Effect of oral administration of chia (Salvia hispanica L.) seed extract on wound healing property in diabetic mice
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Published:
May 20, 2020
Keywords:
chia seed, diabetic wound, oral administration, Salvia hispanica L.
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Abstract
Chia, Salvia hispanica L., a plant containing lipid-antioxidant, has been shown to be beneficial for prevention of risk factors of type 2 diabetes. The objectives of this study were to evaluate oral chia seed extract on wound healing properties including wound contraction and histopathological examination in a diabetic wound model. C57BL/6J mice were fed with standard and high-fat diet for 27 weeks resulting in non-diabetic and diabetic mice respectively, then divided into 4 groups (n=6) as follows: normal control group, fed with standard diet; 4% chia seed extract group, fed with chia seed extract diet; glipizide group, fed with high-fat diet and glipizide; diabetic group; only fed with high-fat diet. The percentage of wound contraction, histopathological score and morphology were compared for evaluating wound healing properties. On day 12 post-wounding, a significant increase in the percentage of wound healing was found in the normal control, 4% chia seed extract and glipizide group as compared to diabetic group (p < 0.05, 99.45 ± 0.865, 98.99 ± 1.948, 99.06 ± 0.779 vs. 81.41 ± 10.759). Histopathological scores of normal control, 4% chia seed extract and Glipizide showed better healing than in the diabetic group (p < 0.05, 10.50 ± 0.837, 10.00 ± 0.632, 9.92 ± 1.625 vs. 3.83 ± 1.169). The results of histopathological morphology showed consistent results with histopathological scores, in which collagen, fibroblast, epithelialization and neovascularization were dominant in granulation tissue of better scores. It may be concluded that chia seed extract was better for diabetic wound healing in mice.
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Pintapagung, T., Asawapattanakul, T. ., Buasrithong, . N. ., Phunnanon, M. ., & Thaingkhan, W. . (2020). Effect of oral administration of chia (Salvia hispanica L.) seed extract on wound healing property in diabetic mice . Veterinary Integrative Sciences, 18(3), 153–171. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/241151
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References
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Ayerza R., Coates W., 2007. Metabolism. Effect of dietary α-linolenic fatty acid derived from chia when fed as ground seed, whole seed and oil on lipid content and fatty acid composition of rat plasma. Ann. Nutr. Metab. 51(1), 27-34.
Boulton A.J., Vileikyte L., Ragnarson-Tennvall G., Apelqvist J., 2005. The global burden of diabetic foot disease. Lancet 366(9498), 1719-1724.
Brem H., Tomic-Canic M.,2007. Cellular and molecular basis of wound healing in diabetes. J. Clin. Invest. 117(5), 1219-1222.
Bushway A.A., Belyea P.R., Bushway R.J., 1981. Chia seed as a source of oil, polysaccharide, and protein. J. food Sci. 46(5), 1349-1350.
Cefalu W.T., 2006. Animal models of type 2 diabetes: clinical presentation and pathophysiological relevance to the human condition. ILAR J. 47(3), 186-198.
Chicco A.G., D'Alessandro M.E., Hein G.J., Oliva M.E., Lombardo Y.B., 2008. Dietary chia seed (Salvia hispanica L.) rich in α-linolenic acid improves adiposity and normalises hypertriacylglycerolaemia and insulin resistance in dyslipaemic rats. Br. J. Nutr. 101(1), 41-50.
Collins S., Martin T.L., Surwit R.S., Robidoux J., 2004. Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol. Behav. 81(2), 243-248.
Dinh T., Veves A., 2005. Microcirculation of the diabetic foot. Curr. Pharm. Des. 11(18), 2301-2309.
Falanga V., 2005. Wound healing and its impairment in the diabetic foot. Lancet 366(9498), 1736-1743.
Ganz M., Bukong T.N., Csak T., Saha B., Park J.K., Ambade A., Kodys K., Szabo G., 2015. Progression of non-alcoholic steatosis to steatohepatitis and fibrosis parallels cumulative accumulation of danger signals that promote inflammation and liver tumors in a high fat–cholesterol–sugar diet model in mice. J. Transl. Med. 13, 193.
