Skip to main content
Top
Published in: BMC Endocrine Disorders 1/2019

Open Access 01-12-2019 | Insulins | Research article

Association between plasma adipsin level and mild cognitive impairment in Chinese patients with type 2 diabetes: a cross-sectional study

Authors: Dan Guo, Yang Yuan, Rong Huang, Sai Tian, Jiaqi Wang, Hongyan Lin, Ke An, Jin Han, Shaohua Wang

Published in: BMC Endocrine Disorders | Issue 1/2019

Login to get access

Abstract

Background

The adipokine adipsin contributes to insulin resistance (IR), inflammation, and obesity, which are all regarded as high-risk factors for mild cognitive impairment (MCI) in patients with type 2 diabetes mellitus. This research aimed to uncover the role of adipsin in Chinese type 2 diabetes mellitus (T2DM) population with early cognitive dysfunction and determine whether adipsin contributes to diabetic MCI caused by IR.

Methods

In our study, 126 patients with T2DM were enrolled. The Montreal Cognitive Assessment (MoCA) was used to assess cognitive impairment. Demographic data and neuropsychological test results were evaluated. Plasma adipsin level was measured by enzyme-linked immunosorbent assay.

Results

The MCI group (n = 57) presented higher plasma adipsin levels compared with the healthy controls (p = 0.018). After adjustment for educational attainment, and age, begative correlations were found between plasma adipsin levels and MoCA, Mini Mental State Exam, and Verbal Fluency Test scores(r = − 0.640, p < 0.001; r = − 0.612, p < 0.001; r = − 0.288, p = 0.035; respectively). Correlation analysis demonstrated that adipsin levels were significantly positively correlated with fasting C-peptide; homeostasis model of assessment for insulin resistance (HOMA-IR) (r = 0.368, p < 0.001; r = 0.494, p < 0.001; respectively). Multivariable regression analysis further indicated that high plasma adipsin level was a significant independent determinant of MCI in the Chinese population withT2DM (p = 0.017).

