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Noninvasive evaluation of diabetic patients with high fasting blood glucose using DWI and BOLD MRI

  • Kidneys, Ureters, Bladder, Retroperitoneum
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Purpose

To investigate the renal microstructure changes and hypoxia changes in type 2 diabetic patients and the relationship between them and glucose using both diffusion-weighted imaging (DWI) and blood oxygenation level-dependent magnetic resonance imaging (BOLD MRI).

Methods

After measuring morning fasting blood glucose, DWI and BOLD MRI were performed in 57 patients with type 2 diabetes mellitus (DM group) and 14 healthy volunteers (NC group). According to the fasting blood glucose levels, diabetic patients were divided into a normoglycemic diabetes group (group A), a less hyperglycemic diabetes group (group B) and a more hyperglycemic diabetes group (group C). The renal parenchymal apparent diffusion coefficient (ADC), renal cortical R2* (CR2*), and medullary R2* (MR2*) were measured, and the R2* ratio between the medulla and cortex (MCR) was calculated. To test for differences in ADC, R2*, and MCR among the four groups, the data were analyzed by separate one-way ANOVAs. The correlations between ADC, R2*, and MCR and the clinical index of renal function were analyzed.

Results

Groups B and C had significantly lower ADC values in the renal parenchyma (P = 0.048, 0.002) and significantly higher MR2* and MCR values (P < 0.000, P = 0.001, 0.001, and 0.005, respectively) than the NC group. ADC was negatively correlated with glucose, and MR2*, MCR and glucose showed a weak positive correlation.

Conclusion

DWI and BOLD may indirectly and qualitatively reflect the kidney microstructure status and hypoxia level of diabetic patients at different blood glucose levels to a certain extent, and possibly guide the clinical treatment of diabetic patients with different blood glucose levels.

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References

  1. Ma RCW (2018) Epidemiology of diabetes and diabetic complications in China. Diabetologia 61(6):1249-1260. https://doi.org/10.1007/s00125-018-4557-7

    Article  PubMed  Google Scholar 

  2. Reutens AT, Atkins RC (2011) Epidemiology of Diabetic Nephropathy. Contrib Nephrol 170: 1-7. https://doi.org/10.1159/000324934

    Article  PubMed  Google Scholar 

  3. Warren AM, Søren T. Knudsen, Cooper ME (2019) Diabetic nephropathy: an insight into molecular mechanisms and emerging therapies. Expert Opin Ther Targets 23(7):579-591. https://doi.org/10.1080/14728222.2019.1624721

    Article  PubMed  Google Scholar 

  4. Zhang L, Long J, Jiang W, Shi Y, He X, Zhou Z, Li Y, Yeung RO, Wang J, Matsushita K, Coresh J, Zhao MH, Wang H (2016) Trends in chronic kidney disease in China. N Engl J Med 375(9):905-906. https://doi.org/10.1056/NEJMc1602469

    Article  PubMed  Google Scholar 

  5. Freedman BI, Bostrom M, Daeihagh P, Bowden DW (2007) Genetic Factors in Diabetic Nephropathy. Clin J Am Soc Nephrol 2(6):1306-1316. https://doi.org/10.2215/CJN.02560607

    Article  CAS  PubMed  Google Scholar 

  6. Rendra E, Riabov V, Mossel DM, Sevastyanova T, Harmsen MC, Kzhyshkowska J (2019) Reactive oxygen species (ROS) in macrophage activation and function in diabetes. Immunobiology 224(2):242-253. https://doi.org/10.1016/j.imbio.2018.11.010

    Article  CAS  PubMed  Google Scholar 

  7. Palm F, Cederberg J, Hansell P, Liss P, Carlsson PO (2003) Reactiv oxygen species cause diabetes-induced decrease in renal oxygen tension. Diabetologia 46(8):1153-1160. https://doi.org/10.1007/s00125-003-1155-z

    Article  CAS  PubMed  Google Scholar 

  8. Peng XG, Bai YY, Fang F, Wang XY, Mao H, Teng GJ, Ju S (2013) Renal lipids and oxygenation in diabetic mice: noninvasive quantification with MR Imaging. Radiology 269 (3): 748-757. https://doi.org/10.1148/radiol.13122860