Gibran N.S., Jang Y.C., Isik F.F., Greenhalgh D.G., Muffley L.A., Underwood R.A., Usui M.L., Larsen J., Smith D.G., Bunnett N., Ansel J.C., Olerud J.E., 2002. Diminished neuropeptide levels contribute to the impaired cutaneous healing response associated with diabetes mellitus. J. Surg. Res. 108(1), 122-128.
Greenhalgh D.G., Sprugel K.H., Murray M.J., Ross R., 1990. PDGF and FGF stimulate wound healing in the genetically diabetic mouse. Am. J. Pathol. 136(6), 1235-1246.
Guevara-Cruz M., Tovar A.R., Aguilar-Salinas C.A., Medina-Vera I., Gil-Zenteno L., Hernández-Viveros I., Lopez-Romero P., Ordaz-Nava G., Canizales-Quinteros S., Guillen Pineda L.E., Torres N., 2011. A dietary pattern including nopal, chia seed, soy protein, and oat reduces serum triglycerides and glucose intolerance in patients with metabolic syndrome. J. Nutr. 142(1), 64-69.
Jeffcoate W.J., Harding K.G., 2003. Diabetic foot ulcers. Lancet 361(9368), 1545-1551.
Jeong S.K., Park H.J., Park B.D., Kim I.H., 2010. Effectiveness of topical chia seed oil on pruritus of end-stage renal disease (ESRD) patients and healthy volunteers. Ann. Dermatol. 22(2), 143-148.
Kim K., Kim H., Kwon J., Lee S., Kong H., Im S.A., Lee Y.H., Lee Y.R., Oh S.T., Jo T.H., Park Y.I., Lee C.K., Kim K., 2009. Hypoglycemic and hypolipidemic effects of processed Aloe vera gel in a mouse model of non-insulin-dependent diabetes mellitus. Phytomedicine 16(9), 856-863.
Kobus-Cisowska J., Szymanowska D., Maciejewska P., Kmiecik D., Gramza-Michałowska A., Kulczyński B., Cielecka-Piontek J., 2019. In vitro screening for acetylcholinesterase and butyrylcholinesterase inhibition and antimicrobial activity of chia seeds (Salvia hispanica). Electron. J. Biotechn. 37, 1-10.
Koca U., Süntar I.P., Keles H., Yesilada E., Akkol E.K., 2009. In vivo anti-inflammatory and wound healing activities of Centaurea iberica Trev. ex Spreng. J. Ethnopharmacol. 126(3), 551-556.
Koya D., Hayashi K., Kitada M., Kashiwagi A., Kikkawa R., Haneda M., 2003. Effects of antioxidants in diabetes-induced oxidative stress in the glomeruli of diabetic rats. J. Am. Soc. Nephrol. 14 suppl. 3, 250-253.
Li E., Nakata M., Shinozaki A., Yang Y., Zhang B., Yada T., 2016. Betatrophin expression is promoted in obese hyperinsulinemic type 2 but not type 1 diabetic mice. Endocr. J. 63(7), 611-619.
Loots M.A., Kenter S.B., Au F.L., Van Galen W.J.M., Middelkoop E., Bos J.D., Mekkes J.R., 2002. Fibroblasts derived from chronic diabetic ulcers differ in their response to stimulation with EGF, IGF-I, bFGF and PDGF-AB compared to controls. Eur. J. Cell Biol. 81(3), 153-160.
Marineli, R.D.S., Moraes, É.A., Lenquiste, S.A., Godoy, A.T., Eberlin, M.N., Maróstica Jr, M.R., 2015. Chemical characterization and antioxidant potential of Chilean chia seeds and oil (Salvia hispanica L.). LWT-Food Sci. Technol.59, 1304-1310.
Messier C., Whately K., Liang J., Du L., Puissant D., 2007. The effects of a high-fat, high-fructose, and combination diet on learning, weight, and glucose regulation in C57BL/6 mice. Behav. Brain Res. 178(1), 139-145.
Mogensen C.E., Christensen C.K., Vittinghus E., 1983. The stages in diabetic renal disease: with emphasis on the stage of incipient diabetic nephropathy. Diabetes 32 Suppl. 2, 64-78.
