The development of low-glycemic, antioxidant-rich moringa–beetroot enteral nutrition for diabetic and stroke patients

Authors

  • Kartika Nugraheni Master’s Program in Nutrition Science, Graduate Program, Universitas Muhammadiyah Semarang, Semarang, 50273, Indonesia https://orcid.org/0000-0002-1853-1171
  • Zahra Maharani Latrobdiba Department of Nutrition, Faculty of Nursing and Health Science, Universitas Muhammadiyah Semarang, Semarang, 50273, Indonesia
  • Listya Anggraeni Department of Nutrition, Faculty of Nursing and Health Science, Universitas Muhammadiyah Semarang, Semarang, 50273, Indonesia
  • Ayu Okvytasari Department of Nutrition, Faculty of Nursing and Health Science, Universitas Muhammadiyah Semarang, Semarang, 50273, Indonesia

DOI:

https://doi.org/10.21927/ijnd.2026.14(3).199-209

Keywords:

Enteral Nutrition, Stroke, Diabetes Mellitus, Beetroot, Moringa, bit, kelor

Abstract

ABSTRAK

Latar Belakang: Pasien dengan stroke dan diabetes melitus (DM) berisiko mengalami disfagia dan rentan terhadap malnutrisi. Oleh karena itu, formula enteral dipilih sebagai bentuk terapi nutrisi dan diformulasikan secara khusus agar memiliki indeks glikemik rendah serta kaya akan antioksidan.

Tujuan: Penelitian ini bertujuan untuk mengetahui komposisi proksimat, kapasitas antioksidan, viskositas, total nilai kalori, dan indeks glikemik dari formula enteral yang disubstitusi dengan bit dan kelor.

Metode: Penelitian ini menggunakan rancangan acak lengkap yang terdiri dari tiga kelompok perlakuan dan satu kelompok kontrol. Kelompok kontrol menerima Formula Rumah Sakit (FRS), sedangkan kelompok perlakuan terdiri dari Formula Modifikasi dengan tambahan bit (FRS-B) dan bubuk kelor (FRS-M). Uji total kalori dilakukan dengan kalorimetri bom, analisis makronutrien dengan uji proksimat, viskositas dengan viskometer rotari, daya alir menggunakan selang NGT 16 Fr, analisis kapasitas antioksidan dengan uji DPPH, dan indeks glikemik dengan respons glukosa darah. Data dianalisis menggunakan uji t independen, uji t berpasangan, uji Mann-Whitney, dan uji Wilcoxon.

Hasil: FRS-B memenuhi prinsip diet stroke-DM dengan kandungan karbohidrat rendah, lemak rendah, dan protein tinggi, meskipun masih perlu peningkatan kadar protein. Viskositasnya memenuhi standar National Dysphagia Diet. Aktivitas antioksidan FRS secara signifikan lebih tinggi dibandingkan dengan formula enteral FRS-B. Indeks glikemik formula FRS-B tergolong tinggi, namun beban glikemiknya rendah. Kandungan energi FRS lebih besar (0.9 kkal/ml) dibandingkan FRS-B (0.7 kkal/ml).

Kesimpulan: Secara keseluruhan, formula enteral FRS-B menunjukkan potensi sebagai terapi nutrisi bagi pasien stroke-DM karena memenuhi kebutuhan diet pada pasien dengan disfagia dan menawarkan manfaat antioksidan. Namun, diperlukan perbaikan pada kandungan protein dan indeks glikemik untuk mengoptimalkan aplikasinya secara klinis.

 

ABSTRACT

Background: Patients with stroke and diabetes mellitus (DM) are at risk of developing dysphagia and are therefore susceptible to malnutrition. Consequently, enteral formulas are selected as a form of nutritional therapy and are specifically formulated to have a low glycemic index and be rich in antioxidants.

Purpose: This study aimed to determine the proximate composition, antioxidant capacity, viscosity, total caloric value, and the glycemic index of the tested enteral nutrition.