    Article  PubMed  Google Scholar 

  9. Friederich-Persson M, Thörn E, Hansell P, Nangaku M, Levin M, Palm F (2013) Kidney Hypoxia, Attributable to increased oxygen consumption, induces nephropathy independently of hyperglycemia and oxidative stress. Hypertension 62(5):914-919. https://doi.org/10.1161/HYPERTENSIONAHA.113.01425

    Article  CAS  PubMed  Google Scholar 

  10. Heyman SN, Khamaisi M, Rosen S, Rosenberger C (2008) Renal parenchymal hypoxia, hypoxia response and the progression of chronic kidney disease. Am J Nephrol 28(6):998–1006. 62(5):914–919.https://doi.org/10.1159/000146075

  11. Schiffer TA, Friederich-Persson M (2017) Mitochondrial reactive oxygen species and kidney hypoxia in the development of diabetic nephropathy. Front Physiol Apr 11; 8:211. https://doi.org/10.3389/fphys.2017.00211

  12. Caroli A, Schneider M, Friedli I, Ljimani A, De Seigneux S, Boor P, Gullapudi L, Kazmi I, Mendichovszky IA, Notohamiprodjo M, Selby NM, Thoeny HC, Grenier N, Vallée JP. Nephrol Dial Transplant (2018) Diffusion-weighted magnetic resonance imaging to assess diffuse renal pathology: a systematic review and statement paper. Nephrol Dial Transplant 33(suppl_2): ii29-ii40. https://doi.org/10.1093/ndt/gfy163

  13. Pruijm M, Mendichovszky IA, Liss P, Van der Niepen P, Textor SC, Lerman LO, Krediet CTP, Caroli A, Burnier M, Prasad PV (2018) Renal blood oxygenation level-dependent magnetic resonance imaging to measure renal tissue oxygenation: a statement paper and systematic review. Nephrol Dial Transplant 33(suppl_2): ii22-ii28.https://doi.org/10.1093/ndt/gfy243

  14. Selby NM, Blankestijn PJ, Boor P, Combe C, Eckardt KU, Eikefjord E, Garcia-Fernandez N, Golay X, Gordon I, Grenier N, Hockings PD, Jensen JD, Joles JA, Kalra PA, Krämer BK, Mark PB, Mendichovszky IA, Nikolic O, Odudu A, Ong ACM, Ortiz A, Pruijm M, Remuzzi G, Rørvik J, de Seigneux S, Simms RJ, Slatinska J, Summers P, Taal MW, Thoeny HC, Vallée JP, Wolf M, Caroli A, Sourbron S (2018) Magnetic resonance imaging biomarkers for chronic kidney disease: a position paper from the European Cooperation in Science and Technology Action PARENCHIMA. Nephrol Dial Transplant 33(suppl_2): ii4-ii14. https://doi.org/10.1093/ndt/gfy152

  15. Ries M, Basseau F, Tyndal B, Jones R, Deminière C, Catargi B, Combe C, Moonen CW, Grenier N (2003) Renal diffusion and BOLD MRI in experimental diabetic nephropathy. J Magn Reson Imaging 17(1): 104-113. https://doi.org/10.1002/jmri.10224

    Article  PubMed  Google Scholar 

  16. Inoue T, Kozawa E, Okada H, Inukai K, Watanabe S, Kikuta T, Watanabe Y, Takenaka T, Katayama S, Tanaka J, Suzuki H (2011) Noninvasive evaluation of kidney hypoxia and fibrosis using magnetic resonance imaging. J Am Soc Nephrol 22(8): 1429-1434. https://doi.org/10.1681/ASN.2010111143

    Article  PubMed  PubMed Central  Google Scholar 

  17. Pruijm M, Hofmann L, Zanchi A, Maillard M, Forni V, Muller ME, Wuerzner G, Vogt B, Stuber M, Burnier M (2013) Blockade of the renin–angiotensin system and renal tissue oxygenation as measured with BOLD-MRI in patients with type 2 diabetes. Diabetes Res Clin Pract 99(2): 136-144. https://doi.org/10.1016/j.diabres.2012.11.004

    Article  CAS  PubMed  Google Scholar 

  18. Hofmann L, Simon-Zoula S, Nowak A, Giger A, Vock P, Boesch C, Frey FJ, Vogt B (2006) BOLD-MRI for the assessment of renal oxygenation in humans: acute effect of nephrotoxic xenobiotics. Kidney Int 70(1): 144-150. https://doi.org/10.1038/sj.ki.5000418