Mohd Ali N., Yeap S.K., Ho W.Y., Beh B.K., Tan S.W., Tan S.G., 2012. The promising future of chia, Salvia hispanica L. J. Biomed. Biotechnol. doi: 10.115/2012/171956.
Orona-Tamayo D., Valverde M.E., Paredes-López O., 2019. Bioactive peptides from selected Latin American food crops–A nutraceutical and molecular approach. Crit. Rev. Food Sci. Nutr. 59(12), 1949-1975.
Oza M.J., Kulkarni Y.A., 2018. Formononetin treatment in type 2 diabetic rats reduces insulin resistance and hyperglycemia. Front. Pharmacol. doi: 10.3389/fphar.2018.00739.
Pence B.D., Woods J.A., 2014. Exercise, Obesity, and Cutaneous Wound Healing: Evidence from Rodent and Human Studies. Adv. Wound Care. 3(1), 71-79.
Prior R.L., Wu X., Schaich K., 2005. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J. Agric. Food Chem. 53(10), 4290-4302.
Purves R.D., 1992. Optimum numerical integration methods for estimation of area-under-the-curve (AUC) and area-under-the-momentcurve (AUMC). J. Pharmacokinet. Biopharm. 20, 211 -227.
Rodrigues H.G., Vinolo M.A.R., Magdalon J., Vitzel K., Nachbar R.T., Pessoa A.F.M., dos Santos M.F., Hatanaka E., Calder P.C., Curi R., 2012. Oral administration of oleic or linoleic acid accelerates the inflammatory phase of wound healing. J. Investig. Dermatol. 132, 208-215.
Scapin G., Schmidt M.M., Prestes R.C., Rosa C.S., 2016. Phenolics compounds, flavonoids and antioxidant activity of chia seed extracts (Salvia hispanica) obtained by different extraction conditions. Int. Food Res. J. 23(6), 2341-2346.
Signorelli S.S., Malaponte G., Libra M., Pino L.D., Celotta G., Bevelacqua V., Petrina M., Nicotra G.S., Indelicato M., Navolanic P.M., Pennisi G., Mazzarino M.C., 2005. Plasma levels and zymographic activities of matrix metalloproteinases 2 and 9 in type II diabetics with peripheral arterial disease. Vasc. Med. 10(1), 1-6.
Singleton V.L., Rossi J.A., 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16(3), 144-158.
Stamenkovic I.,2003. Extracellular matrix remodelling: the role of matrix metalloproteinases. J. Pathol. 200(4), 448-464.
Surwit R.S., Kuhn C.M., Cochrane C., McCubbin J.A., Feinglos M.N., 1988. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37(9), 1163-1167.
Thaipong K., Boonprakob U., Crosby K., Cisneros-Zevallos L., Byrne D.H., 2006. Comparison of ABTS, DPPH, FRAP, and ORAC assays for estimating antioxidant activity from guava fruit extracts. J. Food Compost. Anal. 19(6-7), 669–675.
Toscano L.T., da Silva C.S.O, Toscano L.T., de Almeida A.E.M., da Cruz Santos A., Silva A.S., 2014. Chia Flour Supplementation reduces blood pressure in hypertensive subjects. Plant Foods Hum. Nutr. 69(4), 392-398.
Toscano L.T., Toscano L.T., Tavares R.L., da Silva C.S.O., Silva A.S., 2015. Chia induces clinically discrete weight loss and improves lipid profile only in altered previous values. Nutr. Hosp. 31(3), 1176-1182.
Vuksan V., Jenkins A.L., Brissette C., Choleva L., Jovanovski E., Gibbs A.L., Bazinet R.P., Au-Yeung F., Zurbau A., Ho H.V.T., Duvnjak L., Sievenpiper J.L., Josse R.G., Hanna A., 2017. Salba-chia (Salvia hispanica L.) in the treatment of overweight and obese patients with type 2 diabetes: A double-blind randomized controlled trial. Nutr. Metab. Cardiovasc. Dis. 27(2), 138-146.
Vuksan V., Jenkins A.L., Dias A.G., Lee A.S., Jovanoski E., Rogovik A.L., Hanna A., 2010. Reduction in postprandial glucose excursion and prolongation of satiety: possible explanation of the long-term effects of whole grain Salba (Salvia Hispanica L.). Eur. J. Clin. Nutr. 64, 436-438.
