <0.0001 |
50/50 Mealworm/Soy Tempeh vs. Ground Beef | 264.50 | 96 to 433 | <0.0001 |
100% Soy Tempeh vs. Ground Beef | 113.30 | −55 to 282 | 0.157 |
Beyond Burger vs. Sirloin | 560.60 | 384 to 737 | <0.0001 |
Impossible Burger vs. Sirloin | 235.80 | 59 to 413 | 0.000 |
50/50 Mealworm/Soy Tempeh vs. Sirloin | 225.60 | 49 to 402 | 0.001 |
100% Soy Tempeh vs. Sirloin | 74.47 | −102 to 251 | 0.626 |
Impossible Burger vs. Beyond Burger | −324.80 | −493 to −156 | <0.0001 |
50/50 Mealworm/Soy Tempeh vs. Beyond Burger | −335.00 | −503 to −167 | <0.0001 |
100% Soybean Tempeh vs. Beyond Burger | −486.20 | −655 to −318 | <0.0001 |
50/50 Mealworm/Soy Tempeh vs. Impossible Burger | −10.17 | −179 to 158 | >0.9999 |
100% Soy Tempeh vs. Impossible Burger | −161.30 | −330 to 7 | 0.015 |
100% Soy Tempeh vs. 50/50 Mealworm/Soy Tempeh | −151.20 | −320 to 17 | 0.026 |
Sample Comparison | Mean Diff. | 99% CI | Adjusted p |
---|---|---|---|
Sirloin vs. Ground Beef | 9.25 | −13 to 32 | 0.653 |
Beyond Burger vs. Ground Beef | 4.53 | −18 to 27 | 0.974 |
Impossible Burger vs. Ground Beef | 16.12 | −8 to 40 | 0.148 |
Soy Tempeh vs. Ground Beef | 25.23 | 35 to 48 | 0.003 |
50/50 Mealworm/Soy Tempeh vs. Ground Beef | 34.03 | 11 to 57 | <0.0001 |
Beyond Burger vs. Sirloin | −4.72 | −27 to 18 | 0.969 |
Impossible Burger vs. Sirloin | 6.87 | −17 to 31 | 0.886 |
Soy Tempeh vs. Sirloin | 15.98 | −7 to 39 | 0.122 |
50/50 Mealworm/Soy Tempeh vs. Sirloin | 24.78 | 2 to 47 | 0.004 |
Impossible Burger vs. Beyond Burger | 11.59 | −12 to 35 | 0.470 |
Soy Tempeh vs. Beyond Burger | 20.70 | −2 to 43 | 0.022 |
50/50 Mealworm/Soy Tempeh vs. Beyond Burger | 29.50 | 7 to 52 | 0.001 |
Soy Tempeh vs. Impossible Burger | 9.11 | −15 to 33 | 0.709 |
50/50 Mealworm/Soy Tempeh vs. Impossible Burger | 17.91 | −6 to 42 | 0.084 |
50/50 Mealworm/Soy Tempeh vs. Soy Tempeh | 8.80 | −14 to 31 | 0.698 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wilson, J.W.; Thompson, T.W.; Wei, Y.; Chaparro, J.M.; Stull, V.J.; Nair, M.N.; Weir, T.L. Comparison of the In Vitro Iron Bioavailability of Tempeh Made with Tenebrio molitor to Beef and Plant-Based Meat Alternatives. Nutrients 2024, 16, 2756. https://doi.org/10.3390/nu16162756
Wilson JW, Thompson TW, Wei Y, Chaparro JM, Stull VJ, Nair MN, Weir TL. Comparison of the In Vitro Iron Bioavailability of Tempeh Made with Tenebrio molitor to Beef and Plant-Based Meat Alternatives. Nutrients. 2024; 16(16):2756. https://doi.org/10.3390/nu16162756
Chicago/Turabian StyleWilson, John W., Tyler W. Thompson, Yuren Wei, Jacqueline M. Chaparro, Valerie J. Stull, Mahesh N. Nair, and Tiffany L. Weir. 2024. "Comparison of the In Vitro Iron Bioavailability of Tempeh Made with Tenebrio molitor to Beef and Plant-Based Meat Alternatives" Nutrients 16, no. 16: 2756. https://doi.org/10.3390/nu16162756
APA StyleWilson, J. W., Thompson, T. W., Wei, Y., Chaparro, J. M., Stull, V. J., Nair, M. N., & Weir, T. L. (2024). Comparison of the In Vitro Iron Bioavailability of Tempeh Made with Tenebrio molitor to Beef and Plant-Based Meat Alternatives. Nutrients, 16(16), 2756. https://doi.org/10.3390/nu16162756