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Research Article | Open Access

Rat bioassay for evaluation of protein nutritional quality of wheat and wheat-sorghum biscuits fortified with longhorn grasshopper (Ruspolia differens) powder

Amos Kipkemoi Ronoh1,2( ), Charlotte Atsango Serrem3, Susan Balaba Tumwebaze4, Gertrude Mercy Were3
Faculty of Agriculture, Uganda Martyrs University, Kampala 5498, Uganda
Institute of Food Bioresources Technology, Dedan Kimathi University of Technology, Nyeri 10143, Kenya
Department of Consumer Sciences, School of Agriculture and Biotechnology, University of Eldoret, Eldoret 1125-30100, Kenya
Department of Forestry, Biodiversity & Tourism, School of Forestry, Environmental and Geographical Sciences, Makerere University, Kampala 7062, Uganda
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Abstract

Protein-energy malnutrition (PEM) is a persistent public health challenge in most developing countries. This study investigated the protein nutritional value of wheat and wheat-sorghum biscuits fortified with longhorn grasshopper (Ruspolia differens) to determine their suitability as a supplementary food. Fourteen diets were fed to male weanling Sprague-Dawley rats, including 11 isonitrogenous diets with 10% protein prepared from 10 biscuit variations and skimmed milk powder as a reference, 1 protein-free diet, and 2 rehabilitation diets made with wheat and wheat-sorghum biscuits fortified with 40% Ruspolia differens powder (RDP). The protein efficiency ratio, food efficiency ratio, true and apparent protein digestibility, and net protein retention ratio results for the fortified biscuit diets were all negative, with the exception of wheat biscuits supplemented with RDP 40%. The isonitrogenous diets maintained the rats with no substantial weight gain or loss. Rats on rehabilitation diets gained weight rapidly, by 61% and 69% for wheat-sorghum and wheat diets, respectively. Weight increase during rehabilitation was considerably higher (P < 0.05) by 50% and 54.6% in wheat-sorghum and wheat diet groups compared to normal growth phases. The rehabilitated rats had a greater percentage of body weight than the experimental groups. The protein digestibility-corrected amino acid score (PDCAAS) of fortified biscuits ranged from 26% to 33% for wheat biscuits and 22% to 32% for wheat-sorghum biscuits. The digestible indispensable amino acid score (DIAAS) of the fortified biscuits varied from 47% to 60% for wheat biscuits and 44% to 60% for wheat-sorghum biscuits. As a result, the fortified biscuits fell short of the minimum requirements of 70% for PDCAAS and 75% for DIAAS in fortified protein diets. Furthermore, it appears that substituting 10% RDP to wheat-sorghum and wheat biscuits does not promote rat growth. Fortification with 40% RDP, on the other hand, dramatically improves rat’s growth and rehabilitation. Because of their high protein nutritional content, the biscuits fortified with 40% RDP could be used as a supplementary to help rehabilitate malnourished children.

Keywords

sorghumwheatbiscuitrat bioassayfortificationprotein efficiency ratioprotein-energy malnutrition

References

[1]

F. T. Manjong, V. S. Verla, T. O. Egbe, et al., Risk factors of under nutrition among indigenous children under five years in developing countries: a scoping review, J. Public Health Epidemiol. 12 (2020) 340–348. https://doi.org/10.5897/JPHE2020.1279.
Crossref Google Scholar
[2]
UNICEF/WHO, World Bank Group, UNICEF-WHO-The World Bank. Joint child malnutrition estimates-levels and trends-2021 edition, United Nation Children’s Fund, Washington, DC, 2021. https://data.unicef.org/resources/jme-report-2021/.
[3]

