Traditional medicinal plants used in the treatment of diabetes: Ethnobotanical and ethnopharmacological studies and mechanisms of action

Year 2022, Volume: 2 Issue: 2, 145 - 154, 15.12.2022

Messaoud Belmouhoub Mustapha Tacherfıout Farid Boukhalfa Yazid Khaled Khodja Mostapha Bachir-bey

Abstract

The use of medicinal plants for the prevention and treatment of several diseases, particularly diabetes, remains the remedy and the sustainable source for many diseases. This survey was conducted out in Bejaia province in the center of Algeria to invent the main plants used in folk medicine to treat diabetes mellitus, their availability in this region, and the mode of their use. This study was carried out in 2019 in several municipalities of the study area. Ethnobotanical information was obtained using a questionnaire through direct interviews with 323 people with diabetes. Among people with diabetes interviewed, 82% present type 2 diabetes, from which more than 60% of them use medicinal plants against 36.84% only in type 1 diabetics. Diabetes affected age groups differently; the age range most affected was 61-80 years (43.96%). A total of 43 plant species belonging to 25 families were identified and listed in this study. The most frequent species used by patients are Artemisia herba-alba (34.42%), Olea europaea (13.66%), and Ajuga iva (11.47%). The part of the plant used depends on the plant; the aerial part was the more used (40.9%), followed by leaves (25%) and fruits (13.63%). The other parts, such as seed, root, flower, bark, bulb, epicarp, and rhizome, were used with low frequencies. It was also interesting to indicate that decoction and infusion were the systematic preparation methods compared to others (maceration, cooking with food, and fresh). The present study clearly showed that phytotherapy is widely adopted by center Algerian society, and there is a huge diversity of medicinal plants used for the complementary treatment of diabetes. Moreover, this investigation provides researchers with important information that can be exploited to develop anti-diabetic remedies.

Keywords

Diabetes, Traditional plant, Ethnopharmacological survey, Ethnobotanical survey, Antidiabetic

References

• Abdel-Kader, M.S., Soliman, G.A., Abdel-Rahman, R.F., Saeedan, A.S., Abd-Elsalam, R. M., Ogaly, H.A., 2019. Effect of olive leaves extract on the antidiabetic effect of glyburide for possible herb-drug interaction. Saudi Pharmaceutical Journal, 27(8), 1182-1195.
• Abu Sitta, K.H., Shomah, M.S., Salhab, A.S., 2009. Hepatotoxicity of Teucrium polium L Tea: Supporting Evidence in Mice Models. Australian Journal of Medical Herbalism, 21(4), 106-109.
• Akiyama, S., Katsumata, S.I., Suzuki, K., Ishimi, Y., Wu, J., Uehara, M., 2009. Dietary hesperidin exerts hypoglycemic and hypolipidemic effects in streptozotocin-induced marginal type 1 diabetic rats. Journal of Clinical Biochemistry and Nutrition, 46(1), 87-92.
• Alam, M.A., Subhan, N., Rahman, M.M., Uddin, S.J., Reza, H.M., Sarker, S.D., 2014. Effect of citrus flavonoids, naringin and naringenin, on metabolic syndrome and their mechanisms of action. Advances in Nutrition, 5(4), 404-417.
• Alamgeer, M.N.M., Rashid, M., Malik, M.N.H., Ahmad, T., Khan, A.Q., Javed, I., 2014. Evaluation of Hypoglycemic activity of Thymus serpyllum Linn in glucose treated mice. International Journal of Basic Medical Sciences and Pharmacy (IJBMSP), 3(2).
• Al-Ashban, R.M., Barrett, D.A., Shah, A.H., 2006. Effects of chronic treatment with ethanolic extract of Teucrium polium in mice. Journal of Herbs, Spices & Medicinal Plants, 11(4), 27-36.
• Al-Attar, A.M., Alsalmi, F.A., 2019. Effect of Olea europaea leaves extract on streptozotocin induced diabetes in male albino rats. Saudi Journal of Biological Sciences, 26(1), 118-128.
• Al-Khazraji, S.M., Al-Shamaony, L.A., Twaij, H.A., 1993. Hypoglycaemic effect of Artemisia herba alba. I. Effect of different parts and influence of the solvent on hypoglycaemic activity. Journal of Ethnopharmacology, 40(3), 163-166.
• Allali, H., Benmehdi, H., Dib, M.A., Tabti, B., Ghalem, S., Benabadji, N., 2008. Phytotherapy of diabetes in west Algeria. Asian Journal of Chemistry, 20(4), 2701-2710.
