Moringa oleifera Leaf Supplementation as a Glycemic Control Strategy in Subjects with Prediabetes

Sonia Gómez-Martínez, Ligia E Díaz-Prieto, Iván Vicente Castro, César Jurado, Nerea Iturmendi, Maria Carmen Martín-Ridaura, Nuria Calle, María Dueñas, María J Picón, Ascensión Marcos, Esther Nova, Sonia Gómez-Martínez, Ligia E Díaz-Prieto, Iván Vicente Castro, César Jurado, Nerea Iturmendi, Maria Carmen Martín-Ridaura, Nuria Calle, María Dueñas, María J Picón, Ascensión Marcos, Esther Nova

Abstract

Moringa oleifera (MO) is a multipurpose plant with a high polyphenol content, which is being increasingly consumed to lessen the risk of chronic metabolic diseases such as Type 2 diabetes; however, scientific evidence from clinical trials is scarce. A double-blind, randomized, placebo-controlled, parallel group intervention study with MO leaves as a food supplement was conducted in subjects with prediabetes. They consumed six daily capsules of MO dry leaf powder (2400 mg/day) (MO, n = 31) or placebo (PLC, n = 34) over 12 weeks. Glycemia, appetite-controlling hormones and gut microbiota composition were studied. ANCOVA with the fixed factor "treatment" and the basal value as covariate was used to compare the change score between the groups. The results showed significant differences between groups in the rate of change of fasting blood glucose (FBG) and glycated hemoglobin (HbA1c), which showed opposite directions during the intervention, decreasing in MO and increasing in PLC. No different change scores were found between the groups in microbiota, hepatic and renal function markers or the appetite-controlling hormones measured. In conclusion, MO supplementation resulted in favorable changes in glycaemia markers compared to placebo in the subjects with prediabetes studied, suggesting that MO might act as a natural antihyperglycemic agent.

Keywords: Moringa oleifera; food supplement; gastrointestinal hormones; glycemic control; gut microbiota; polyphenol-rich plant food; prediabetes.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Flow chart of study subjects. PLC, Placebo; MO, Moringa oleifera; wk, weeks.
Figure 2
Figure 2
Potential predictor variables between subjects improving and not improving HbA1c during the intervention in the MO group. Bacteroides, ANCOVA with BMI adjustment, p = 0.085; GOT, GPT and Bilirubin, Mann Whitney U test, p = 0.032 p = 0.022 and p = 0.014, respectively. No differences were found in basal values in the PLC group in those variables.