Conclusions

Elevated plasma adipsin level was associated with MCI in Chinese T2DM patients. Further large-scale studies should be designed to determine whether adipsin is linked to IR-associated susceptibility to early cognitive decline in T2DM patients.
Literature
1.
go back to reference Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94(3):311–21.PubMedCrossRef Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94(3):311–21.PubMedCrossRef
2.
go back to reference van Harten B, de Leeuw FE, Weinstein HC, Scheltens P, Biessels GJ. Brain imaging in patients with diabetes: a systematic review. Diabetes Care. 2006;29(11):2539–48.PubMedCrossRef van Harten B, de Leeuw FE, Weinstein HC, Scheltens P, Biessels GJ. Brain imaging in patients with diabetes: a systematic review. Diabetes Care. 2006;29(11):2539–48.PubMedCrossRef
3.
go back to reference Mariani E, Monastero R, Mecocci P. Mild cognitive impairment: a systematic review. J Alzheimers Dis. 2007;12(1):23–35.PubMedCrossRef Mariani E, Monastero R, Mecocci P. Mild cognitive impairment: a systematic review. J Alzheimers Dis. 2007;12(1):23–35.PubMedCrossRef
4.
go back to reference Li W, Huang E. An update on type 2 diabetes mellitus as a risk factor for dementia. J Alzheimers Dis. 2016;53(2):393–402.PubMedCrossRef Li W, Huang E. An update on type 2 diabetes mellitus as a risk factor for dementia. J Alzheimers Dis. 2016;53(2):393–402.PubMedCrossRef
5.
go back to reference Kimm H, Lee PH, Shin YJ, Park KS, Jo J, Lee Y, Kang HC, Jee SH. Mid-life and late-life vascular risk factors and dementia in Korean men and women. Arch Gerontol Geriatr. 2011;52(3):e117–22.PubMedCrossRef Kimm H, Lee PH, Shin YJ, Park KS, Jo J, Lee Y, Kang HC, Jee SH. Mid-life and late-life vascular risk factors and dementia in Korean men and women. Arch Gerontol Geriatr. 2011;52(3):e117–22.PubMedCrossRef
6.
go back to reference De Felice FG, Ferreira ST. Inflammation, defective insulin signaling, and mitochondrial dysfunction as common molecular denominators connecting type 2 diabetes to Alzheimer disease. Diabetes. 2014;63(7):2262–72.CrossRefPubMed De Felice FG, Ferreira ST. Inflammation, defective insulin signaling, and mitochondrial dysfunction as common molecular denominators connecting type 2 diabetes to Alzheimer disease. Diabetes. 2014;63(7):2262–72.CrossRefPubMed
7.
go back to reference Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol. 2004;24(5):816–23.PubMedCrossRef Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol. 2004;24(5):816–23.PubMedCrossRef
8.
go back to reference Kahn SE. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of type 2 diabetes. Diabetologia. 2003;46(1):3–19.CrossRefPubMed Kahn SE. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of type 2 diabetes. Diabetologia. 2003;46(1):3–19.CrossRefPubMed
9.
go back to reference Umegaki H, Makino T, Uemura K, Shimada H, Hayashi T, Cheng XW, Kuzuya M. The associations among insulin resistance, hyperglycemia, physical performance, diabetes mellitus, and cognitive function in relatively healthy older adults with subtle cognitive dysfunction. Front Aging Neurosci. 2017;9:72.PubMedPubMedCentralCrossRef Umegaki H, Makino T, Uemura K, Shimada H, Hayashi T, Cheng XW, Kuzuya M. The associations among insulin resistance, hyperglycemia, physical performance, diabetes mellitus, and cognitive function in relatively healthy older adults with subtle cognitive dysfunction. Front Aging Neurosci. 2017;9:72.PubMedPubMedCentralCrossRef
10.
go back to reference Baker LD, Cross DJ, Minoshima S, Belongia D, Watson GS, Craft S. Insulin resistance and Alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early type 2 diabetes. Arch Neurol. 2011;68(1):51–7.PubMedCrossRef Baker LD, Cross DJ, Minoshima S, Belongia D, Watson GS, Craft S. Insulin resistance and Alzheimer-like reductions in regional cerebral glucose metabolism for cognitively normal adults with prediabetes or early type 2 diabetes. Arch Neurol. 2011;68(1):51–7.PubMedCrossRef
11.