• Annunziata, G., Maisto, M., Schisano, C., Barrea, L., Ciampaglia, R., Novellinoet, E., 2018. Oleuropein as a novel anti-diabetic nutraceutical. An overview. Archives of Diabetes & Obesity, 1(3), 54-58.
• Ardestani, A., Yazdanparast, R., Jamshidi, S.H., 2008. Therapeutic effects of Teucrium polium extract on oxidative stress in pancreas of streptozotocin-induced diabetic rats. Journal of Medicinal Food, 11(3), 525-532.
• Arya, A., Looi, C.Y., Cheah, S.C., Mustafa, M.R., Mohd, M.A., 2012. Anti-diabetic effects of Centratherum anthelminticum seeds methanolic fraction on pancreatic cells, β-TC6 and its alleviating role in type 2 diabetic rats. Journal of Ethnopharmacology, 144(1), 22-32.
• ASWB, 2015. Annuaire Statistique de la Wilaya de Bejaia. http://www.univ-bejaia.dz/doc/Annuaire%20Statistique%202015 (accessed November 07, 2021).
• Awad, N.E., Seida, A.A., Shaffie, Z.E., El-Aziz, A.M., Awad, N.E., 2012. Hypoglycemic activity of Artemisia herba-alba (Asso.) used in Egyptian traditional medicine as hypoglycemic remedy. Journal of Applied Pharmaceutical Science, 2, 30-39.
• Ayaz, N.O., 2012. Antidiabetic and renoprotective effects of water extract of Rosmarinus officinalis in streptozotocin-induced diabetic rat. African Journal of Pharmacy and Pharmacology, 6(37), 2664-2669.
• Bailey, C.J., Day, C., 2004. Metformin: its botanical background. Practical Diabetes International, 21(3), 115-117.
• Bakırel, T., Bakırel, U., Keleş, O.Ü., Ülgen, S.G., Yardibi, H., 2008. In vivo assessment of antidiabetic and antioxidant activities of rosemary (Rosmarinus officinalis) in alloxan-diabetic rabbits. Journal of Ethnopharmacology, 116(1), 64-73.
• Belmouhoub, M., Bribi, N., Iguer-ouada, M., 2017. Alpha-glucosidase inhibition and antihyperglycemic activity of flavonoids rich fractions of Rosmarinus officinalis in normal and streptozotocin diabetic mice. Oriental Pharmacy and Experimental Medicine, 17(1), 29-39.
• Belmouhoub, M., Chebout, I., Iguer-Ouada, M., 2018. Antidiabetic and anti-hypercholesterolemic effects of flavonoid-rich fractions of Rosmarinus officinalis in streptozotocin-induced diabetes in mice. Phytotherapie, 16(4), 204-210.
• Bendif, H., Lazali, M., Harir, M., Miara, M.D., Boudjeniba, M., Venskutonis, P.R., 2017. Biological screening of Ajuga iva extracts obtained by supercritical carbon dioxide and pressurized liquid extraction. Journal of Medicinal Botany, 1, 33-41.
• Benhabyles, N., Arab, K., Bouchenak, O., Baz, A., 2015. Phytochemical screening, hypoglycemic and antihyperglycemic effect of flavonoids from the leaves of Algerian Olea europaea L. in normal and alloxan-induced diabetic rats. International Journal of Pharmacology, 11(5), 477-483.
• Boudjelal, A., Henchiri, C., Sari, M., Sarri, D., Hendel, N., Benkhaled, A., Ruberto, G., 2013. Herbalists and wild medicinal plants in M'Sila (North Algeria): An ethnopharmacology survey. Journal of Ethnopharmacology, 148(2), 395-402.
• Boudjelal, A., Siracusa, L., Henchiri, C., Sarri, M., Abderrahim, B., Baali, F., Ruberto, G., 2015. Antidiabetic effects of aqueous infusions of Artemisia herba-alba and Ajuga iva in alloxan-induced diabetic rats. Planta Medica, 81(09), 696-704.
• Bouyahya, A., Belmehdi, O., El Jemli, M., Marmouzi, I., Bourais, I., Abrini, J., Bakri, Y., 2019. Chemical variability of Centaurium erythraea essential oils at three developmental stages and investigation of their in vitro antioxidant, antidiabetic, dermatoprotective and antibacterial activities. Industrial Crops and Products, 132, 111-117.
• Büyükbalci, A., El, S.N., 2008. Determination of in vitro antidiabetic effects, antioxidant activities and phenol contents of some herbal teas. Plant Foods for Human Nutrition, 63(1), 27-33.