O. R. Katoch, Determinants of malnutrition among children: a systematic review, Nutrition 96 (2022) 111565. https://doi.org/10.1016/j.nut.2021.111565.
Crossref Google Scholar
[4]
FAO/WHO, Codex Alimentarius: foods for special dietary uses (including foods for infants and children). Joint FAO/WHO Food Standards Programme, Codex Alimentarius Commission, 1994. Available from: https://www.fao.org/3/ca2329en/ca2329en.pdf.
[5]
S. N. Serrano-Sandoval, D. Guardado-Felix, J. A. Gutiérrez-Uribe, Legumes in human health and nutrition, in: C. Rauh (Ed.), Reference module in food science, Elsevier, 2022, pp. 430–437. https://doi.org/10.1016/B978-0-12-821848-8.00061-5.
Crossref
[6]
J. R. N. Taylor, K. G. Duodu, Sorghum and millets: grain-quality characteristics and management of quality requirements, in: C. Wrigley, I. Batey, D. Miskelly (Eds.), Cereal grains, Elsevier, 2017, pp. 317–351. https://doi.org/10.1016/B978-0-08-100719-8.00013-9.
Crossref
[7]

M. Goubgou, L. T. Songré-Ouattara, F. Bationo, et al., Biscuits: a systematic review and meta-analysis of improving the nutritional quality and health benefits, Food Prod. Process. Nutr. 3 (2021) 26. https://doi.org/10.1186/s43014-021-00071-z.
Crossref Google Scholar
[8]

C. A. Serrem, H. L. de Kock, J. R. N. Taylor, Nutritional quality, sensory quality and consumer acceptability of sorghum and bread wheat biscuits fortified with defatted soy flour, Int. J. Food Sci. Technol. 46 (2011) 74–83. https://doi.org/10.1111/j.1365-2621.2010.02451.x.
Crossref Google Scholar
[9]

A. K. Ronoh, C. A. Serrem, S. B. Tumwebaze, et al., Effect of fortifying sorghum and wheat with longhorn grasshopper ( Ruspolia differens) powder on nutritional composition and consumer acceptability of biscuits, Food Sci. Nutr. 12 (2024) 3492–3507. https://doi.org/10.1002/fsn3.4018.
Crossref Google Scholar
[10]

M. W. Mmari, J. N. Kinyuru, H. S. Laswai, et al., Traditions, beliefs and indigenous technologies in connection with the edible longhorn grasshopper Ruspolia differens (Serville 1838) in Tanzania, J. Ethnobiol. Ethnomed. 13 (2017) 60. https://doi.org/10.1186/s13002-017-0191-6.
Crossref Google Scholar
[11]

G. Ssepuuya, R. Smets, D. Nakimbugwe, et al., Nutrient composition of the long-horned grasshopper Ruspolia differens Serville: effect of swarming season and sourcing geographical area, Food Chem. 301 (2019) 125305. https://doi.org/10.1016/j.foodchem.2019.125305.
Crossref Google Scholar
[12]

N. Siulapwa, A. Mwambungu, E. Lungu, et al., Nutritional value of four common edible insects in Zambia, Int. J. Sci. Res. 3 (2014) 876–884.
Google Scholar
[13]

E. P. Shabo, E. Owaga, J. Kinyuru, Physico-chemical characterization, acceptability and shelf stability of extruded composite flour enriched with long-horned grasshopper ( Ruspolia differens), J. Agric. Sci. Technol. 21 (2022) 4–32. https://doi.org/10.4314/jagst.v21i2.2.
Crossref Google Scholar
[14]

C. Chuwa, T. Ngendello, P. Saidia, et al., Edible grasshoppers ( Ruspolia differens) as alternative source of protein from insects to combat malnutrition, Afr. J. Food Agric. Nutr. Dev. 23 (2023) 23576–23589. https://doi.org/10.18697/ajfand.121.23680.
Crossref Google Scholar
[15]

B. O. Ochieng, J. O. Anyango, F. M. Khamis, et al., Nutritional characteristics, microbial loads and consumer acceptability of cookies enriched with insect ( Ruspolia differens) meal, LWT-Food Sci. Technol. 184 (2023) 115012. https://doi.org/10.1016/j.lwt.2023.115012.
Crossref Google Scholar
[16]

