Propolis extract supplementation in the complementary treatment of adults and elderly with Type 2 Diabetes Mellitus: a systematic review of clinical trial

Authors

  • Yuri Silva dos Santos
  • Lucas Lombardo Borda
  • Roberta Soares Casaes
  • Alessandra da Silva Pereira
  • Elaine Cristina de Souza Lima
  • Felipe de Souza Cardoso

DOI:

https://doi.org/10.55905/oelv22n1-094

Keywords:

propolis, antioxidants, dietary supplement, diabetes mellitus

Abstract

Background & aims: bee products, such as propolis, have important natural properties to help reduce the risk of chronic noncommunicable diseases. Therefore, the objective of this review was to determine whether propolis intake helps to improve laboratory and anthropometrics indicators related to metabolic changes in type 2 Diabetes mellitus. Methods: systematic review of randomized clinical trials, published between 2000 and 2021, in Pubmed, Lilacs and SciELO databases, which indicated significant effects of propolis on laboratory indicators related to glycemic homeostasis, antioxidant and anti-inflammatory status. The articles were obtained according to the model recommended by PRISMA. After general analysis, protocols were used to assess the quality of evidence, using the Jadad scale, Consort and Cochrane. Results: glycemic homeostasis was evaluated using the following laboratory indicators: HOMA-IR, HOMA-β, fructosamine, fasting glucose and glycated hemoglobin. Significant changes in fasting glucose, 2-hour postprandial glucose were indicated in 71.43% of the studies. The antioxidant potential of propolis was evaluated in 71.43% of clinical trials. There was a significant reduction in pro-inflammatory cytokines, an increase in catalase activity and an increase in the antioxidant capacity of glutathione. The lipid profile was analyzed in 42.86% of the studies, indicating significant changes in total, LDL and HDL cholesterol. Conclusion: propolis can be considered an aggregating alternative for the conventional treatment of type 2 Diabetes mellitus. However, this food supplement is not a “miraculous” product, which eliminates the need for changes in lifestyle, including eating habits and regular physical activity, as well as the use of drugs, when necessary.

References

Cao, B., Bray, F., Ilbawi, A., and Soerjomataram, I. 2018. Effect on longevity of one-third reduction in premature mortality from non-communicable diseases by 2030: a global analysis of the Sustainable Development Goal health target. The Lancet Global Health, 6(12), e1288-e1296. Doi: 10.1016/S2214-109X(18)30411-X.

Trierweiler, H., Kisielewicz, G., Hoffmann Jonasson, T., Rasmussen Petterle, R., Aguiar Moreira, C., and Zeghbi Cochenski Borba, V. 2018. Sarcopenia: a chronic complication of type 2 diabetes mellitus. Diabetology & metabolic syndrome, 10(1), 1-9. Doi: 10.1186/s13098-018-0326-5.

Chang, E., and Kim, C. Y. 2019. Natural products and obesity: a focus on the regulation of mitotic clonal expansion during adipogenesis. Molecules, 24(6), 1157. Doi: 10.3390/molecules24061157.

Nilson, E. A. F., Andrade, R. D. C. S., Brito, D. A. D., and Oliveira, M. L. D. 2020. Custos atribuíveis a obesidade, hipertensão e diabetes no Sistema Único de Saúde, Brasil, 2018. Revista Panamericana de Salud Pública, 44, e32. Doi: 10.26633/RPSP.2020.32.

Pahlavani, N., Malekahmadi, M., Firouzi, S., Rostami, D., Sedaghat, A., Moghaddam, A. B., and Ghayour-Mobarhan, M. 2020. Molecular and cellular mechanisms of the effects of Propolis in inflammation, oxidative stress and glycemic control in chronic diseases. Nutrition & Metabolism, 17(1), 1-12. Doi: 10.1186/s12986-020-00485-5.

Kocot, J., Kiełczykowska, M., Luchowska-Kocot, D., Kurzepa, J., and Musik, I. 2018. Antioxidant potential of propolis, bee pollen, and royal jelly: possible medical application. Oxidative medicine and cellular longevity, v. 2018. Doi: 10.1155/2018/7074209.