• Clewell, A.E., Béres, E., Vértesi, A., Glávits, R., Hirka, G., Endres, J.R., Szakonyiné, I.P., 2016. A comprehensive toxicological safety assessment of an extract of Olea europaea L. leaves (bonolive™). International Journal of Toxicology, 35(2), 208-221.
• Coman, C., Rugina, O.D., Socaciu, C., 2012. Plants and natural compounds with antidiabetic action. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 40(1), 314-325.
• Dastjerdi, Z.M., Namjoyan, F., Azemi, M.E., 2015. Alpha amylase inhibition activity of some plants extract of Teucrium species. European Journal of Biological Sciences, 7(1), 26-31.
• Đorđević, M., Grdović, N., Mihailović, M., Jovanović, J.A., Uskoković, A., Rajić, J., Dinić, S., 2019. Centaurium erythraea extract improves survival and functionality of pancreatic beta-cells in diabetes through multiple routes of action. Journal of Ethnopharmacology, 242, 112043.
• Eddouks, M., Ouahidi, M.L., Farid, O., Moufid, A., Khalidi, A., Lemhadri, A., 2007. L’utilisation des plantes médicinales dans le traitement du diabète au Maroc. Phytothérapie, 5(4), 194-203.
• El Hilaly, J., Israili, Z.H., Lyoussi, B., 2004. Acute and chronic toxicological studies of Ajuga iva in experimental animals. Journal of Ethnopharmacology, 91(1), 43-50.
• Esmaeili, M.A., Yazdanparast, R., 2004. Hypoglycaemic effect of Teucrium polium: studies with rat pancreatic islets. Journal of Ethnopharmacology, 95(1), 27-30.
• Esmaeili, M.A., Zohari, F., Sadeghi, H., 2009. Antioxidant and protective effects of major flavonoids from Teucrium polium on β-cell destruction in a model of streptozotocin-induced diabetes. Planta Medica, 75(13), 1418-1420.
• Fadili, K., Amalich, S., N’dedianhoua, S.K., Bouachrine, M., Mahjoubi, M., El Hilali, F., Zair, T., 2015. Polyphenols content and antioxidant activity of two species from Moroccan High Atlas: Rosmarinus officinalis and Thymus satureioides. International Journal of Innovation and Scientific Research, 4(17), 24-33.
• Fettach, S., Mrabti, H.N., Sayah, K., Bouyahya, A., Salhi, N., Cherrah, Y., El Abbes, F.M., 2019. Phenolic content, acute toxicity of Ajuga iva extracts and assessment of their antioxidant and carbohydrate digestive enzyme inhibitory effects. South African Journal of Botany, 125, 381-385.
• Ghasemi, T., Keshavarz, M., Parviz, M., 2019. Acute hepatorenal dose dependent toxicity of Teucrium polium hydro alcoholic extract in rat. International Journal of Pediatrics, 7(9), 10099-10107.
• Guex, C.G., Reginato, F.Z., de Jesus, P.R., Brondani, J.C., Lopes, G.H.H., de Freitas Bauermann, L., 2019. Antidiabetic effects of Olea europaea L. leaves in diabetic rats induced by high-fat diet and low-dose streptozotocin. Journal of Ethnopharmacology, 235, 1-7.
• Guex, C.G., Reginato, F.Z., Figueredo, K.C., da Silva, A.R.H., Pires, F.B., da Silva Jesus, R., de Freitas Bauermann, L., 2018. Safety assessment of ethanolic extract of Olea europaea L. leaves after acute and subacute administration to Wistar rats. Regulatory Toxicology and Pharmacology, 95, 395-399.
• Hsieh, C.W., Cheng, J.Y., Wang, T.H., Wang, H.J., Ho, W.J., 2014. Hypoglycaemic effects of Ajuga extract in vitro and in vivo. Journal of Functional Foods, 6, 224-230.
• Ibarra, A., Cases, J., Roller, M., Chiralt-Boix, A., Coussaert, A., Ripoll, C., 2011. Carnosic acid-rich rosemary (Rosmarinus officinalis L.) leaf extract limits weight gain and improves cholesterol levels and glycaemia in mice on a high-fat diet. British Journal of Nutrition, 106(8), 1182-1189.
• IDF, 2013. International Diabetes Federation. https://www.idf.org/ (accessed December 28, 2021).
• Iriadam, M., Musa, D., Gumushan, H., Baba, F., 2006. Effects of two Turkish medicinal plants Artemisia herba-alba and Teucrium polium on blood glucose levels and other biochemical parameters in rabbits. Journal of Molecular Cell Biology, 5(1), 19-24.
• Jamshidi-Kia, F., Lorigooini, Z., Amini-Khoei, H., 2018. Medicinal plants: Past history and future perspective. Journal of Herbmed Pharmacology, 7(1), 1-7.