go back to reference Talbot K, Wang HY, Kazi H, Han LY, Bakshi KP, Stucky A, Fuino RL, Kawaguchi KR, Samoyedny AJ, Wilson RS, et al. Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest. 2012;122(4):1316–38.PubMedPubMedCentralCrossRef Talbot K, Wang HY, Kazi H, Han LY, Bakshi KP, Stucky A, Fuino RL, Kawaguchi KR, Samoyedny AJ, Wilson RS, et al. Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline. J Clin Invest. 2012;122(4):1316–38.PubMedPubMedCentralCrossRef
12.
go back to reference Berglund ED, Vianna CR, Donato J Jr, Kim MH, Chuang JC, Lee CE, Lauzon DA, Lin P, Brule LJ, Scott MM, et al. Direct leptin action on POMC neurons regulates glucose homeostasis and hepatic insulin sensitivity in mice. J Clin Invest. 2012;122(3):1000–9.PubMedPubMedCentralCrossRef Berglund ED, Vianna CR, Donato J Jr, Kim MH, Chuang JC, Lee CE, Lauzon DA, Lin P, Brule LJ, Scott MM, et al. Direct leptin action on POMC neurons regulates glucose homeostasis and hepatic insulin sensitivity in mice. J Clin Invest. 2012;122(3):1000–9.PubMedPubMedCentralCrossRef
13.
go back to reference Davis C, Mudd J, Hawkins M: Neuroprotective effects of leptin in the context of obesity and metabolic disorders. Neurobiology of disease 2014, 72 Pt A:61–71. Davis C, Mudd J, Hawkins M: Neuroprotective effects of leptin in the context of obesity and metabolic disorders. Neurobiology of disease 2014, 72 Pt A:61–71.
14.
go back to reference Gao C, Liu Y, Li L, Holscher C. New animal models of Alzheimer's disease that display insulin desensitization in the brain. Rev Neurosci. 2013;24(6):607–15.PubMedCrossRef Gao C, Liu Y, Li L, Holscher C. New animal models of Alzheimer's disease that display insulin desensitization in the brain. Rev Neurosci. 2013;24(6):607–15.PubMedCrossRef
15.
go back to reference Rosen BS, Cook KS, Yaglom J, Groves DL, Volanakis JE, Damm D, White T, Spiegelman BM. Adipsin and complement factor D activity: an immune-related defect in obesity. Science (New York, NY). 1989;244(4911):1483–7.CrossRef Rosen BS, Cook KS, Yaglom J, Groves DL, Volanakis JE, Damm D, White T, Spiegelman BM. Adipsin and complement factor D activity: an immune-related defect in obesity. Science (New York, NY). 1989;244(4911):1483–7.CrossRef
16.
go back to reference Schmid A, Hochberg A, Berghoff M, Schlegel J, Karrasch T, Kaps M, Schaffler A. Quantification and regulation of adipsin in human cerebrospinal fluid (CSF). Clin Endocrinol. 2016;84(2):194–202.CrossRef Schmid A, Hochberg A, Berghoff M, Schlegel J, Karrasch T, Kaps M, Schaffler A. Quantification and regulation of adipsin in human cerebrospinal fluid (CSF). Clin Endocrinol. 2016;84(2):194–202.CrossRef
17.
go back to reference Lo JC, Ljubicic S, Leibiger B, Kern M, Leibiger IB, Moede T, Kelly ME, Chatterjee Bhowmick D, Murano I, Cohen P, et al. Adipsin is an adipokine that improves beta cell function in diabetes. Cell. 2014;158(1):41–53.PubMedPubMedCentralCrossRef Lo JC, Ljubicic S, Leibiger B, Kern M, Leibiger IB, Moede T, Kelly ME, Chatterjee Bhowmick D, Murano I, Cohen P, et al. Adipsin is an adipokine that improves beta cell function in diabetes. Cell. 2014;158(1):41–53.PubMedPubMedCentralCrossRef
18.
go back to reference Wang JS, Lee WJ, Lee IT, Lin SY, Lee WL, Liang KW, Sheu WH. Association between serum Adipsin levels and insulin resistance in subjects with various degrees of glucose intolerance. J Endocr Soc. 2019;3(2):403–10.PubMedCrossRef Wang JS, Lee WJ, Lee IT, Lin SY, Lee WL, Liang KW, Sheu WH. Association between serum Adipsin levels and insulin resistance in subjects with various degrees of glucose intolerance. J Endocr Soc. 2019;3(2):403–10.PubMedCrossRef
19.
go back to reference Song NJ, Kim S, Jang BH, Chang SH, Yun UJ, Park KM, Waki H, Li DY, Tontonoz P, Park KW. Small molecule-induced complement factor D (Adipsin) promotes lipid accumulation and adipocyte differentiation. PLoS One. 2016;11(9):e0162228.PubMedPubMedCentralCrossRef Song NJ, Kim S, Jang BH, Chang SH, Yun UJ, Park KM, Waki H, Li DY, Tontonoz P, Park KW. Small molecule-induced complement factor D (Adipsin) promotes lipid accumulation and adipocyte differentiation. PLoS One. 2016;11(9):e0162228.PubMedPubMedCentralCrossRef
20.
