Glycemic profile, inflammatory markers, biochemical and histopathological parameters of mice fed with fermented dairy beverage with clove essential oil
DOI:
https://doi.org/10.33448/rsd-v10i4.13826Keywords:
Syzygium aromaticum; Tolerância a glicose; Sensibilidade a insulina; Citocinas; Hepatotoxicidade.Abstract
Previous studies have shown that the clove essential oil concentration of 200 mg/kg did not present toxicity and histopathological changes in the liver. Based on the evidence presented in this study, we decided to evaluate in vivo the ability of a previously developed fermented dairy beverage, tested only in vitro, in which the standard chemical preservative, potassium sorbate, was replaced by clove essential oil (2 μl/ml), to be a functional food. To this end, twenty-four male Swiss mice were divided into three groups and submitted insulin sensitivity (IST) and glucose tolerance (GTT) testing, evaluation of physiological and biochemical parameters, histopathological analysis and quantification of the expression of anti-inflammatory and pro-inflammatory cytokines in the liver, after administering daily of the fermented dairy beverage with or without clove essential oil by gavage during 30 days. The group that received the fermented dairy beverage with clove essential oil showed a lower glycemic level in GTT, a higher sensitivity to insulin and a higher glucose decay constant rate (Kitt), with relation to the other groups. In the evaluation of physiological parameters there were no signs of toxicity in the mice during the experimental period. The biochemical parameters, histopathological analysis and expression of anti-inflammatory (IL-10) and pro-inflammatory (IL1β, IL6 e TNFα) cytokines in the liver of the mice, was not significantly affected by the treatment. These results corroborated by bioinformatics analysis demonstrate that the fermented dairy beverage with clove essential oil it can function as a substitute for conventional chemical preservatives and reduce glycemic levels.
References
Agência Nacional de Vigilância Sanitária. (2015). Anvisa. Guia de Procedimentos para Pedidos de Inclusão e Extensão de Uso de Aditivos Alimentares e Coadjuvantes de Tecnologia de Fabricação na Legislação Brasileira. http://portal.anvisa.gov.br/alimentos/aditivos-alimentares
Al-attar, A. M., & Zari, T. A. Z. (2007). Modulatory Effects of Ginger and Clove Oils on Physiological Responses in Streptozotocin-Induced Diabetic Rats. International Journal of Pharmacology, 3(1), 34–40. https://doi.org/10.3923/ijp.2007.34.40
Al-Okbi, S. Y., Mohamed, D. A., Hamed, T. E., & Edris, A. E. (2014). Protective effect of clove oil and eugenol microemulsions on fatty liver and dyslipidemia as components of metabolic syndrome. Journal of Medicinal Food, 17(7), 764–771. https://doi.org/10.1089/jmf.2013.0033
American Diabetes Association. (2016). 2. Classification and Diagnosis of Diabetes. Diabetes Care, 39(Supplement 1), S13–S22. https://doi.org/10.2337/dc16-S005
Araújo, J. R., & Martel, F. (2009). Regulação da absorção intestinal de glicose. Arquivos de Medicina, 23(2), 35–43.
Bao, C., Guo, J., Lin, G., Hu, M., & Hu, Z. (2008). TNFR gene-modified mesenchymal stem cells attenuate inflammation and cardiac dysfunction following MI. Scandinavian Cardiovascular Journal, 42(1), 56–62. https://doi.org/10.1080/14017430701543556
Barbosa, I. A., Santos, E. M., Paraíso, A. F., Chagas, P. V. F., Oliveira, L. P., Andrade, J. M. O., Farias, L. C., Carvalho, B. M. A. de, de Paula, A. M. B., Guimarães, A. L. S., & Santos, S. H. S. (2019). Liraglutide alters hepatic metabolism in high-fat fed obese mice: A bioinformatic prediction and functional analysis. Meta Gene, 20, 100553. https://doi.org/10.1016/j.mgene.2019.100553