Methods: This study employed a completely randomized design, featuring three treatment groups and one control group. The control group received the Hospital Formula (FRS-C), while the treatment groups included a Modified Formula with added beetroot (FRS-B) and moringa powder (FRS-M). Total calorie test using bomb calorimetry, macronutrient analysis with proximate test, viscosity with rotary viscometer, flow power on 16 Fr NGT tube, antioxidant capacity analysis with DPPH test, and glycemic index with blood glucose response. Data were analyzed using an independent T-test, a paired sample T-test, Mann-Whitney, and Wilcoxon.

Results: FRS-B meets the principles of stroke-DM diet with low carbohydrate, low fat, and high protein, although it needs to increase protein. Its viscosity meets the National Dysphagia Diet standards. The antioxidant activity of FRS is significantly higher than FRS-B enteral formula. The FRS-B glycemic index formula is high, but the glycemic load is low. The energy content of FRS is greater (0.9 kcal/ml) than the FRS-B (0.7 kcal/ml).

Conclusions: To summarize, the FRS-B enteral formula demonstrates potential as a nutritional therapy for stroke-DM patients, as it meets dietary requirements for dysphagia and offers antioxidant benefits, although improvements in protein content and glycemic index are necessary to optimize its clinical applicability.

Downloads

Download data is not yet available.

References

1. International Diabetes Federation. Diabetes Atlas. 10th edn. Brussels; 2021.

2. Mosenzon O, Cheng AYY, Rabinstein AA, Sacco S. Diabetes and stroke: what are the connections? J Stroke. 2023;25(1):26–38. https://doi:10.5853/jos.2022.02306

3. Noh J. The connection between diabetes mellitus and stroke: a brief review. Cardiovascular Prevention and Pharmacotherapy. 2025;7(2):55–60. https://doi.org/10.36011/cpp.2025.7.e7

4. Khunti K, Zaccardi F, Amod A, Aroda VR, Aschner P, Colagiuri S, et al. Glycaemic control is still central in the hierarchy of priorities in type 2 diabetes management. Diabetologia. 2025;68(1):17–28. https://doi:10.1007/s00125-024-06254-w

5. Ni C, Jia Q, Ding G, Wu X, Yang M. Low-glycemic index diets as an intervention in metabolic diseases: a systematic review and meta-analysis. Nutrients. 2022;14(2):307. https://doi.org/10.3390/nu14020307

6. Zhou Y, Zhang S, Fan X. Role of polyphenols as antioxidant supplementation in ischemic stroke. Oxid Med Cell Longev. 2021;2021(1):5471347. https://doi.org/10.1155/2021/5471347

7. dos S. Baião D, da Silva DVT, Paschoalin VMF. Beetroot, a remarkable vegetable: Its nitrate and phytochemical contents can be adjusted in novel formulations to benefit health and support cardiovascular disease therapies. Antioxidants. 2020;9(10):960. https://doi.org/10.3390/antiox9100960

8. Wang Y, Chen W, Zhou J, Wang Y, Wang H, Wang Y. Nitrate metabolism and ischemic cerebrovascular disease: A narrative review. Front Neurol. 2022;13:735181. https://doi.org/10.3389/fneur.2022.735181

9. Chiș A, Noubissi PA, Pop OL, Mureșan CI, Fokam Tagne MA, Kamgang R, et al. Bioactive compounds in Moringa oleifera: mechanisms of action, focus on their anti-inflammatory properties. Plants. 2023;13(1):20. https://doi.org/10.3390/plants13010020

10. Cuschieri A, Camilleri E, Blundell R. Cerebroprotective effects of Moringa oleifera derivatives extracts against MCAO ischemic stroke: A systematic review and meta-analysis. Heliyon. 2023;9(6). https://doi.org/10.1016/j.heliyon.2023.e16622

11. Bering J, DiBaise JK. Home parenteral and enteral nutrition. Nutrients. 2022;14(13):2558. https://doi.org/10.3390/nu14132558

12. Doley J. Enteral nutrition overview. Nutrients. 2022;14(11):2180. https://doi.org/10.3390/nu14112180

13. Mayasari M, Mahmudah FF, Perwitasari S, Rahayu U. Evaluation of the provision of enteral nutrition in critically ill patients receiving mechanical ventilation. Jurnal Gizi dan Dietetik Indonesia (Indonesian Journal of Nutrition and Dietetics). 2023;11(1):30–9. https://doi.org/10.21927/ijnd.2023.11(1).30-39