    Article  CAS  PubMed  Google Scholar 

  19. Thoeny HC, Kessler TM, Simon-Zoula S, De Keyzer F, Mohaupt M, Studer UE, Vermathen P (2008) Renal oxygenation changes during acute unilateral ureteral obstruction: assessment with blood oxygen level dependent MR imaging—initial experience. Radiology 47(3):754. https://doi.org/10.1148/radiol.2473070877

    Article  Google Scholar 

  20. Hueper K, Hartung D, Gutberlet M, Gueler F, Sann H, Husen B, Wacker F, Reiche D (2013) Assessment of impaired vascular reactivity in a rat model of diabetic nephropathy: effect of nitric oxide synthesis inhibition on intrarenal diffusion and oxygenation measured by magnetic resonance imaging. Am J Physiol Renal Physiol 305(10): F1428-F1435. https://doi.org/10.1152/ajprenal.00123.2013

    Article  CAS  PubMed  Google Scholar 

  21. Lu L, Sedor JR, Gulani V, Schelling JR, O'Brien A, Flask CA, MacRae Dell K (2011) Use of Diffusion Tensor MRI to Identify Early Changes in Diabetic Nephropathy. Am J Nephrol. 34(5):476-482. https://doi.org/10.1159/000333044

    Article  PubMed  PubMed Central  Google Scholar 

  22. Cakmak P, Yağcı AB, Dursun B, Herek D, Fenkçi SM (2014) Renal diffusion-weighted imaging in diabetic nephropathy: correlation with clinical stages of disease. Diagn Interv Radiol 20(5): 374-378. https://doi.org/10.5152/dir.2014.13513

    Article  PubMed  PubMed Central  Google Scholar 

  23. Li ZC, Cai YZ, Tang ZG, Zuo PL, Liu RB, Liu F (2018) Lipo-prostaglandin E1 improves renal hypoxia evaluated by BOLD-MRI in patients with diabetic kidney disease. Clin Imaging 50:239-242. https://doi.org/10.1016/j.clinimag.2018.04.015

    Article  PubMed  Google Scholar 

  24. Feng YZ, Ye YJ, Cheng ZY, Hu JJ, Zhang CB, Qian L, Lu XH, Cai XR (2020) Non-invasive assessment of early stage diabetic nephropathy by DTI and BOLD MRI. Br J Radiol 93(1105): 20190562. https://doi.org/10.1259/bjr.20190562

    Article  PubMed  PubMed Central  Google Scholar 

  25. Yin WJ, Liu F, Li XM, Yang L, Zhao S, Huang ZX, Huang YQ, Liu RB (2012) Noninvasive evaluation of renal oxygenation in diabetic nephropathy by BOLD-MRI. Eur J Radiol 81(7):1426-1431. https://doi.org/10.1016/j.ejrad.2011.03.045

    Article  PubMed  Google Scholar 

  26. Vexler VS, Roberts TP, Rosenau W (1996) Early detection of acute tubular injury with diffusion-weighted magnetic resonance imaging in a rat model of myohemoglobinuric acute renal failure. Ren Fail 18 (1):41-57. https://doi.org/10.3109/08860229609052773

    Article  CAS  PubMed  Google Scholar 

  27. Wang Y, Zhang H, Zhang R, Zhao Z, Xu Z, Wang L, Liu R, Gao F (2017) Investigation of aquaporins and apparent diffusion coefficient from ultra-high b- values in a rat model of diabetic nephropathy. ang RZ, et al. Eur Radiol Exp 1 (1): 13. https://doi.org/10.1186/s41747-017-0016-3

  28. Caramori ML, Fioretto P, Mauer M (2003) Low glomerular filtration rate in normoalbuminuric type 1 diabetic patients an indicator of more advanced glomerular lesions. Diabetes 52 (4):1036-1040. https://doi.org/10.2337/diabetes.52.4.1036

    Article  CAS  PubMed  Google Scholar 

  29. Luo B, Wen S, Chen YC, Cui Y, Gao FB, Yao YY, Ju SH, Teng GJ (2015) Lox-1-targeted iron oxide nanoparticles detect early diabetic nephropathy in db/db Mice. Mol Imaging Biol 17(5): 652-660. https://doi.org/10.1007/s11307-015-0829-5