Bonora, E., Moghetti, P., Zancanaro, C., Cigolini, M., Querena, M., Cacciatori, V., Corgnati, A., & Muggeo, M. (1989). Estimates of in vivo insulin action in man: Comparison of insulin tolerance tests with euglycemic and hyperglycemic glucose clamp studies. Journal of Clinical Endocrinology and Metabolism, 68(2), 374–378. https://doi.org/10.1210/jcem-68-2-374
Brasil. (2003). Ministério da Agricultura Pecuária e Abastecimento. Instrução Normativa no 62, de 26 de agosto de 2003. Oficializa os Métodos Analíticos Oficiais para Análises Microbiológicas para Controle de Produtos de Origem Animal e Água. Diário Oficial Da República Federativa Do Brasil. http://extranet.agricultura.gov.br/sislegis-consulta/consultarLegislacao.do?operacao=visualizar&id=2851
Brasil. (2005). Ministério da Agricultura Pecuária e Abastecimento. Instrução Normativa n.o 16, de 23 de agosto de 2005. Aprova o regulamento Técnico de Identidade e Qualidade de Bebidas Láctea. Diário Oficial Da República Federativa Do Brasil. https://www2.cead.ufv.br/sgal/files/apoio/legislacao/legislacao6.pdf
Brasil. (2006). Ministério da Agricultura Pecuária e Abastecimento. Instrução Normativa no 68 de 12 de dezembro de 2006. Oficializa os Métodos Analíticos Oficiais Físico-Químicos, para Controle de Leite e Produtos Lácteos. Diário Oficial Da República Federativa Do Brasil. https://www.diariodasleis.com.br/busca/exibelink.php?numlink=1-77-23-2006-12-12-68
Brasil. (2007). Ministério da Agricultura Pecuária e Abastecimento. Instrução Normativa n° 46, de 23 de outubro de 2007. Regulamento Técnico de Identidade e Qualidade de Leites Fermentados. Diário Oficial Da República Federativa Do Brasil. http://www.cidasc.sc.gov.br/inspecao/files/2012/08/instruÇÃo-normativa-no-46-de-23-de-outubro-de-2007.pdf
Brasil. (2015). Ministério da Ciência Tecnologia e Inovação Conselho Nacional de Controle de Experimentação Animal. Normativas do CONCEA para produção, manutenção ou utilização de animais em atividades de ensino ou pesquisa científica. Lei, Decreto, Portarias, Resoluções (MCTI/CONCEA (ed.); 2nd ed.).
Brunt, E. M., Janney, C. G., Bisceglie, A. M. Di, Neuschwander-tetri, B. A., & Bacon, B. R. (1999). Nonalcoholic Steatohepatitis : A Proposal for Grading and Staging the Histological Lesions. The American Journal of Gastroenterology, 94(9).
Cortés-Rojas, D. F., de Souza, C. R. F., & Oliveira, W. P. (2014). Clove (Syzygium aromaticum): a precious spice. Asian Pacific Journal of Tropical Biomedicine, 4(2), 90–96. https://doi.org/10.1016/S2221-1691(14)60215-X
Dhama, K., Karthik, K., Khandia, R., Munjal, A., Tiwari, R., Rana, R., Khurana, S. K., Sana Ullah, Khan, R. U., Alagawany, M., Farag, M. R., Dadar, M., & Joshi, S. K. (2018). Medicinal and therapeutic potential of herbs and plant metabolites / extracts countering viral pathogens - current knowledge and future prospects. Current Drug Metabolism, 19(3), 236–263. https://doi.org/10.2174/1389200219666180129145252
Di Cerbo, A., Morales-Medina, J. C., Palmieri, B., Pezzuto, F., Cocco, R., Flores, G., & Iannitti, T. (2017). Functional foods in pet nutrition: focus on dogs and cats. Research in Veterinary Science, 112, 161–166. https://doi.org/10.1016/j.rvsc.2017.03.020
Elkomy, A., Aboubakr, M., Ibrahim, S., & Abdelhamid, Y. (2018). Protective effects of Syzygium aromaticum oil ( Clove ) against acrylamide induced hepatic , renal , and testicular toxicity in rats. 6(1), 12–17. https://doi.org/10.14419/ijpt.v6i1.10972
Fan, S., Yin, Q., Li, D., Ma, J., Li, L., Chai, S., Guo, H., & Yang, Z. (2020). Anti-neuroinflammatory effects of Eucommia ulmoides Oliv. In a Parkinson’s mouse model through the regulation of p38/JNK-Fosl2 gene expression. Journal of Ethnopharmacology, 260, 113016. https://doi.org/10.1016/j.jep.2020.113016
Farias, P. K. S. (2016). Elaboração de bebida láctea fermentada com adição de óleo essencial. Instituto de Ciências Agrárias - Universidade Federal de Minas Gerais(ICA-UFMG).