• Jemai, H., El Feki, A., Sayadi, S., 2009. Antidiabetic and antioxidant effects of hydroxytyrosol and oleuropein from olive leaves in alloxan-diabetic rats. Journal of Agricultural and Food Chemistry, 57(19), 8798-8804.
• Kadan, S., Sasson, Y., Abu-Reziq, R., Saad, B., Benvalid, S., Linn, T., Zaid, H., 2018. Teucrium polium extracts stimulate GLUT4 translocation to the plasma membrane in L6 muscle cells. Advancement in Medicinal Plant Research, 6(1), 1-8.
• Khalil, O.A., Ramadan, K.S., Danial, E.N., Alnahdi, H.S., Ayaz, N.O., 2012. Antidiabetic activity of Rosmarinus officinalis and its relationship with the antioxidant property. African Journal of Pharmacy and Pharmacology, 6(14), 1031-1036.
• Khatteli, A., Benabderrahim, M.A., Triki, T., Guasmi, F., 2020. Aroma volatiles, phenolic profile and hypoglycaemic activity of Ajuga iva L. Food Bioscience, 36, 100578.
• Koga, K., Shibata, H., Yoshino, K., Nomoto, K., 2006. Effects of 50% Ethanol Extract from Rosemary (Rosmarinus officinalis) on α‐Glucosidase Inhibitory Activity and the Elevation of Plasma Glucose Level in Rats, and Its Active Compound. Journal of Food Science, 71(7), S507-S512.
• Komaki, E., Yamaguchi, S., Maru, I., Kinoshita, M., Kakehi, K., Ohta, Y., Tsukada, Y., 2003. Identification of anti-α-amylase components from olive leaf extracts. Food Science and Technology Research, 9(1), 35-39.
• Krache, I., Boussoualim, N., Ouhida, S., Amraoui, N., Baghiani, A., Arrar, L., 2017. Acute and chronic effects of methanolic extract of Teucrium polium on blood parameters and histopathology of liver and kidney in female rats. Asian Journal of Research in Medical and Pharmaceutical Sciences, 2, 1-11.
• Labban, L., Mustafa, U.E.S., Ibrahim, Y.M., 2014. The effects of rosemary (Rosmarinus officinalis) leaves powder on glucose level, lipid profile and lipid perodoxation. International Journal of Clinical Medicine, 2014.
• Lv, J., Cao, L., Li, M., Zhang, R., Bai, F., Wei, P., 2018. Effect of hydroalcohol extract of lemon (Citrus limon) peel on a rat model of type 2 diabetes. Tropical Journal of Pharmaceutical Research, 17(7), 1367-1372.
• Mahmoud, A.M., Ahmed, O.M., Ashour, M.B., Abdel-Moneim, A., 2015. In vivo and in vitro antidiabetic effects of citrus flavonoids; a study on the mechanism of action. International Journal of Diabetes in Developing Countries, 35(3), 250-263.
• Mansi, K., Amneh, M., Nasr, H., 2007. The hypolipidemic effects of Artemisia sieberi (A. herba-alba) in alloxan induced diabetic rats. International Journal of Pharmacology, 3(6), 487-491.
• Mirghazanfari, S.M., Keshavarz, M., Nabavizadeh, F., Soltani, N., Kamalinejad, M., 2010. The effect of “Teucrium polium L.” extracts on insulin release from in situ isolated perfused rat pancreas in a newly modified isolation method: the role of Ca2+ and K+ Channels. Iranian Biomedical Journal, 14(4), 178.
• Mushtaq, M.N., Bashir, S., Ullah, I., Karim, S., Rashid, M., Hayat Malik, M.N., 2016. Comparative hypoglycemic activity of different fractions of Thymus serpyllum L. in alloxan induced diabetic rabbits. Pakistan Journal of Pharmaceutical Sciences, 29(5), 1483–1488.
• Punithavathi, V.R., Anuthama, R., Prince, P.S.M., 2008. Combined treatment with naringin and vitamin C ameliorates streptozotocin‐induced diabetes in male Wistar rats. Journal of Applied Toxicology: An International Journal, 28(6), 806-813.
• Quezel, P., Santa, S., Schotter, O., 1962. Nouvelle flore de l'Algerie et des regions desertiques meridionales. Volume 2. Editions du Centre National de la Recherche Scientifique, Paris.
• Rachid, A., Rabah, D., Farid, L., Zohra, S.F., Houcine, B., Nacéra, B., 2012) Ethnopharmacological survey of medicinal plants used in the traditional treatment of diabetes mellitus in the North Western and South Western Algeria. Journal of Medicinal Plants Research, 6(10), 2041-2050.