Wang Q., Brubaker P.L., 2002. Glucagon-like peptide-1 treatment delays the onset of diabetes in 8 week-old db/db mice. Diabetologia 45(9), 1263-1273.
Whiting, D.R., Guariguata L., Weil C., 2011. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res. Clin. Pract. 94(3), 311-321.
Yagihashi S., Yamagishi S., Wada R., 2007. Pathology and pathogenetic mechanisms of diabetic neuropathy: correlation with clinical signs and symptoms. Diabetes Res. Clin. Pract. 77 Suppl. 1, 184-189.
Zykova S.N., Jenssen T.G., Berdal M., Olsen R., Myklebust R., Seljelid R., 2000. Altered cytokine and nitric oxide secretion in vitro by macrophages from diabetic type II-like db/db mice. Diabetes 49(9), 1451-1458.
Ayerza R., 1995. Oil content and fatty acid composition of chia (Salvia hispanica L.) from five northwestern locations in Argentina. J. Am. Oil Chem. Soc. 72, 1079-1081.
Ayerza R., Coates W., 2007. Metabolism. Effect of dietary α-linolenic fatty acid derived from chia when fed as ground seed, whole seed and oil on lipid content and fatty acid composition of rat plasma. Ann. Nutr. Metab. 51(1), 27-34.
Boulton A.J., Vileikyte L., Ragnarson-Tennvall G., Apelqvist J., 2005. The global burden of diabetic foot disease. Lancet 366(9498), 1719-1724.
Brem H., Tomic-Canic M.,2007. Cellular and molecular basis of wound healing in diabetes. J. Clin. Invest. 117(5), 1219-1222.
Bushway A.A., Belyea P.R., Bushway R.J., 1981. Chia seed as a source of oil, polysaccharide, and protein. J. food Sci. 46(5), 1349-1350.
Cefalu W.T., 2006. Animal models of type 2 diabetes: clinical presentation and pathophysiological relevance to the human condition. ILAR J. 47(3), 186-198.
Chicco A.G., D'Alessandro M.E., Hein G.J., Oliva M.E., Lombardo Y.B., 2008. Dietary chia seed (Salvia hispanica L.) rich in α-linolenic acid improves adiposity and normalises hypertriacylglycerolaemia and insulin resistance in dyslipaemic rats. Br. J. Nutr. 101(1), 41-50.
Collins S., Martin T.L., Surwit R.S., Robidoux J., 2004. Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol. Behav. 81(2), 243-248.
Dinh T., Veves A., 2005. Microcirculation of the diabetic foot. Curr. Pharm. Des. 11(18), 2301-2309.
Falanga V., 2005. Wound healing and its impairment in the diabetic foot. Lancet 366(9498), 1736-1743.
Ganz M., Bukong T.N., Csak T., Saha B., Park J.K., Ambade A., Kodys K., Szabo G., 2015. Progression of non-alcoholic steatosis to steatohepatitis and fibrosis parallels cumulative accumulation of danger signals that promote inflammation and liver tumors in a high fat–cholesterol–sugar diet model in mice. J. Transl. Med. 13, 193.
Gibran N.S., Jang Y.C., Isik F.F., Greenhalgh D.G., Muffley L.A., Underwood R.A., Usui M.L., Larsen J., Smith D.G., Bunnett N., Ansel J.C., Olerud J.E., 2002. Diminished neuropeptide levels contribute to the impaired cutaneous healing response associated with diabetes mellitus. J. Surg. Res. 108(1), 122-128.
Greenhalgh D.G., Sprugel K.H., Murray M.J., Ross R., 1990. PDGF and FGF stimulate wound healing in the genetically diabetic mouse. Am. J. Pathol. 136(6), 1235-1246.
Guevara-Cruz M., Tovar A.R., Aguilar-Salinas C.A., Medina-Vera I., Gil-Zenteno L., Hernández-Viveros I., Lopez-Romero P., Ordaz-Nava G., Canizales-Quinteros S., Guillen Pineda L.E., Torres N., 2011. A dietary pattern including nopal, chia seed, soy protein, and oat reduces serum triglycerides and glucose intolerance in patients with metabolic syndrome. J. Nutr. 142(1), 64-69.