References

    1. Leone A., Spada A., Battezzati A., Schiraldi A., Aristil J., Bertoli S. Cultivation, Genetic, Ethnopharmacology, Phytochemistry and Pharmacology of Moringa oleifera Leaves: An Overview. Int. J. Mol. Sci. 2015;16:12791–12835. doi: 10.3390/ijms160612791.
    1. Taher M., Bin Nyeem M., Ahammed M., Hossain M., Nazrul Islam M. Moringa oleifera (Shajna): The wonderful indigenous medicinal plant. Asian J. Med. Biol. Res. 2017;3:20–30. doi: 10.3329/ajmbr.v3i1.32032.
    1. Kou X., Li B., Olayanju J.B., Drake J.M., Chen N. Nutraceutical or Pharmacological Potential of Moringa oleifera Lam. Nutrients. 2018;10:343. doi: 10.3390/nu10030343.
    1. Waterman C., Rojas-Silva P., Tumer T.B., Kuhn P., Richard A.J., Wicks S., Stephens J.M., Wang Z., Mynatt R., Cefalu W., et al. Isothiocyanate-rich Moringa oleifera extract reduces weight gain, insulin resistance, and hepatic gluconeogenesis in mice. Mol. Nutr. Food Res. 2015;59:1013–1024. doi: 10.1002/mnfr.201400679.
    1. Vergara-Jimenez M., Almatrafi M.M., Fernandez M.L. Bioactive Components in Moringa Oleifera Leaves Protect against Chronic Disease. Antioxidants. 2017;6:91. doi: 10.3390/antiox6040091.
    1. Dou Z., Chen C., Fu X. Bioaccessibility, antioxidant activity and modulation effect on gut microbiota of bioactive compounds from Moringa oleifera Lam. leaves during digestion and fermentation in vitro. Food Funct. 2019;10:5070–5079. doi: 10.1039/C9FO00793H.
    1. González Garza N.G., Chuc Koyoc J.A., Torres Castillo J.A., García Zambrano E.A., Betancur Ancona D., Chel Guerrero L., Sinagawa García S.R. Biofunctional properties of bioactive peptide fractions from protein isolates of moringa seed (Moringa oleifera) J. Food Sci. Technol. 2017;54:4268–4276. doi: 10.1007/s13197-017-2898-8.
    1. Wang F., Bao Y.F., Si J.J., Duan Y., Weng Z.B., Shen X.C. The Beneficial Effects of a Polysaccharide from Moringa oleifera Leaf on Gut Microecology in Mice. J. Med. Food. 2019;22:907–918. doi: 10.1089/jmf.2018.4382.
    1. Tian H., Liang Y., Liu G., Li Y., Deng M., Liu D., Guo Y., Sun B. Moringa oleifera polysaccharides regulates caecal microbiota and small intestinal metabolic profile in C57BL/6 mice. Int. J. Biol. Macromol. 2021;1:595–611. doi: 10.1016/j.ijbiomac.2021.03.144.
    1. Jaja-Chimedza A., Graf B.L., Simmler C., Kim Y., Kuhn P., Pauli G.F., Raskin I. Biochemical characterization and anti-inflammatory properties of an isothiocyanate-enriched moringa (Moringa oleifera) seed extract. PLoS ONE. 2017;12:e0182658. doi: 10.1371/journal.pone.0182658.
    1. Li S., Li W., Wu R., Yin R., Sargsyan D., Raskin I., Kong A.N. Epigenome and transcriptome study of moringa isothiocyanate in mouse kidney mesangial cells induced by high glucose, a potential model for diabetic-induced nephropathy. AAPS J. 2019;5:8. doi: 10.1208/s12248-019-0393-z.
    1. Sreedharan N., Mahadev R., Sonal Sekhar M. Targeting Prediabetes to Preempt Diabetes (Chap 3) In: Bagchi D., Nair S., editors. Nutritional and Therapeutic Interventions for Diabetes and Metabolic Syndrome. 2nd ed. Elsevier; Amsterdam, The Netherlands: Academic Press; Cambridge, MA, USA: 2018. pp. 33–42.
    1. Nova E., Redondo-Useros N., Martínez-García R.M., Gómez-Martínez S., Díaz-Prieto L.E., Marcos A. Potential of Moringa oleifera to Improve Glucose Control for the Prevention of Diabetes and Related Metabolic Alterations: A Systematic Review of Animal and Human Studies. Nutrients. 2020;10:2050. doi: 10.3390/nu12072050.
    1. Vargas-Sánchez K., Garay-Jaramillo E., González-Reyes R.E. Effects of Moringa oleifera on Glycemia and Insulin Levels: A Review of Animal and Human Studies. Nutrients. 2019;11:2907. doi: 10.3390/nu11122907.
    1. Ahmad J., Khan I., Johnson S.K., Alam I., Din Z.U. Effect of Incorporating Stevia and Moringa in Cookies on Postprandial Glycemia, Appetite, Palatability, and Gastrointestinal Well-Being. J. Am. Coll. Nutr. 2018;37:133–139. doi: 10.1080/07315724.2017.1372821.
    1. Anthanont P., Lumlerdkij N., Akarasereenont P., Vannasaeng S., Sriwijitkamol A. Moringa oleifera Leaf Increases Insulin Secretion after Single Dose Administration: A Preliminary Study in Healthy Subjects. J. Med. Assoc. Thail. 2016;99:308–313.
    1. Fombang E.N., Saa W.R. Antihyperglycemic Activity of Moringa oleifera Lam leaf functional tea in rat models and human subjects. Food Nutr. Sci. 2016;7:1021–1032. doi: 10.4236/fns.2016.711099.
    1. Leone A., Bertoli S., Di Lello S., Bassoli A., Ravasenghi S., Borgonovo G., Forlani F., Battezzati A. Effect of Moringa oleifera Leaf Powder on Postprandial Blood Glucose Response: In Vivo Study on Saharawi People Living in Refugee Camps. Nutrients. 2018;10:1494. doi: 10.3390/nu10101494.
    1. Kumari D.J. Hypoglycemic effect of Moringa oleifera and Azadirachta indica in type-2 diabetes. Bioscan. 2010;5:211–214.