14. Nugraheni K, Anggraeni L, Okvytasari A, Latrobdiba ZM. Acceptability and Sensory Properties of Specific Enteral Formula for Stroke-Diabetes Mellitus Patients. In: 2nd Lawang Sewu International Symposium on Health Sciences: Nutrition (LSISHSN 2023). Atlantis Press; 2024. p. 116–24. https://doi.org/10.2991/978-94-6463-550-8_13

15. Yu Y, Li X, Zhang J, Li X, Wang J, Sun B. Oat milk analogue versus traditional milk: Comprehensive evaluation of scientific evidence for processing techniques and health effects. Food Chem X. 2023;19:100859. https://doi.org/10.1016/j.fochx.2023.100859

16. Rathore Y, Meena S, Joshi P. Formulation and quality evaluation of Moringa leaves powder and development of value-added products. The Pharma Innovation Journal. 2022;11(10):1605–15.

17. Mitrevski J, Pantelić NĐ, Dodevska MS, Kojić JS, Vulić JJ, Zlatanović S, et al. Effect of beetroot powder incorporation on functional properties and shelf life of biscuits. Foods. 2023;12(2):322. https://doi.org/10.3390/foods12020322

18. Margareta M. Pengaruh Lama Perendaman Biji Kedelai (Glycine max L. Merr) terhadap Karakateristik Organoleptik Susu Kedelai. AgriHumanis: Journal of Agriculture and Human Resource Development Studies. 2021;2(1):9–14. https://doi.org/10.46575/agrihumanis.v2i1

19. Hopper Z, Desbrow B, Roberts S, Irwin C. Preparation procedures of food and beverage samples for oxygen bomb calorimetry: A scoping review and reporting checklist. J Food Drug Anal. 2023;31(2):232. https://doi.org/10.38212/2224-6614.3461

20. Latimer G. Official Methods of Analysis: 22nd Edition (2023). In: Latimer G, editor. Official Methods of Analysis of AOAC INTERNATIONAL [Internet]. 22nd ed. AOAC Publications; 2023 [cited 2025 Oct 21]. p. 127A. https://doi.org/10.1093/9780197610145.002.001

21. International Dysphagia Diet Standardisation Initiative (IDDSI). IDDSI Framework and Testing Methods [Internet]. 2019 [cited 2025 Apr 19]. Available from: https://www.iddsi.org/images/Publications-Resources/DetailedDefnTestMethods/English/V2TestingMethodsEnglish31july2019.pdf

22. Gulcin İ, Alwasel SH. DPPH radical scavenging assay. Processes. 2023;11(8):2248. https://doi.org/10.1093/9780197610145.002.001

23. Boonyavarakul A. STUDY OF GLYCEMIC INDEX OF DIABETES-SPECIFIC MODIFIED FORMULA AMONG HEALTHY ADULTS. Journal of Southeast Asian Medical Research. 2024;8:e0188–e0188. https://doi.org/10.55374/jseamed.v8.188

24. Annan, S.F., Higgins, L.A., Jelleryd, E., Hannon, T., Rose, S., Salis, S., Baptista, J., Chinchilla, P. and Marcovecchio, M.L., 2022. ISPAD Clinical Practice Consensus Guidelines 2022: Nutritional management in children and adolescents with diabetes. Pediatr Diabetes, 23(8), pp.1297-1321. https://doi:10.1111/pedi.13429

25. Korai A, Thomson I, Carey S, Allman-Farinelli M. A systematic review and quality appraisal of guidelines and recommendations for home enteral tube feeding in adults. Eur J Clin Nutr. 2025;79(2):104–12. https://doi:10.1038/s41430-024-01500-1

26. Singh B, Pavithran N, Rajput R. Effects of food processing on nutrients. Current Journal of Applied Science and Technology. 2023;42(46):34–49. https://doi.org/10.9734/cjast/2023/v42i464292