N. Shaheen, S. Islam, S. Munmun, et al., Amino acid profiles and digestible indispensable amino acid scores of proteins from the prioritized key foods in Bangladesh, Food Chem. 213 (2016) 83–89. https://doi.org/10.1016/j.foodchem.2016.06.057.
Crossref Google Scholar
[17]
FAO, Dietary protein quality evaluation in human nutrition: report of an FAO Expert Consultation, Food and Agriculture Organization of the United Nations, Rome, Italy, 2011. Available from: https://www.fao.org/3/i3124e/i3124e.pdf.
[18]
Z. A. Bhutta, K. Sadiq, Protein digestion and bioavailability, in: B. Caballero (Ed.), Encyclopaedia of human nutrition, 3rd ed, Academic Press, 2013, pp. 116–122. https://doi.org/10.1016/B978-0-12-375083-9.00240-3.
Crossref
[19]
D. Tomé, Protein quality and sources, in: B. Caballero (Ed.), Reference module in food science, Elsevier, 2021, pp. 559-567. https://doi.org/10.1016/B978-0-12-821848-8.00028-7.
Crossref
[20]
M. Rodríguez-Rodríguez, F. G. Barroso, D. Fabrikov, et al., In vitro crude protein digestibility of insects: a review, Insects 13 (2022) 682. https://doi.org/10.3390/insects13080682.
Crossref
[21]
P. Nolan, A. E. Mahmoud, R. R. Kavle, et al., Edible insects: protein composition, digestibility, and biofunctionalities, in: Z. F. Bhat, J. D. Morton, A. E.-D. A. Bekhit, et al. (Eds.), Processing technologies and food protein digestion, Academic Press, 2023, pp. 429–494. https://doi.org/10.1016/B978-0-323-95052-7.00020-0.
Crossref
[22]

F. I. Oibiokpa, H. O. Akanya, A. A. Jigam, et al., Protein quality of four indigenous edible insect species in Nigeria, Food Sci. Hum. Wellness 7 (2018) 175–183. https://doi.org/10.1016/j.fshw.2018. 05.003.
Crossref Google Scholar
[23]

M. Bauserman, A. Lokangaka, J. Gado, et al., A cluster-randomized trial determining the efficacy of caterpillar cereal as a locally available and sustainable complementary food to prevent stunting and anaemia, Public Health Nutr. 18 (2015) 1785–1792. https://doi.org/10.1017/S1368980014003334.
Crossref Google Scholar
[24]

C. Dexter, G. T. Matanhire, T. Jombo, et al., Protein quality of commonly consumed edible insects in Zimbabwe, Afr. J. Food Agric. Nutr. Dev. 19(3) (2019) 14674–14689. https://doi.org/10.18697/ajfand.86.17645.
Crossref Google Scholar
[25]

C. Poelaert, F. Francis, T. Alabi, et al., Protein value of two insects, subjected to various heat treatments, using growing rats and the protein digestibility-corrected amino acid score, J. Insects Food Feed 4 (2018) 77–87. https://doi.org/10.3920/JIFF2017.0003.
Crossref Google Scholar
[26]

Y. Singh, M. Cullere, A. Kovitvadhi, et al., Effect of different killing methods on physicochemical traits, nutritional characteristics, in vitro human digestibility and oxidative stability during storage of the house cricket ( Acheta domesticus L.), Innov. Food Sci. Emerg. Technol. 65 (2020) 102444. https://doi.org/10.1016/j.ifset.2020.102444.
Crossref Google Scholar
[27]

M. Ochiai, M. Inada, Powdered edible locust enhances nitrogen excretion and presents a low-energy value in growing rats, J. Asia-Pac. Entomol. 23 (2020) 1138–1143. https://doi.org/10.1016/j.aspen.2020.08.019.
Crossref Google Scholar
[28]

M. Ochiai, K. Tezuka, H. Yoshida, et al., Edible insect Locusta migratoria shows intestinal protein digestibility and improves plasma and hepatic lipid metabolism in male rats, Food Chem. 396 (2022) 133701. https://doi.org/10.1016/j.foodchem.2022.133701.
Crossref Google Scholar
[29]
Institute of Medicine, Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids (macronutrients), The National Academies Press, Washington, DC, 2005.
[30]
AOAC, Official methods of analysis. Method 960-48, 17th ed, The Association, Washington, DC, 2000.
[31]