    1. Giridhari V.A., Malathi D., Geetha K. Anti diabetic property of drumstick (Moringa oleifera) leaf tablets. Int. J. Health Nutr. 2011;2:1–5.
    1. Kushwaha S., Chawla P., Kochhar A. Effect of supplementation of drumstick (Moringa oleifera) and amaranth (Amaranthus tricolor) leaves powder on antioxidant profile and oxidative status among postmenopausal women. J. Food Sci. Technol. 2014;51:3464–3469. doi: 10.1007/s13197-012-0859-9.
    1. Taweerutchana R., Lumlerdkij N., Vannasaeng S., Akarasereenont P., Sriwijitkamol A. Effect of Moringa oleifera Leaf Capsules on Glycemic Control in Therapy-Naïve Type 2 Diabetes Patients: A Randomized Placebo Controlled Study. Evid.-Based Complementary Altern. Med. 2017;2017:6581390. doi: 10.1155/2017/6581390.
    1. American Diabetes Association Standards of medical care in diabetes. Diabetes Care. 2013;36:S11–S66. doi: 10.2337/dc13-S011.
    1. González-Zancada N., Redondo-Useros N., Díaz L.E., Gómez-Martínez S., Marcos A., Nova E. Association of Moderate Beer Consumption with the Gut Microbiota and SCFA of Healthy Adults. Molecules. 2020;25:4772. doi: 10.3390/molecules25204772.
    1. Redondo N., García-González N., Diaz-Prieto L.E., Olmedilla-Alonso B., Martín-Diana A.B., Asensio-Vegas C., Nova E. Effects of ewe’s milk yogurt (whole and semi-skimmed) and cow’s milk yogurt on inflammation markers and gut microbiota of subjects with borderline-high plasma cholesterol levels: A crossover study. Eur. J. Nutr. 2019;58:1113–1124. doi: 10.1007/s00394-018-1626-0.
    1. Olayaki L.A., Irekpita J.E., Yakubu M.T., Ojo O.O. Methanolic extract of Moringa oleifera leaves improves glucose tolerance, glycogen synthesis and lipid metabolism in alloxan-induced diabetic rats. J. Basic Clin. Physiol. Pharmacol. 2015;26:585–593. doi: 10.1515/jbcpp-2014-0129.
    1. Tang Y., Choi E.J., Han W.C., Oh M., Kim J., Hwang J.Y., Park P.J., Moon S.H., Kim Y.S., Kim E.K. Moringa oleifera from Cambodia ameliorates oxidative stress, hyperglycemia, and kidney dysfunction in type 2 diabetic mice. J. Med. Food. 2017;20:502–510. doi: 10.1089/jmf.2016.3792.
    1. Paula P.C., Sousa D.O., Oliveira J.T., Carvalho A.F., Alves B.G., Pereira M.L., Farias D.F., Viana M.P., Santos F.A., Morais T.C., et al. A protein isolate from Moringa oleifera leaves has hypoglycemic and antioxidant effects in alloxan-induced diabetic mice. Molecules. 2017;22:271. doi: 10.3390/molecules22020271.
    1. Egbuna C., Awuchi C.G., Kushwaha G., Rudrapal M., Patrick-Iwuanyanwu K.C., Singh O., Odoh U.E., Khan J., Jeevanandam J., Kumarasamy S., et al. Bioactive Compounds Effective Against Type 2 Diabetes Mellitus: A Systematic Review. Curr. Top. Med. Chem. 2021;21:1067–1095. doi: 10.2174/1568026621666210509161059.
    1. Chen G.L., Xu Y.B., Wu J.L., Li N., Guo M.Q. Hypoglycemic and hypolipidemic effects of Moringa oleifera leaves and their functional chemical constituents. Food Chem. 2020;15:127478. doi: 10.1016/j.foodchem.2020.127478.
    1. Zainab B., Ayaz Z., Alwahibi M.S., Khan S., Rizwana H., Soliman D.W., Alawaad A., Mehmood Abbasi A. In-silico elucidation of Moringa oleifera phytochemicals against diabetes mellitus. Saudi J. Biol. Sci. 2020;27:2299–2307. doi: 10.1016/j.sjbs.2020.04.002.
    1. Oboh G., Oyeleye S.I., Akintemi O.A., Olasehinde T.A. Moringa oleifera supplemented diet modulates nootropic-related biomolecules in the brain of STZ-induced diabetic rats treated with acarbose. Metab. Brain Dis. 2018;33:457–466. doi: 10.1007/s11011-018-0198-2.
    1. Villarruel-López A., López-de la Mora D.A., Vázquez-Paulino O.D., Puebla-Mora A.G., Torres-Vitela M.R., Guerrero-Quiroz L.A., Nuño K. Effect of Moringa oleifera consumption on diabetic rats. BMC Complementary Altern. Med. 2018;18:127. doi: 10.1186/s12906-018-2180-2.
    1. Bisanz J.E., Enos M.K., PrayGod G., Seney S., Macklaim J.M., Chilton S., Willner D., Knight R., Fusch C., Fusch G., et al. Microbiota at Multiple Body Sites during Pregnancy in a Rural Tanzanian Population and Effects of Moringa-Supplemented Probiotic Yogurt. Appl. Environ. Microbiol. 2015;81:4965–4975. doi: 10.1128/AEM.00780-15.
    1. Colldén G., Tschöp M.H., Müller T.D. Therapeutic Potential of Targeting the Ghrelin Pathway. Int. J. Mol. Sci. 2017;18:798. doi: 10.3390/ijms18040798.
    1. Ajibade T.O., Arowolo R., Olayemi F.O. Phytochemical screening and toxicity studies on the methanol extract of the seeds of Moringa oleifera. J. Complementary Integr. Med. 2013;10:11–16. doi: 10.1515/jcim-2012-0015.
    1. Stohs S.J., Hartman M.J. Review of the Safety and Efficacy of Moringa oleifera. Phytother. Res. 2015;29:796–804. doi: 10.1002/ptr.5325.
    1. Omodanisi E.I., Aboua Y.G., Chegou N.N., Oguntibeju O.O. Hepatoprotective, Antihyperlipidemic, and Anti-inflammatory Activity of Moringa oleifera in Diabetic-induced Damage in Male Wistar Rats. Pharmacogn. Res. 2017;9:182–187. doi: 10.4103/0974-8490.204651.

Source: PubMed

3
Sottoscrivi