go back to reference Stahl GL, Xu Y, Hao L, Miller M, Buras JA, Fung M, Zhao H. Role for the alternative complement pathway in ischemia/reperfusion injury. Am J Pathol. 2003;162(2):449–55.PubMedPubMedCentralCrossRef Stahl GL, Xu Y, Hao L, Miller M, Buras JA, Fung M, Zhao H. Role for the alternative complement pathway in ischemia/reperfusion injury. Am J Pathol. 2003;162(2):449–55.PubMedPubMedCentralCrossRef
21.
go back to reference Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med. 1998;15(7):539–53.CrossRefPubMed Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med. 1998;15(7):539–53.CrossRefPubMed
22.
go back to reference Portet F, Ousset PJ, Visser PJ, Frisoni GB, Nobili F, Scheltens P, Vellas B, Touchon J. Mild cognitive impairment (MCI) in medical practice: a critical review of the concept and new diagnostic procedure. Report of the MCI working Group of the European Consortium on Alzheimer's disease. J Neurol Neurosurg Psychiatry. 2006;77(6):714–8.PubMedPubMedCentralCrossRef Portet F, Ousset PJ, Visser PJ, Frisoni GB, Nobili F, Scheltens P, Vellas B, Touchon J. Mild cognitive impairment (MCI) in medical practice: a critical review of the concept and new diagnostic procedure. Report of the MCI working Group of the European Consortium on Alzheimer's disease. J Neurol Neurosurg Psychiatry. 2006;77(6):714–8.PubMedPubMedCentralCrossRef
23.
go back to reference Liu LS. Chinese guidelines for the management of hypertension. Zhonghua xin xue guan bing za zhi 2011. 2010;39(7):579–615. Liu LS. Chinese guidelines for the management of hypertension. Zhonghua xin xue guan bing za zhi 2011. 2010;39(7):579–615.
24.
go back to reference Kim JD, Kang SJ, Lee MK, Park SE, Rhee EJ, Park CY, Oh KW, Park SW, Lee WY. C-Peptide-Based Index Is More Related to Incident Type 2 Diabetes in Non-Diabetic Subjects than Insulin-Based Index. Endocrinology and metabolism (Seoul, Korea). 2016;31(2):320–7.CrossRef Kim JD, Kang SJ, Lee MK, Park SE, Rhee EJ, Park CY, Oh KW, Park SW, Lee WY. C-Peptide-Based Index Is More Related to Incident Type 2 Diabetes in Non-Diabetic Subjects than Insulin-Based Index. Endocrinology and metabolism (Seoul, Korea). 2016;31(2):320–7.CrossRef
25.
go back to reference Herbert V, Brookes RL, Markus HS, Morris RG. Verbal fluency in cerebral small vessel disease and Alzheimer's disease. J Int Neuropsychol Soc. 2014;20(4):413–21.PubMedCrossRef Herbert V, Brookes RL, Markus HS, Morris RG. Verbal fluency in cerebral small vessel disease and Alzheimer's disease. J Int Neuropsychol Soc. 2014;20(4):413–21.PubMedCrossRef
26.
go back to reference Xiang Q, Zhang J, Li CY, Wang Y, Zeng MJ, Cai ZX, Tian RB, Jia W, Li XH. Insulin resistance-induced hyperglycemia decreased the activation of Akt/CREB in hippocampus neurons: molecular evidence for mechanism of diabetes-induced cognitive dysfunction. Neuropeptides. 2015;54:9–15.PubMedCrossRef Xiang Q, Zhang J, Li CY, Wang Y, Zeng MJ, Cai ZX, Tian RB, Jia W, Li XH. Insulin resistance-induced hyperglycemia decreased the activation of Akt/CREB in hippocampus neurons: molecular evidence for mechanism of diabetes-induced cognitive dysfunction. Neuropeptides. 2015;54:9–15.PubMedCrossRef
27.
go back to reference Yaffe K, Blackwell T, Whitmer RA, Krueger K, Barrett Connor E. Glycosylated hemoglobin level and development of mild cognitive impairment or dementia in older women. J Nutr Health Aging. 2006;10(4):293–5.PubMed Yaffe K, Blackwell T, Whitmer RA, Krueger K, Barrett Connor E. Glycosylated hemoglobin level and development of mild cognitive impairment or dementia in older women. J Nutr Health Aging. 2006;10(4):293–5.PubMed
28.
go back to reference SR-F J, Sa-Roriz TM, Rosset I, Camozzato AL, Santos AC, Chaves ML, Moriguti JC, Roriz-Cruz M. (pre) diabetes, brain aging, and cognition. Biochim Biophys Acta. 2009;1792(5):432–43.CrossRef SR-F J, Sa-Roriz TM, Rosset I, Camozzato AL, Santos AC, Chaves ML, Moriguti JC, Roriz-Cruz M. (pre) diabetes, brain aging, and cognition. Biochim Biophys Acta. 2009;1792(5):432–43.CrossRef
29.