Llauradó Maury, G., Méndez Rodríguez, D., Hendrix, S., Escalona Arranz, J. C., Fung Boix, Y., Pacheco, A. O., and Cuypers, A. 2020. Antioxidants in plants: A valorization potential emphasizing the need for the conservation of plant biodiversity in Cuba. Antioxidants, 9(11), 1048. Doi: 10.3390/antiox9111048.

Toreti, V. C., Sato, H. H., Pastore, G. M., and Park, Y. K. 2013. Recent progress of propolis for its biological and chemical compositions and its botanical origin. Evidence-based complementary and alternative medicine, 2013. Doi: 10.1155/2013/697390.

Bankova, V., Bertelli, D., Borba, R., Conti, B. J., da Silva Cunha, I. B., Danert, C., and Zampini, C. 2019. Standard methods for Apis mellifera propolis research. Journal of Apicultural Research, 58(2), 1-49. Doi: 10.1080/00218839.2016.1222661.

Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., and Moher, D. 2021. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Systematic reviews, 10(1), 1-11. Doi: 10.1186/s13643-021-01626-4.

Jadad, A. R., Moore, R. A., Carroll, D., Jenkinson, C., Reynolds, D. J. M., Gavaghan, D. J., and McQuay, H. J. 1996. Assessing the quality of reports of randomized clinical trials: is blinding necessary?. Controlled clinical trials, 17(1), 1-12. Doi: 10.1016/0197-2456(95)00134-4.

Schulz, K. F., Altman, D. G., Moher, D., and CONSORT Group. 2010. CONSORT 2010 statement: updated guidelines for reporting parallel group randomized trials. Annals of internal medicine, 152(11), 726-732. Doi: 10.7326/0003-4819-152-11-201006010-00232.

Higgins, J. P. 2011. Cochrane handbook for systematic reviews of interventions. Version 5.1. 0 [updated March 2011]. The Cochrane Collaboration. www. cochrane-handbook. org.

El‐Sharkawy, H. M., Anees, M. M., and Van Dyke, T. E. 2016. Propolis improves periodontal status and glycemic control in patients with type 2 diabetes mellitus and chronic periodontitis: a randomized clinical trial. Journal of periodontology, 87(12), 1418-1426. Doi: 10.1902/jop.2016.150694.

Zakerkish, M., Jenabi, M., Zaeemzadeh, N., Hemmati, A. A., and Neisi, N. 2019. The effect of Iranian propolis on glucose metabolism, lipid profile, insulin resistance, renal function and inflammatory biomarkers in patients with type 2 diabetes mellitus: A randomized double-blind clinical trial. Scientific reports, 9(1), 1-11. Doi: 10.1038/s41598-019-43838-8.

Fukuda, T., Fukui, M., Tanaka, M., Senmaru, T., Iwase, H., Yamazaki, M., and Marunaka, Y. 2015. Effect of Brazilian green propolis in patients with type 2 diabetes: A double-blind randomized placebo-controlled study. Biomedical reports, 3(3), 355-360. Doi: 10.3892/br.2015.436.

Samadi, N., Mozaffari-Khosravi, H., Rahmanian, M., and Askarishahi, M. 2017. Effects of bee propolis supplementation on glycemic control, lipid profile and insulin resistance indices in patients with type 2 diabetes: a randomized, double-blind clinical trial. Journal of integrative medicine, 15(2), 124-134. Doi: 10.1016/S2095-4964(17)60315-7.

Afsharpour, F., Hashemipour, S., Khadem-Haghighian, H., and Koushan, Y. 2017. Effects of Iranian propolis on glycemic status, inflammatory factors, and liver enzyme levels in type 2 diabetic patients: a randomized, double-blind, placebo- controlled, clinical trial. Journal of Nutritional Sciences and Dietetics, p. 9-14. Doi: 10.1007/s40200-020-00696-w.

Hesami, S., Hashemipour, S., Shiri-Shahsavar, M. R., Koushan, Y., and Haghighian, H. K. 2019. Administration of Iranian Propolis attenuates oxidative stress and blood glucose in type II diabetic patients: A randomized, double-blind, placebo-controlled, clinical trial. Caspian journal of internal medicine, 10(1), 48. Doi: 10.22088/cjim.10.1.48.