27. Moyo HN. The Impact of Food Processing Techniques on Nutrient Retention and Bioavailability. 2024.

28. Alemayehu GF, Forsido SF, Tola YB, Amare E. Nutritional and Phytochemical Composition and Associated Health Benefits of Oat (Avena sativa) Grains and Oat‐Based Fermented Food Products. The Scientific World Journal. 2023;2023(1):2730175. https://doi.org/10.1155/2023/2730175

29. Zhang Y, Sun M, Huo R, Gu Q, Miao Y, Zhang M. The effect of stir‐frying on the aging of oat flour during storage: A study based on lipidomics. Food Sci Nutr. 2024;12(5):3188–98. https://doi.org/10.1155/2023/2730175

30. Luparelli A, Trisciuzzi D, Schirinzi WM, Caputo L, Smiriglia L, Quintieri L, et al. Whey Proteins and Bioactive Peptides: Advances in Production, Selection and Bioactivity Profiling. Biomedicines. 2025;13(6):1311. https://doi.org/10.3390/biomedicines13061311

31. Lueders B, Kanney BC, Krone MJ, Gannon NP, Vaughan RA. Effect of branched-chain amino acids on food intake and indicators of hunger and satiety-a narrative summary. Human Nutrition & Metabolism. 2022;30:200168. https://doi.org/10.1016/j.hnm.2022.200168

32. Qin C, Yang S, Chu YH, Zhang H, Pang XW, Chen L, et al. Signaling pathways involved in ischemic stroke: molecular mechanisms and therapeutic interventions. Signal Transduct Target Ther. 2022;7(1):215. https://doi.org/10.1038/s41392-022-01064-1

33. Burgos R, Bretón I, Cereda E, Desport JC, Dziewas R, Genton L, et al. ESPEN guideline clinical nutrition in neurology. Clinical Nutrition. 2018;37(1):354–96. https://doi.org/10.1016/j.clnu.2017.09.003

34. Wang X, Liu T, Song H, Cui S, Liu G, Christoforou A, et al. Targeted metabolomic profiling reveals association between altered amino acids and poor functional recovery after stroke. Front Neurol. 2020;10:1425. https://doi.org/10.3389/fneur.2019.01425

35. Muscaritoli M, Pradelli L. Medium-chain triglyceride (MCT) content of adult enteral tube feeding formulas and clinical outcomes. A systematic review. Front Nutr. 2021;8:697529. https://doi.org/10.3389/fnut.2021.697529

36. Watanabe S, Tsujino S. Applications of medium-chain triglycerides in foods. Front Nutr. 2022;9:802805. https://doi.org/10.3389/fnut.2022.802805

37. Nguyen DL, Schott LL, Lowen CC, Desai AM, Baumer DL, Miranowski MK, et al. Characteristics and feeding intolerance in critically ill adult patients receiving peptide-based enteral nutrition: A retrospective cross-sectional study. Clin Nutr ESPEN. 2024;59:270–8. https://doi.org/10.1016/j.clnesp.2023.12.007

38. López-Gómez JJ, Delgado García E, Primo-Martín D, Simón de la Fuente M, Gómez-Hoyos E, Jiménez-Sahagún R, et al. Effect of a diabetes-specific formula in non-diabetic inpatients with stroke: a randomized controlled trial. Nutr Diabetes. 2024;14(1):34. https://doi.org/10.1038/s41387-024-00292-4

39. Boullata JI, Carrera AL, Harvey L, Escuro AA, Hudson L, Mays A, et al. ASPEN safe practices for enteral nutrition therapy. Journal of Parenteral and Enteral Nutrition. 2017;41(1):15–103. https://doi.org/10.1177/0148607116673053

40. Raheem D, Carrascosa C, Ramos F, Saraiva A, Raposo A. Texture-modified food for dysphagic patients: A comprehensive review. Int J Environ Res Public Health. 2021;18(10):5125. https://doi.org/10.3390/ijerph18105125

41. Korwin A, Honiden S. Reconsidering nutritional support in critically ill patients. In: Seminars in Respiratory and Critical Care Medicine. Thieme Medical Publishers; 2019. p. 580–93. https://doi.org/10.1055/s-0039-1697967

42. Fernández A, Toca M del C, Vinderola G, Sosa P. Fiber in enteral nutrition: why and what for? Arch Argent Pediatr. 2025;123(1). https://doi.org/10.5546/aap.2023-10274.eng