go back to reference Sanz CM, Ruidavets JB, Bongard V, Marquie JC, Hanaire H, Ferrieres J, Andrieu S. Relationship between markers of insulin resistance, markers of adiposity, HbA1c, and cognitive functions in a middle-aged population-based sample: the MONA LISA study. Diabetes Care. 2013;36(6):1512–21.PubMedPubMedCentralCrossRef Sanz CM, Ruidavets JB, Bongard V, Marquie JC, Hanaire H, Ferrieres J, Andrieu S. Relationship between markers of insulin resistance, markers of adiposity, HbA1c, and cognitive functions in a middle-aged population-based sample: the MONA LISA study. Diabetes Care. 2013;36(6):1512–21.PubMedPubMedCentralCrossRef
30.
go back to reference Tangvarasittichai S, Pongthaisong S, Meemark S, Tangvarasittichai O. Abdominal obesity associated with elevated serum Butyrylcholinesterase activity, insulin resistance and reduced high density lipoprotein-cholesterol levels. Indian J Clinical Biochem. 2015;30(3):275–80.CrossRef Tangvarasittichai S, Pongthaisong S, Meemark S, Tangvarasittichai O. Abdominal obesity associated with elevated serum Butyrylcholinesterase activity, insulin resistance and reduced high density lipoprotein-cholesterol levels. Indian J Clinical Biochem. 2015;30(3):275–80.CrossRef
31.
go back to reference Sallam HS, Tumurbaatar B, Zhang WR, Tuvdendorj D, Chandalia M, Tempia F, Laezza F, Taglialatela G, Abate N. Peripheral adipose tissue insulin resistance alters lipid composition and function of hippocampal synapses. J Neurochem. 2015;133(1):125–33.PubMedPubMedCentralCrossRef Sallam HS, Tumurbaatar B, Zhang WR, Tuvdendorj D, Chandalia M, Tempia F, Laezza F, Taglialatela G, Abate N. Peripheral adipose tissue insulin resistance alters lipid composition and function of hippocampal synapses. J Neurochem. 2015;133(1):125–33.PubMedPubMedCentralCrossRef
32.
go back to reference Flier JS, Cook KS, Usher P, Spiegelman BM. Severely impaired adipsin expression in genetic and acquired obesity. Science (New York, NY). 1987;237(4813):405–8.CrossRef Flier JS, Cook KS, Usher P, Spiegelman BM. Severely impaired adipsin expression in genetic and acquired obesity. Science (New York, NY). 1987;237(4813):405–8.CrossRef
33.
go back to reference Napolitano A, Lowell BB, Damm D, Leibel RL, Ravussin E, Jimerson DC, Lesem MD, Van Dyke DC, Daly PA, Chatis P, et al. Concentrations of adipsin in blood and rates of adipsin secretion by adipose tissue in humans with normal, elevated and diminished adipose tissue mass. Int J Obes Relat Metab Disord. 1994;18(4):213–8.PubMed Napolitano A, Lowell BB, Damm D, Leibel RL, Ravussin E, Jimerson DC, Lesem MD, Van Dyke DC, Daly PA, Chatis P, et al. Concentrations of adipsin in blood and rates of adipsin secretion by adipose tissue in humans with normal, elevated and diminished adipose tissue mass. Int J Obes Relat Metab Disord. 1994;18(4):213–8.PubMed
34.
go back to reference Maslowska M, Vu H, Phelis S, Sniderman AD, Rhode BM, Blank D, Cianflone K. Plasma acylation stimulating protein, adipsin and lipids in non-obese and obese populations. Eur J Clin Investig. 1999;29(8):679–86.CrossRef Maslowska M, Vu H, Phelis S, Sniderman AD, Rhode BM, Blank D, Cianflone K. Plasma acylation stimulating protein, adipsin and lipids in non-obese and obese populations. Eur J Clin Investig. 1999;29(8):679–86.CrossRef
35.
go back to reference Abu-Farha M, Behbehani K, Elkum N. Comprehensive analysis of circulating adipokines and hsCRP association with cardiovascular disease risk factors and metabolic syndrome in Arabs. Cardiovasc Diabetol. 2014;13:76.PubMedPubMedCentralCrossRef Abu-Farha M, Behbehani K, Elkum N. Comprehensive analysis of circulating adipokines and hsCRP association with cardiovascular disease risk factors and metabolic syndrome in Arabs. Cardiovasc Diabetol. 2014;13:76.PubMedPubMedCentralCrossRef
36.
go back to reference Schrover IM, van der Graaf Y, Spiering W, Visseren FL. The relation between body fat distribution, plasma concentrations of adipokines and the metabolic syndrome in patients with clinically manifest vascular disease. Eur J Prev Cardiol. 2018;25(14):1548–57.PubMedPubMedCentralCrossRef Schrover IM, van der Graaf Y, Spiering W, Visseren FL. The relation between body fat distribution, plasma concentrations of adipokines and the metabolic syndrome in patients with clinically manifest vascular disease. Eur J Prev Cardiol. 2018;25(14):1548–57.PubMedPubMedCentralCrossRef
37.