Zhao, L., Pu, L., Wei, J., Li, J., Wu, J., Xin, Z., and Guo, C. 2016. Brazilian green propolis improves antioxidant function in patients with type 2 diabetes mellitus. International journal of environmental research and public health, 13(5), 498. Doi: 10.3390/ijerph13050498.

Koya-Miyata, S., Arai, N., Mizote, A., Taniguchi, Y., Ushio, S., Iwaki, K., Fukuda, S. 2009. Propolis prevents diet-induced hyperlipidemia and mitigates weight gain in diet-induced obesity in mice. Biological and Pharmaceutical Bulletin, 32(12), 2022-2028. Doi: 10.1248/bpb.32.2022.

Zheng, Y., Wu, Y., Tao, L., Chen, X., Jones, T. J., Wang, K., and Hu, F. 2020. Chinese Propolis prevents obesity and metabolism syndromes induced by a high fat diet and accompanied by an altered gut microbiota structure in mice. Nutrients, 12(4), 959. Doi: 10.3390/nu12040959.

Bugger, H. and Abel, D. E. 2014. Molecular mechanisms of diabetic cardiomyopathy. Diabetologia, 57(4), 660-671. Doi: 10.1007/s00125-014-3171-6.

Petrie, J. R., Guzik, T. J., and Touyz, R. M. 2018. Diabetes, hypertension, and cardiovascular disease: clinical insights and vascular mechanisms. Canadian Journal of Cardiology, 34(5), 575-584. Doi: 10.1016/j.cjca.2017.12.005.

Braga, D. C., Panka, M., Cabral, S., Bonamigo, E. L., and Bortolini, S. M. 2016. Avaliação da função renal em pacientes com diabetes mellitus em um município rural do meio oeste de Santa Catarina. Arquivos Catarinenses de Medicina, 45(3), 84-92.

Kellum, J. A., Romagnani, P., Ashuntantang, G., Ronco, C., Zarbock, A., and Anders, H. J. 2021. Acute kidney injury. Nature reviews Disease primers, 7(1), 1-17. Doi: 10.1038/s41572-021-00284-z.

Silveira, M. A. D., Teles, F., Berretta, A. A., Sanches, T. R., Rodrigues, C. E., Seguro, A. C., and Andrade, L. 2019. Effects of Brazilian green propolis on proteinuria and renal function in patients with chronic kidney disease: a randomized, double-blind, placebo-controlled trial. BMC nephrology, 20(1), 1-12. Doi: 10.1186/s12882-019-1337-7.

Zulhendri, F., Ravalia, M., Kripal, K., Chandrasekaran, K., Fearnley, J., and Perera, C. O. 2021. Propolis in metabolic syndrome and its associated chronic diseases: A narra-tive review. Antioxidants, 10(3), 348. Doi: 10.3390/antiox10030348.

Mafra, D., G. Baptista, B., Fanton, S., M. Ribeiro, M., R. Paiva, B., Cardozo, L., and A. Berretta, A. 2022. MO585: Effects of EPP-AF® Green Propolis Extract Supplementation on Inflammatory Markers in Patients With chronic Kidney Disease on Peritoneal Dialysis. Nephrology Dialysis Transplantation, 37(Supplement_3), gfac074-030. Doi: 10.1093/ndt/gfac074.030.

Tavakolpour, S., Mahmoudi, H., Mirzazadeh, A., Balighi, K., Darabi-Monadi, S., Hatami, S., and Daneshpazhooh, M. 2020. Pathogenic and protective roles of cytokines in pemphigus: a systematic review. Cytokine, 129, 155026. Doi: 10.1016/j.cyto.2020.155026.

Wiater, A., Paduch, R., Trojnar, S., Choma, A., Pleszczyńska, M., Adamczyk, P., and Tomczyk, M. 2020. The effect of water-soluble polysaccharide from jackfruit (Artocarpus heterophyllus Lam.) on human colon carcinoma cells cultured in vitro. Plants, 9(1), 103. Doi: 10.3390/plants9010103.

Gao, W., Pu, L., Wei, J., Yao, Z., Wang, Y., Shi, T., and Guo, C. 2018. Serum antioxidant parameters are significantly increased in patients with type 2 diabetes mellitus after consumption of Chinese propolis: a randomized controlled trial based on fasting serum glucose level. Diabetes Therapy, 9(1), 101-111. Doi: 10.1007/s13300-017-0341-9.