43. Zhu Y, Dong L, Huang L, Shi Z, Dong J, Yao Y, et al. Effects of oat β-glucan, oat resistant starch, and the whole oat flour on insulin resistance, inflammation, and gut microbiota in high-fat-diet-induced type 2 diabetic rats. J Funct Foods. 2020 Jun;69:103939. https://doi:10.1016/j.jff.2020.103939

44. Hotchkiss AT, Chau HK, Strahan GD, Nuñez A, Simon S, White AK, et al. Structural characterization of red beet fiber and pectin. Food Hydrocoll. 2022;129:107549. https://doi.org/10.1016/j.foodhyd.2022.107549

45. Tomsen N, Bolívar-Prados M, Ortega O, Clavé P. Therapeutic effect on swallowing function and on hydration status of a new liquid gum-based thickener in independently-living older patients with oropharyngeal dysphagia. Nutrients. 2023;15(21):4621. https://doi.org/10.3390/nu15214621

46. Hadde EK, Chen J. Shear and extensional rheological characterization of thickened fluid for dysphagia management. J Food Eng. 2019;245:18–23. https://doi.org/10.3390/nu15214621

47. Patra T, Rinnan Å, Olsen K. The physical stability of plant-based drinks and the analysis methods thereof. Food Hydrocoll. 2021;118:106770. https://doi.org/10.1016/j.foodhyd.2021.106770

48. Fernandes CG, Sonawane SK, Arya SS. Optimization and modeling of novel multigrain beverage: Effect of food additives on physicochemical and functional properties. J Food Process Preserv. 2019;43(10):e14151. https://doi.org/10.1111/jfpp.14151

49. DeBenedictis JN, de Kok TM, van Breda SG. Impact of processing method and storage time on phytochemical concentrations in an antioxidant-rich food mixture. Antioxidants. 2023;12(6):1252. https://doi.org/10.3390/antiox12061252

50. Poljsak B, Kovač V, Milisav I. Antioxidants, food processing and health. Antioxidants. 2021;10(3):433. https://doi.org/10.3390/antiox10030433

51. Preti R, Rapa M, Vinci G. Effect of steaming and boiling on the antioxidant properties and biogenic amines content in green bean (Phaseolus vulgaris) varieties of different colours. J Food Qual. 2017;2017(1):5329070. https://doi.org/10.1155/2017/5329070

52. Wruss J, Waldenberger G, Huemer S, Uygun P, Lanzerstorfer P, Müller U, et al. Compositional characteristics of commercial beetroot products and beetroot juice prepared from seven beetroot varieties grown in Upper Austria. Journal of Food Composition and Analysis. 2015;42:46–55. https://doi.org/10.1016/j.jfca.2015.03.005

53. Sadowska-Bartosz I, Bartosz G. Biological properties and applications of betalains. Molecules. 2021;26(9):2520. https://doi.org/10.3390/molecules26092520

54. Pasmans K, Meex RCR, van Loon LJC, Blaak EE. Nutritional strategies to attenuate postprandial glycemic response. Obesity Reviews. 2022;23(9):e13486. https://doi.org/10.1111/obr.13486

55. Soomro MA, Khan S, Majid A, Bhatti S, Perveen S, Phull AR. Pectin as a biofunctional food: comprehensive overview of its therapeutic effects and antidiabetic-associated mechanisms. Discover Applied Sciences. 2024;6(6):298. https://doi.org/10.1007/s42452-024-05968-1

56. Meng H, Matthan NR, Ausman LM, Lichtenstein AH. Effect of macronutrients and fiber on postprandial glycemic responses and meal glycemic index and glycemic load value determinations. Am J Clin Nutr. 2017;105(4):842–53. https://doi.org/10.3945/ajcn.116.144162

57. Peres M, Costa HS, Silva MA, Albuquerque TG. The health effects of low glycemic index and low glycemic load interventions on prediabetes and type 2 diabetes mellitus: a literature review of RCTs. Nutrients. 2023;15(24):5060. https://doi.org/10.3390/nu15245060

Downloads

Published

2026-05-29

Issue

Section

Articles