• Sato, H., Genet, C., Strehle, A., Thomas, C., Lobstein, A., Wagner, A., Saladin, R., 2007. Anti-hyperglycemic activity of a TGR5 agonist isolated from Olea europaea. Biochemical and Biophysical Research Communications, 362(4), 793-798.
• Senouci, F., Ababou, A., Chouieb, M., 2019. Ethnobotanical survey of the medicinal plants used in the Southern Mediterranean. Case study: the region of Bissa (Northeastern Dahra Mountains, Algeria). Pharmacognosy Journal, 11(4), 647-659.
• Skouri, M., 1994. Les ressources physiques de la région méditerranéenne, In: Dupuy, B. (Ed.) Equilibre alimentaire, agriculture et environnement en Méditerranée. Ciheam, Montpellier, pp. 15–30.
• Stefkov, G., Kulevanova, S., Miova, B., Dinevska-Kjovkarovska, S., Mølgaard, P., Jäger, A. K., Josefsen, K., 2011. Effects of Teucrium polium spp. capitatum flavonoids on the lipid and carbohydrate metabolism in rats. Pharmaceutical Biology, 49(9), 885-892.
• Stefkov, G., Miova, B., Dinevska-Kjovkarovska, S., Stanoeva, J.P., Stefova, M., Petrusevska, G., Kulevanova, S., 2014. Chemical characterization of Centaurium erythrea L. and its effects on carbohydrate and lipid metabolism in experimental diabetes. Journal of Ethnopharmacology, 152(1), 71-77.
• Tafesse, T.B., Hymete, A., Mekonnen, Y., Tadesse, M., 2017. Antidiabetic activity and phytochemical screening of extracts of the leaves of Ajuga remota Benth on alloxan-induced diabetic mice. BMC Complementary and Alternative Medicine, 17(1), 1-9.
• Tardío, J., Pardo-de-Santayana, M., 2008. Cultural importance indices: a comparative analysis based on the useful wild plants of Southern Cantabria (Northern Spain) 1. Economic Botany, 62(1), 24-39.
• Taştekin, D., Atasever, M., Adigüzel, G., Keleş, M., Taştekin, A., 2006. Hypoglycaemic effect of Artemisia herba-alba in experimental hyperglycaemic rats. Bulletin of the Veterinary Institute in Pulawy, 50, 235-238.
• Telli, A., Esnault, M.A., Khelil, A.O.E.H., 2016. An ethnopharmacological survey of plants used in traditional diabetes treatment in south-eastern Algeria (Ouargla province). Journal of Arid Environments, 127, 82-92.
• Tu, Z., Moss-Pierce, T., Ford, P., Jiang, T.A., 2013. Rosemary (Rosmarinus officinalis L.) extract regulates glucose and lipid metabolism by activating AMPK and PPAR pathways in HepG2 cells. Journal of Agricultural and Food Chemistry, 61(11), 2803-2810.
• Vlad, I., Popa, A.R., 2012. Epidemiology of diabetes mellitus: a current review. Romanian Journal of Diabetes Nutrition and Metabolic Diseases, 19, 433–440.
• Wainstein, J., Ganz, T., Boaz, M., Bar Dayan, Y., Dolev, E., Kerem, Z., Madar, Z., 2012. Olive leaf extract as a hypoglycemic agent in both human diabetic subjects and in rats. Journal of Medicinal Food, 15(7), 605-610.
• Wang, J.J., Jin, H., Zheng, S.L., Xia, P., Cai, Y., Ni, X.J., 2017. Phytoecdysteroids from Ajuga iva act as potential antidiabetic agent against alloxan-induced diabetic male albino rats. Biomedicine & Pharmacotherapy, 96, 480-488.
• Whiting, D.R., Guariguata, L., Weil, C., Shaw, J., 2011. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Research and Clinical Practice, 94(3), 311-321.
• WHO, 2016. World Health Organization. Global Report on Diabetes. Geneva. http://apps.who.int/iris/bitstream/10665/204871/1/9789241565257_eng.pdf. (accessed October 12, 2021).
• Zhang, Y., Wu, L., Ma, Z., Cheng, J., Liu, J., 2016. Anti-diabetic, anti-oxidant and anti-hyperlipidemic activities of flavonoids from corn silk on STZ-induced diabetic mice. Molecules, 21(1), E7.
• Zygmunt, K., Faubert, B., MacNeil, J., Tsiani, E., 2010. Naringenin, a citrus flavonoid, increases muscle cell glucose uptake via AMPK. Biochemical and Biophysical Research Communications, 398(2), 178-183.