Incalza, M. A., D'Oria, R., Natalicchio, A., Perrini, S., Laviola, L., and Giorgino, F. 2018. Oxidative stress and reactive oxygen species in endothelial dysfunction associated with cardiovascular and metabolic diseases. Vascular pharmacology, 100, 1-19. Doi: 10.1016/j.vph.2017.05.005.

Rendra, E., Riabov, V., Mossel, D. M., Sevastyanova, T., Harmsen, M. C., and Kzhyshkowska, J. 2019. Reactive oxygen species (ROS) in macrophage activation and function in diabetes. Immunobiology, 224(2), 242-253. Doi: 10.1016/j.imbio.2018.11.010.

Mujica, V., Orrego, R., Pérez, J., Romero, P., Ovalle, P., Zúñiga-Hernández, J., Arredondo, M., Leiva, E. 2017. The Role of Propolis in Oxidative Stress and Lipid Metabolism: A Randomized Controlled Trial. Evid Based Complement Alternat Med. 2017:4272940. doi: 10.1155/2017/4272940.

Hahn, G. F., de Oliveira, J. R., and Bock, P. M. 2017. O papel do fator nuclear eritróide 2 relacionado ao fator 2 (Nrf2) no diabetes mellitus. Clinical & Biomedical Research, 37(3). Doi: 10.4322/2357-9730.73884.

Hadi, A., Rafie, N., and Arab, A. 2021. Bee products consumption and cardiovascular diseases risk factors: a systematic review of interventional studies. International Journal of Food Properties, 24(1), 115-128. Doi: 10.1080/10942912.2020.1867568.

Maher, S., and Brayden, D. J. 2021. Formulation strategies to improve the efficacy of intestinal permeation enhancers. Advanced Drug Delivery Reviews, 177, 113925. Doi: 10.1016/j.addr.2021.113925.

Wan, M. L. Y., Co, V. A., and El-Nezami, H. 2021. Dietary polyphenol impact on gut health and microbiota. Critical reviews in food science and nutrition, 61(4), 690-711. Doi: 10.1080/10408398.2020.1744512.

Aravind, S. M., Wichienchot, S., Tsao, R., Ramakrishnan, S., and Chakkaravarthi, S. 2021. Role of dietary polyphenols on gut microbiota, their metabolites and health benefits. Food Research International, v. 142, p. 110189. Doi: 10.1016/j.foodres.2021.110189.

Pasupuleti, V. R., Sammugam, L., Ramesh, N., and Gan, S. H. 2017. Honey, propolis, and royal jelly: a comprehensive review of their biological actions and health benefits. Oxidative medicine and cellular longevity, 2017. Doi: 10.1155/2017/1259510.

Abreu, V. G., da Silva Lopes, R. S., Lima, E. M., and Santos, J. S. 2021. A importância da alimentação na hipertrofia. Research, Society and Development, 10(14), e431101422041. Doi: 10.33448/rsd-v10i14.22041.

Von Kortzfleisch, V. T., Karp, N. A., Palme, R., Kaiser, S., Sachser, N., and Richter, S. H. 2020. Improving reproducibility in animal research by splitting the study population into several ‘mini-experiments’. Scientific reports, 10(1), 1-16. Doi: 10.1038/s41598-020-73503-4.

Sathler, M. M., and Menezes, M. Â. D. B. C. 2021. NUTRICIONISMO: Uma abordagem que ignora a complexidade dos alimentos. PISTA: Periódico Interdisciplinar [Sociedade Tecnologia Ambiente], 3(1), 79-95.

Published

2024-01-18

How to Cite

dos Santos, Y. S., Borda, L. L., Casaes, R. S., Pereira, A. da S., Lima, E. C. de S., & Cardoso, F. de S. (2024). Propolis extract supplementation in the complementary treatment of adults and elderly with Type 2 Diabetes Mellitus: a systematic review of clinical trial. OBSERVATÓRIO DE LA ECONOMÍA LATINOAMERICANA, 22(1), 1769–1800. https://doi.org/10.55905/oelv22n1-094

Issue

Section

Articles