go back to reference Cianflone K. The acylation stimulating protein pathway: clinical implications. Clin Biochem. 1997;30(4):301–12.PubMedCrossRef Cianflone K. The acylation stimulating protein pathway: clinical implications. Clin Biochem. 1997;30(4):301–12.PubMedCrossRef
38.
go back to reference Kim TE, Lee DH, Kim YJ, Mok JO, Kim CH, Park JH, Lee TK, Yoo K, Jeong Y, Lee Y, et al. The relationship between cognitive performance and insulin resistance in non-diabetic patients with mild cognitive impairment. Int J Geriatr Psychiatry. 2015;30(6):551–7.PubMedCrossRef Kim TE, Lee DH, Kim YJ, Mok JO, Kim CH, Park JH, Lee TK, Yoo K, Jeong Y, Lee Y, et al. The relationship between cognitive performance and insulin resistance in non-diabetic patients with mild cognitive impairment. Int J Geriatr Psychiatry. 2015;30(6):551–7.PubMedCrossRef
39.
go back to reference Ekblad LL, Rinne JO, Puukka P, Laine H, Ahtiluoto S, Sulkava R, Viitanen M, Jula A. Insulin resistance predicts cognitive decline: an 11-year follow-up of a nationally representative adult population sample. Diabetes Care. 2017;40(6):751–8.PubMedCrossRef Ekblad LL, Rinne JO, Puukka P, Laine H, Ahtiluoto S, Sulkava R, Viitanen M, Jula A. Insulin resistance predicts cognitive decline: an 11-year follow-up of a nationally representative adult population sample. Diabetes Care. 2017;40(6):751–8.PubMedCrossRef
40.
go back to reference Gursoy Calan O, Calan M, Yesil Senses P, Unal Kocabas G, Ozden E, Sari KR, Kocar M, Imamoglu C, Senses YM, Bozkaya G, et al. Increased adipsin is associated with carotid intima media thickness and metabolic disturbances in polycystic ovary syndrome. Clin Endocrinol. 2016;85(6):910–7.CrossRef Gursoy Calan O, Calan M, Yesil Senses P, Unal Kocabas G, Ozden E, Sari KR, Kocar M, Imamoglu C, Senses YM, Bozkaya G, et al. Increased adipsin is associated with carotid intima media thickness and metabolic disturbances in polycystic ovary syndrome. Clin Endocrinol. 2016;85(6):910–7.CrossRef
41.
go back to reference Derosa G, Fogari E, D'Angelo A, Bianchi L, Bonaventura A, Romano D, Maffioli P. Adipocytokine levels in obese and non-obese subjects: an observational study. Inflammation. 2013;36(4):914–20.PubMedCrossRef Derosa G, Fogari E, D'Angelo A, Bianchi L, Bonaventura A, Romano D, Maffioli P. Adipocytokine levels in obese and non-obese subjects: an observational study. Inflammation. 2013;36(4):914–20.PubMedCrossRef
42.
go back to reference Zhong Y, Miao Y, Jia WP, Yan H, Wang BY, Jin J. Hyperinsulinemia, insulin resistance and cognitive decline in older cohort. Biomed Environ Sci. 2012;25(1):8–14.PubMed Zhong Y, Miao Y, Jia WP, Yan H, Wang BY, Jin J. Hyperinsulinemia, insulin resistance and cognitive decline in older cohort. Biomed Environ Sci. 2012;25(1):8–14.PubMed
43.
go back to reference Sripetchwandee J, Chattipakorn N, Chattipakorn SC. Links between obesity-induced brain insulin resistance, brain mitochondrial dysfunction, and dementia. Front Endocrinol. 2018;9:496.CrossRef Sripetchwandee J, Chattipakorn N, Chattipakorn SC. Links between obesity-induced brain insulin resistance, brain mitochondrial dysfunction, and dementia. Front Endocrinol. 2018;9:496.CrossRef
44.
go back to reference Zhou Y, Fang R, Liu LH, Chen SD, Tang HD. Clinical characteristics for the relationship between Type-2 diabetes mellitus and cognitive impairment: a Cross-sectional study. Aging Dis. 2015;6(4):236–44.PubMedPubMedCentralCrossRef Zhou Y, Fang R, Liu LH, Chen SD, Tang HD. Clinical characteristics for the relationship between Type-2 diabetes mellitus and cognitive impairment: a Cross-sectional study. Aging Dis. 2015;6(4):236–44.PubMedPubMedCentralCrossRef
Metadata
Title
Association between plasma adipsin level and mild cognitive impairment in Chinese patients with type 2 diabetes: a cross-sectional study
Authors
Dan Guo
Yang Yuan
Rong Huang
Sai Tian
Jiaqi Wang
Hongyan Lin
Ke An
Jin Han
Shaohua Wang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Endocrine Disorders / Issue 1/2019
Electronic ISSN: 1472-6823
DOI
https://doi.org/10.1186/s12902-019-0431-y

Other articles of this Issue 1/2019

BMC Endocrine Disorders 1/2019 Go to the issue