D. G. Chapman, R. Castillo, J. A. Campbell, Evaluation of protein in foods: I. a method for the determination of protein efficiency ratios, Can. J. Biochem. Physiol. 37 (1959) 679–686. https://doi.org/10.1139/o59-074.
Crossref Google Scholar
[32]

K. G. Dewey, Formulations for fortified complementary foods and supplements: review of successful products for improving the nutritional status of infants and young children, Food Nutr. Bull. 30 (2009) S239–S255. https://doi.org/10.1177/15648265090302S209.
Crossref Google Scholar
[33]
National Research Council of the National Academies, Guide for the care and use of laboratory animals, 8th ed, The National Academies Press, Washington, DC, 2011. https://grants.nih.gov/grants/olaw/guide-for-the-care-and-use-of-laboratory-animals.pdf.
[34]
FAO/WHO, Protein quality evaluation: report of the joint FAO/WHO expert consultation, FAO, Rome, Italy, 1991. http://www.fao.org/docrep/013/t0501e/t0501e00.pdf.
[35]
L. W. George, Official methods of analysis of AOAC INTERNATIONAL, 22nd ed, New York, AOAC Publications, 2023. https://doi.org/10.1093/9780197610145.001.0001.
Crossref
[36]
WHO/FAO/UNU Expert Consultation, Protein and amino acids requirements in human nutrition: a report of a joint FAO/WHO/UNU expert consoultation, WHO Technical Report Series Report No. 935, WHO Media Centre, Geneva, Switzerland, 2007.
[37]
FAO, Dietary protein quality evaluation in human nutrition: report of an FAO expert consultation, Food and Agriculture Organization of the United Nations, Rome, 2013. Available from: https://www.fao.org/documents/card/en/c/ab5c9fca-dd15-58e0-93a8-d71e028c8282/.
[38]

A. M. M. Sanchez, A. M. C. Nuñez, L. T. Meza-Cureño, et al., Biochemical and morphometric parameters support nutritional benefits in laboratory rats fed with an orthopteran-based ( Sphenarium purpurascens) Diet, Food Nutr. J. 7 (2022) 1–14. https://doi.org/10.29011/2575-7091.100236.
Crossref Google Scholar
[39]

D. K. Gessner, A. Schwarz, S. Meyer, et al., Insect meal as alternative protein source exerts pronounced lipid-lowering effects in hyperlipidemic obese Zucker rats, J. Nutr. 149 (2019) 566–577. https://doi.org/10.1093/jn/nxy256.
Crossref Google Scholar
[40]

C. A. Serrem, H. L. de Kock, A. Oelofse, et al., Rat bioassay of the protein nutritional quality of soy-fortified sorghum biscuits for supplementary feeding of school-age children, J. Sci. Food Agr. 91 (2011) 1814–1821. https://doi.org/10.1002/jsfa.4389.
Crossref Google Scholar
[41]

F. B. Agengo, A. N. Onyango, C. A. Serrem, et al., Efficacy of compositing with snail meat powder on protein nutritional quality of sorghum-wheat buns using a rat bioassay, J. Sci. Food Agr. 100 (2020) 2963–2970. https://doi.org/10.1002/jsfa.10324.
Crossref Google Scholar
[42]

I. Agbemafle, N. Hanson, A. E. Bries, et al., Alternative protein and iron sources from edible insects but not Solanum torvum improved body composition and iron status in Malnourished rats, Nutrients 11 (2019) E2481. https://doi.org/10.3390/nu11102481.
Crossref Google Scholar
[43]

F. Azimi, A. Esmaillzadeh, E. Alipoor, et al., Effect of a newly developed ready-to-use supplementary food on growth indicators in children with mild to moderate malnutrition, Public Health 185 (2020) 290–297. https://doi.org/10.1016/j.puhe.2020.06.025.
Crossref Google Scholar
[44]