Figueiredo, J. S. B., Santos, G. L. M., Lopes, J. P. A., Fernandes, L. B., Silva, F. N., Faria, R. B., Rocha, A. C. S., Farias, P. K. S., Lima, W. J. N., Durães, C. A. F., Xavier, A. R. E. de O., Carvalho, B. M. A. de, Careli, R. T., Almeida, A. C. de, & Brandi, I. V. (2019). Sensory evaluation of fermented dairy beverages supplemented with iron and added by Cerrado fruit pulps. Food Science and Technology, 39(2), 410–414. https://doi.org/10.1590/fst.32616
Food and Drug Administration FDA. (2018). Departament of Health & Human Service. Code of Federal Regulations: Title 21- food and drugs. Chapter - I food and drug administration. Department of health and human services. Subchapter B - food for human consumption (continued). Part 184 -direct food s. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfCFR/CFRSearch.cfm?fr=170.30
Hall, P., & Cash, J. (2012). What is the Real Function of the Liver ‘ Function ’ Tests ? 81(August 2011), 30–36.
Hopkins, B. D., Goncalves, M. D., & Cantley, L. C. (2020). Insulin–PI3K signalling: an evolutionarily insulated metabolic driver of cancer. Nature Reviews Endocrinology, 16(5), 276–283. https://doi.org/10.1038/s41574-020-0329-9
Huang, X., Liu, G., Guo, J., & Su, Z. (2018). The PI3K/AKT pathway in obesity and type 2 diabetes. International Journal of Biological Sciences, 14(11), 1483–1496. https://doi.org/10.7150/ijbs.27173
Jørgensen, M. S., Tornqvist, K. S., & Hvid, H. (2017). Calculation of glucose dose for intraperitoneal glucose tolerance tests in lean and obese mice. Journal of the American Association for Laboratory Animal Science, 56(1), 95–97.
Karadogan, A., Arikiglu, H., Gokturk, F., Iscioglu, F., & Ipekci, S. (2018). PIK3R1 gene polymorphisms are associated with type 2 diabetes and related features in the Turkish population. Advances in Clinical and Experimental Medicine, 27(7), 921–927. https://doi.org/10.17219/acem/68985
Khalil, A., Omran, H., & Alsheikh, F. (2018). Balance of pro- and anti-inflammatory cytokines in livers of high fat diet rats exposed to fractionated gamma irradiation. BMC Research Notes, 11(1), 741. https://doi.org/10.1186/s13104-018-3851-2
Kwiatkowski, R. P., & Antunes, M. D. (2016). Efeito da administração dos hormônios contrarreguladores sobre o perfil profile of mice undergoing glycemic insulin-induced hypoglycemia. Brazilian Journal of Surgery and Clinical Research, 17, 68–73.
Liu, B.-B., Luo, L., Liu, X.-L., Geng, D., Li, C.-F., Chen, S.-M., Chen, X.-M., Yi, L.-T., & Liu, Q. (2015). Essential oil of Syzygium aromaticum reverses the deficits of stress-induced behaviors and hippocampal p-ERK/p-CREB/Brain-derived neurotrophic factor expression. Planta Medica, 81(03), 185–192. https://doi.org/10.1055/s-0034-1396150
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25(4), 402–408. https://doi.org/10.1006/meth.2001.1262
Machado, U. F. (1998). Transportadores de glicose. Arquivos Brasileiros de Endocrinologia & Metabologia, 42(6), 413–421. https://doi.org/10.1590/S0004-27301998000600003
Malone, M. H., & Robichaud, R. (1962). A hippocratic screen for pure or crude drug materials. Lloydia, 25, 320–332.