Jeffcoate W.J., Harding K.G., 2003. Diabetic foot ulcers. Lancet 361(9368), 1545-1551.
Jeong S.K., Park H.J., Park B.D., Kim I.H., 2010. Effectiveness of topical chia seed oil on pruritus of end-stage renal disease (ESRD) patients and healthy volunteers. Ann. Dermatol. 22(2), 143-148.
Kim K., Kim H., Kwon J., Lee S., Kong H., Im S.A., Lee Y.H., Lee Y.R., Oh S.T., Jo T.H., Park Y.I., Lee C.K., Kim K., 2009. Hypoglycemic and hypolipidemic effects of processed Aloe vera gel in a mouse model of non-insulin-dependent diabetes mellitus. Phytomedicine 16(9), 856-863.
Kobus-Cisowska J., Szymanowska D., Maciejewska P., Kmiecik D., Gramza-Michałowska A., Kulczyński B., Cielecka-Piontek J., 2019. In vitro screening for acetylcholinesterase and butyrylcholinesterase inhibition and antimicrobial activity of chia seeds (Salvia hispanica). Electron. J. Biotechn. 37, 1-10.
Koca U., Süntar I.P., Keles H., Yesilada E., Akkol E.K., 2009. In vivo anti-inflammatory and wound healing activities of Centaurea iberica Trev. ex Spreng. J. Ethnopharmacol. 126(3), 551-556.
Koya D., Hayashi K., Kitada M., Kashiwagi A., Kikkawa R., Haneda M., 2003. Effects of antioxidants in diabetes-induced oxidative stress in the glomeruli of diabetic rats. J. Am. Soc. Nephrol. 14 suppl. 3, 250-253.
Li E., Nakata M., Shinozaki A., Yang Y., Zhang B., Yada T., 2016. Betatrophin expression is promoted in obese hyperinsulinemic type 2 but not type 1 diabetic mice. Endocr. J. 63(7), 611-619.
Loots M.A., Kenter S.B., Au F.L., Van Galen W.J.M., Middelkoop E., Bos J.D., Mekkes J.R., 2002. Fibroblasts derived from chronic diabetic ulcers differ in their response to stimulation with EGF, IGF-I, bFGF and PDGF-AB compared to controls. Eur. J. Cell Biol. 81(3), 153-160.
Marineli, R.D.S., Moraes, É.A., Lenquiste, S.A., Godoy, A.T., Eberlin, M.N., Maróstica Jr, M.R., 2015. Chemical characterization and antioxidant potential of Chilean chia seeds and oil (Salvia hispanica L.). LWT-Food Sci. Technol.59, 1304-1310.
Messier C., Whately K., Liang J., Du L., Puissant D., 2007. The effects of a high-fat, high-fructose, and combination diet on learning, weight, and glucose regulation in C57BL/6 mice. Behav. Brain Res. 178(1), 139-145.
Mogensen C.E., Christensen C.K., Vittinghus E., 1983. The stages in diabetic renal disease: with emphasis on the stage of incipient diabetic nephropathy. Diabetes 32 Suppl. 2, 64-78.
Mohd Ali N., Yeap S.K., Ho W.Y., Beh B.K., Tan S.W., Tan S.G., 2012. The promising future of chia, Salvia hispanica L. J. Biomed. Biotechnol. doi: 10.115/2012/171956.
Orona-Tamayo D., Valverde M.E., Paredes-López O., 2019. Bioactive peptides from selected Latin American food crops–A nutraceutical and molecular approach. Crit. Rev. Food Sci. Nutr. 59(12), 1949-1975.
Oza M.J., Kulkarni Y.A., 2018. Formononetin treatment in type 2 diabetic rats reduces insulin resistance and hyperglycemia. Front. Pharmacol. doi: 10.3389/fphar.2018.00739.
Pence B.D., Woods J.A., 2014. Exercise, Obesity, and Cutaneous Wound Healing: Evidence from Rodent and Human Studies. Adv. Wound Care. 3(1), 71-79.
Prior R.L., Wu X., Schaich K., 2005. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J. Agric. Food Chem. 53(10), 4290-4302.