W. M. López-Alonso, J. Gallegos-Martínez, J. Reyes-Hernández, Impact of a nutritional intervention based on amaranth flour consumption to recovery undernourished children, Curr. Res. Nutr. Food Sci. J. 9 (2021) 222–232. https://doi.org/10.12944/CRNFSJ. 9.1.22.
Crossref Google Scholar
[45]

T. C. E. Mosha, M. R. Bennink, P. K. W. Ng, Nutritional quality of drum-processed and extruded composite supplementary foods, J. Food Sci. 70 (2005) C138–C144. https://doi.org/10.1111/j.1365-2621.2005.tb07074.x.
Crossref Google Scholar
[46]

J. D. Axtell, A. W. Kirleis, M. M. Hassen, et al., Digestibility of sorghum proteins, Proc. Natl. Acad. Sci. 78 (1981) 1333–1335. https://doi.org/10.1073/pnas.78.3.1333.
Crossref Google Scholar
[47]

B. O. Eggum, I. Kreft, B. Javornik, Chemical composition and protein quality of buckwheat ( Fagopyrum esculentum Moench), Plant Foods Hum. Nutr. 30 (1980) 175–179. https://doi.org/10.1007/BF01094020.
Crossref Google Scholar
[48]

K. G. Duodu, A. Nunes, I. Delgadillo, et al., Effect of grain structure and cooking on sorghum and maize in vitro protein digestibility, J. Cereal Sci. 35 (2002) 161–174. https://doi.org/10.1006/jcrs.2001.0411.
Crossref Google Scholar
[49]

K. G. Duodu, J. R. N. Taylor, P. S. Belton, et al., Factors affecting sorghum protein digestibility, J. Cereal Sci. 38 (2003) 117–131. https://doi.org/10.1016/S0733-5210(03)00016-X.
Crossref Google Scholar
[50]

J. R. N. Taylor, H. L. de Kock, E. Makule, et al., Opportunities and challenges for wholegrain staple foods in sub-Saharan Africa, J. Cereal Sci. 104 (2022) 103438. https://doi.org/10.1016/j.jcs.2022.103438.
Crossref Google Scholar
[51]
J. P. Williams, J. R. Williams, A. Kirabo, et al. , Nutrient content and health benefits of insects, in: A. T. Dossey, J. A. Morales-Ramos, M. Guadalupe Rojas (Eds.), Insects as sustainable food ingredients, Elsevier, 2016, pp. 61–84. https://doi.org/10.1016/B978-0-12-802856-8.00003-X.
Crossref
[52]

K. E. Ekpo, Effect of processing on the protein quality of four popular insects consumed in Southern Nigeria, Arch. Appl. Sci. Res. 3 (2011) 307–326.
Google Scholar
[53]

R. A. Samra, G. H. Anderson, Insoluble cereal fiber reduces appetite and short-term food intake and glycemic response to food consumed 75 min later by healthy men, Am. J. Clin. Nutr. 86 (2007) 972–979. https://doi.org/10.1093/ajcn/86.4.972.
Crossref Google Scholar
[54]

S. Fuller, E. Beck, H. Salman, et al., New horizons for the study of dietary fiber and health: a review, Plant Foods Hum. Nutr. Dordr. Neth. 71 (2016) 1–12. https://doi.org/10.1007/s11130-016-0529-6.
Crossref Google Scholar
[55]

H. S. Koopmans, An integrated organismic response to lower gut stimulation, Scand. J. Gastroenterol. Suppl. 82 (1983) 143–153.
Google Scholar
[56]

L. M. Zem, C. V. Helm, G. S. Henriques, et al., Pereskia aculeata: biological analysis on wistar rats, Food Sci. Technol. 37 (2017) 42–47. https://doi.org/10.1590/1678-457x.29816.
Crossref Google Scholar
[57]

M. Skotnicka, A. Mazurek, K. Karwowska, et al., Satiety of edible insect-based food products as a component of body weight control, Nutrients 14 (2022) 2147. https://doi.org/10.3390/nu14102147.
Crossref Google Scholar
[58]

C. Delgado-Andrade, J. A. Rufián-Henares, F. J. Morales, Lysine availability is diminished in commercial fibre-enriched breakfast cereals, Food Chem. 100 (2007) 725–731. https://doi.org/10.1016/j.foodchem.2005.10.031.
Crossref Google Scholar
[59]