Matthews, J. N., Altman, D. G., Campbell, M. J., & Royston, P. (1990). Analysis of serial measurements in medical research. BMJ, 300(6719), 230–235. https://doi.org/10.1136/bmj.300.6719.230
Medzhitov, R. (2008). Origin and physiological roles of inflammation. Nature, 454(7203), 428–435. https://doi.org/10.1038/nature07201
Murakami, M., Okuyama, Y., Ogura, H., Asano, S., Arima, Y., Tsuruoka, M., Harada, M., Kanamoto, M., Sawa, Y., Iwakura, Y., Takatsu, K., Kamimura, D., & Hirano, T. (2011). Local microbleeding facilitates IL-6– and IL-17–dependent arthritis in the absence of tissue antigen recognition by activated T cells. The Journal of Experimental Medicine, 208(1), 103–114. https://doi.org/10.1084/jem.20100900
Rines, A. K., Sharabi, K., Tavares, C. D. J., & Puigserver, P. (2016). Targeting hepatic glucose metabolism in the treatment of type 2 diabetes. Nature Reviews Drug Discovery, 15(11), 786–804. https://doi.org/10.1038/nrd.2016.151
Sampaio, I. C., Medeiros, P. H. Q. S., Rodrigues, F. A. P., Cavalcante, P. A., Ribeiro, S. A., Oliveira, J. S., Prata, M. M. G., Costa, D. V. S., Fonseca, S. G. C., Guedes, M. M., Soares, A. M., Brito, G. A. C., Havt, A., Moore, S. R., & Lima, A. A. M. (2016). Impact of acute undernutrition on growth, ileal morphology and nutrient transport in a murine model. Brazilian Journal of Medical and Biological Research, 49(10). https://doi.org/10.1590/1414-431x20165340
Santos, E. M., Farias, L. C., Santos, S. H. S., de Paula, A. M. B., Oliveira e Silva, C. S. de, & Guimarães, A. L. S. (2017). Molecular finds of pressure ulcer: A bioinformatics approach in pressure ulcer. Journal of Tissue Viability, 26(2), 119–124. https://doi.org/10.1016/j.jtv.2017.01.002
Secchi, M. F., Crescenzi, M., Masola, V., Russo, F. P., Floreani, A., & Onisto, M. (2017). Heparanase and macrophage interplay in the onset of liver fibrosis. Scientific Reports, 7(1), 14956. https://doi.org/10.1038/s41598-017-14946-0
Smith, S. R., Edgar, P. J., Pozefsky, T., Chhetri, M. K., & Prout, T. E. (1975). Insulin secretion and glucose tolerance in adults with protein-calorie malnutrition. Metabolism, 24(9), 1073–1084. https://doi.org/10.1016/0026-0495(75)90101-8
Souza, K. S. S., Oliveira, S. P., Duarte, S. M., Brandi, I. V., Santos, S. H. S., Santos, E. M. S., Farias, P. K. S., Santos, H. O., & Almeida, A. C. (2018). Standardization of the methodology for calorimetric analysis of a fermented milk drink. Caderno de Ciências Agrárias, 10(2), 61–63.
Szklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N. T., Morris, J. H., Bork, P., Jensen, L. J., & Mering, C. von. (2019). STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research, 47(D1), D607–D613. https://doi.org/10.1093/nar/gky1131
Tu, Z., Moss-Pierce, T., Ford, P., & Jiang, T. A. (2014). Syzygium aromaticum L. (Clove) Extract regulates energy metabolism in myocytes. Journal of Medicinal Food, 17(9), 1003–1010. https://doi.org/10.1089/jmf.2013.0175
Vinué, Á., & González-Navarro, H. (2015). Glucose and insulin tolerance tests in the mouse. In Humana Press (pp. 247–254). https://doi.org/10.1007/978-1-4939-2929-0_17
Vo, M.-C., Nguyen-Pham, T.-N., Lee, H.-J., Lakshmi, T. J., Yang, S., Jung, S.-H., Kim, H.-J., & Lee, J.-J. (2017). Combination therapy with dendritic cells and lenalidomide is an effective approach to enhance antitumor immunity in a mouse colon cancer model. Oncotarget, 8(16), 27252–27262. https://doi.org/10.18632/oncotarget.15917
Wajchenberg, B. L., Santomauro, A. T. M. G., Nery, M., Santos, R. F., Silva, M. E. L. R., Ursich, M. J. M., & Rocha, D. M. (1999). Resistência à insulina: métodos diagnósticos e fatores que influenciam a ação da insulina. Arquivos Brasileiros de Endocrinologia & Metabologia, 43(2), 76–85. https://doi.org/10.1590/S0004-27301999000200003
Xu, Q., Higgins, T., & Cembrowski, G. S. (2015). Limiting the Testing of AST. American Journal of Clinical Pathology, 144(3), 423–426. https://doi.org/10.1309/AJCPO47VAWYRIDHG
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Keicy Sandy Silvestre de Souza; Anna Christina de Almeida; Stephanie Pedrosa de Oliveira; Igor Viana Brandi; Sérgio Henrique Sousa Santos; Francine Souza Alves Fonseca; Eliane Macedo Sobrinho Santos; Janaína Ribeiro Oliveira; Daniela Fernanda de Freitas; Deborah de Farias Lelis; Daniel Silva Moraes; João Matheus de Almeida Silva; Cintya Neves Souza; Paula Karoline Soares Farias; Raphael Rodrigues Porto; Hércules Otacilio Santos
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.