Purves R.D., 1992. Optimum numerical integration methods for estimation of area-under-the-curve (AUC) and area-under-the-momentcurve (AUMC). J. Pharmacokinet. Biopharm. 20, 211 -227.
Rodrigues H.G., Vinolo M.A.R., Magdalon J., Vitzel K., Nachbar R.T., Pessoa A.F.M., dos Santos M.F., Hatanaka E., Calder P.C., Curi R., 2012. Oral administration of oleic or linoleic acid accelerates the inflammatory phase of wound healing. J. Investig. Dermatol. 132, 208-215.
Scapin G., Schmidt M.M., Prestes R.C., Rosa C.S., 2016. Phenolics compounds, flavonoids and antioxidant activity of chia seed extracts (Salvia hispanica) obtained by different extraction conditions. Int. Food Res. J. 23(6), 2341-2346.
Signorelli S.S., Malaponte G., Libra M., Pino L.D., Celotta G., Bevelacqua V., Petrina M., Nicotra G.S., Indelicato M., Navolanic P.M., Pennisi G., Mazzarino M.C., 2005. Plasma levels and zymographic activities of matrix metalloproteinases 2 and 9 in type II diabetics with peripheral arterial disease. Vasc. Med. 10(1), 1-6.
Singleton V.L., Rossi J.A., 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16(3), 144-158.
Stamenkovic I.,2003. Extracellular matrix remodelling: the role of matrix metalloproteinases. J. Pathol. 200(4), 448-464.
Surwit R.S., Kuhn C.M., Cochrane C., McCubbin J.A., Feinglos M.N., 1988. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37(9), 1163-1167.
Thaipong K., Boonprakob U., Crosby K., Cisneros-Zevallos L., Byrne D.H., 2006. Comparison of ABTS, DPPH, FRAP, and ORAC assays for estimating antioxidant activity from guava fruit extracts. J. Food Compost. Anal. 19(6-7), 669–675.
Toscano L.T., da Silva C.S.O, Toscano L.T., de Almeida A.E.M., da Cruz Santos A., Silva A.S., 2014. Chia Flour Supplementation reduces blood pressure in hypertensive subjects. Plant Foods Hum. Nutr. 69(4), 392-398.
Toscano L.T., Toscano L.T., Tavares R.L., da Silva C.S.O., Silva A.S., 2015. Chia induces clinically discrete weight loss and improves lipid profile only in altered previous values. Nutr. Hosp. 31(3), 1176-1182.
Vuksan V., Jenkins A.L., Brissette C., Choleva L., Jovanovski E., Gibbs A.L., Bazinet R.P., Au-Yeung F., Zurbau A., Ho H.V.T., Duvnjak L., Sievenpiper J.L., Josse R.G., Hanna A., 2017. Salba-chia (Salvia hispanica L.) in the treatment of overweight and obese patients with type 2 diabetes: A double-blind randomized controlled trial. Nutr. Metab. Cardiovasc. Dis. 27(2), 138-146.
Vuksan V., Jenkins A.L., Dias A.G., Lee A.S., Jovanoski E., Rogovik A.L., Hanna A., 2010. Reduction in postprandial glucose excursion and prolongation of satiety: possible explanation of the long-term effects of whole grain Salba (Salvia Hispanica L.). Eur. J. Clin. Nutr. 64, 436-438.
Wang Q., Brubaker P.L., 2002. Glucagon-like peptide-1 treatment delays the onset of diabetes in 8 week-old db/db mice. Diabetologia 45(9), 1263-1273.
Whiting, D.R., Guariguata L., Weil C., 2011. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res. Clin. Pract. 94(3), 311-321.
Yagihashi S., Yamagishi S., Wada R., 2007. Pathology and pathogenetic mechanisms of diabetic neuropathy: correlation with clinical signs and symptoms. Diabetes Res. Clin. Pract. 77 Suppl. 1, 184-189.
Zykova S.N., Jenssen T.G., Berdal M., Olsen R., Myklebust R., Seljelid R., 2000. Altered cytokine and nitric oxide secretion in vitro by macrophages from diabetic type II-like db/db mice. Diabetes 49(9), 1451-1458.