B. Sarriá, R. López-Fandiño, M. P. Vaquero, Does processing of a powder or in-bottle-sterilized liquid infant formula affect calcium bioavailability?, Nutrition 17 (2001) 326–331. https://doi.org/10.1016/s0899-9007(00)00585-2.
Crossref Google Scholar
[60]

B. D. White, F. Du, D. A. Higginbotham, Low dietary protein is associated with an increase in food intake and a decrease in the in vitro release of radiolabeled glutamate and GABA from the lateral hypothalamus, Nutr. Neurosci. 6 (2003) 361–367. https://doi.org/10.1080/10284150310001640365.
Crossref Google Scholar
[61]

S. Aparecida de França, M. P. dos Santos, M. A. R. Garófalo, et al., Low protein diet changes the energetic balance and sympathetic activity in brown adipose tissue of growing rats, Nutrition 25 (2009) 1186–1192. https://doi.org/10.1016/j.nut.2009.03.011.
Crossref Google Scholar
[62]
J. Taylor, G. Duodu, Resistant-type starch in sorghum foods-factors involved and health implications, Starch-Starke 75(9/10) (2022). https://doi.org/10.1002/star.202100296.
Crossref
[63]

T. H. Vu, S. Bean, C. F. Hsieh, et al., Changes in protein and starch digestibility in sorghum flour during heat-moisture treatments, J. Sci. Food Agr. 97 (2017) 4770–4779. https://doi.org/10.1002/jsfa.8346.
Crossref Google Scholar
[64]
M. D. Finke, D. Oonincx, Insects as food for insectivores, in: J. A. Morales-Ramos, M. Guadalupe Rojas, D. I. Shapiro-Ilan (Eds), Mass production of beneficial organisms, 2nd ed, Academic Press, 2014, pp. 583–616. https://doi.org/10.1016/B978-0-12-391453-8.00017-0.
Crossref
[65]
National Research Council, Nutrient requirements of laboratory animals, National Academy of Sciences Press, Washington, DC, 2011.
[66]
F. T. Fombong, M. Van Der Borght, J. Vanden broeck, influence of freeze-drying and oven-drying post blanching on the nutrient composition of the edible insect Ruspolia differens, Insects 8 (2017) 102. https://doi.org/10.3390/insects8030102.
Crossref
[67]

M. D. Finke, G. R. DeFoliart, N. J. Benevenga, Use of a four-parameter logistic model to evaluate the quality of the protein from three insect species when fed to rats, J. Nutr. 119 (1989) 864–871. https://doi.org/10.1093/jn/119.6.864.
Crossref Google Scholar
[68]

T. C. Mosha, M. R. Bennink, Protein quality of drum-processed cereal-bean-sardine composite supplementary foods for preschool-age children, J. Sci. Food Agr. 84 (2004) 1111–1118. https://doi.org/10.1002/jsfa.1756.
Crossref Google Scholar
[69]
AVMA, AVMA Guidelines on euthanasia of animals: 2020 edition, American Veterinary Medical Association, Schaumburg, Illinois, 2020. https://www.avma.org/sites/default/files/2020-02/Guidelines-on-Euthanasia-2020.pdf.
Food Science of Animal Products
Volume 2 Issue 2,
June 2024
Article number: 9240062
DOI: 10.26599/FSAP.2024.9240062
Cite this article:
Ronoh AK, Serrem CA, Tumwebaze SB, et al. Rat bioassay for evaluation of protein nutritional quality of wheat and wheat-sorghum biscuits fortified with longhorn grasshopper (Ruspolia differens) powder. Food Science of Animal Products, 2024, 2(2): 9240062. https://doi.org/10.26599/FSAP.2024.9240062

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Received: 23 May 2024
Revised: 14 June 2024
Accepted: 08 July 2024
Published: 12 August 2024
© Beijing Academy of Food Sciences 2024.

Food Science of Animal Products published by Tsinghua University Press. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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