    Article  CAS  PubMed  Google Scholar 

  30. Xiao L, Zhu X, Yang S, Liu F, Zhou Z, Zhan M, Xie P, Zhang D, Li J, Song P, Kanwar YS, Sun L (2014) Rap1 ameliorates renal tubular injury in diabetic nephropathy. Diabetes 63 (4):1366-1380. https://doi.org/10.2337/db13-1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Yamashita Y, Tang Y, Takahashi M (1998) Ultrafast MR imaging of the abdomen: echo planar imaging and diffusion-weighted imaging. J Magn Reson Imaging 8(2):367-374. https://doi.org/10.1002/jmri.1880080216

    Article  CAS  PubMed  Google Scholar 

  32. Hueper K, Hartung D, Gutberlet M, Gueler F, Sann H, Husen B, Wacker F, Reiche D (2012) Magnetic resonance diffusion tensor imaging for evaluation of histopathological changes in a rat model of diabetic nephropathy. Invest Radiol 47(7):430-437. https://doi.org/10.1097/RLI.0b013e31824f272d

    Article  PubMed  Google Scholar 

  33. Chen X, Xiao W, Li X, He J, Huang X, Tan Y (2014) In vivo evaluation of renal function using diffusion weighted imaging and diffusion tensor imaging in type 2 diabetics with normoalbuminuria versus microalbuminuria. Front Med 8(4): 471-476. https://doi.org/10.1007/s11684-014-0365-8

    Article  PubMed  Google Scholar 

  34. Baines A, Ho P (2002) Glucose stimulates O2 consumption, NOS, and Na/H exchange in diabetic rat proximal tubules. Am J Physiol Renal Physiol 283(2): F286-F293. https://doi.org/10.1152/ajprenal.00330.2001

    Article  CAS  PubMed  Google Scholar 

  35. Palm F, Fasching A, Hansell P, Källskog O (2010) Nitric oxide originating from NOS1 controls oxygen utilization and electrolyte transport efficiency in the diabetic kidney. Am J Physiol Renal Physiol 298(2): F416-F420. https://doi.org/10.1152/ajprenal.00229.2009

    Article  CAS  PubMed  Google Scholar 

  36. Palm, F (2006) Intrarenal Oxygen in diabetes and a possible link to diabetic nephropathy. Clin Exp Pharmacol Physiol 33(10): 997-1001. https://doi.org/10.1111/j.1440-1681.2006.04473.x

    Article  CAS  PubMed  Google Scholar 

  37. Magri CJ, Fava S (2009) The role of tubular injury in diabetic nephropathy. Eur J Intern Med 20(6): 551-555. https://doi.org/10.1016/j.ejim.2008.12.012

    Article  CAS  PubMed  Google Scholar 

  38. Hansell P, Welch WJ, Blantz RC, Palm F (2013) Determinants of kidney oxygen consumption and their relationship to tissue oxygen tension in diabetes and hypertension. Clin Exp Pharmacol Physiol 40(2): 123-137. https://doi.org/10.1111/1440-1681.12034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Pohlmann A, Arakelyan K, Hentschel J, Cantow K, Flemming B, Ladwig M, Waiczies S, Seeliger E, Niendorf T (2014) Detailing the relation between renal T2* and renal tissue pO2 using an integrated approach of parametric magnetic resonance imaging and invasive physiological measurements. Invest Radiol 49 (8): 547-560. https://doi.org/10.1097/RLI.0000000000000054

    Article  CAS  PubMed  Google Scholar 

  40. Wang ZJ, Kumar R, Banerjee S, Hsu CY (2011) Blood oxygen level-dependent (BOLD) MRI of diabetic nephropathy: Preliminary experience. J Magn Reson Imaging 33(3): 655-660. https://doi.org/10.1002/jmri.22501

    Article  PubMed  PubMed Central  Google Scholar 

  41. Niendorf T, Pohlmann A, Arakelyan K, Flemming B, Cantow K, Hentschel J, Grosenick D, Ladwig M, Reimann H, Klix S, Waiczies S, Seeliger E (2015) How bold is blood oxygenation level-dependent (BOLD) magnetic resonance imaging of the kidney? Opportunities, challenges and future directions. Acta Physiol (Oxf) 13(1):19-38. https://doi.org/10.1111/apha.12393

    Article  CAS  Google Scholar 

  42. Wang Q, Guo C, Zhang L, Zhang R, Wang Z, Xu Y, Xiao W (2018) BOLD MRI to evaluate early development of renal injury in a rat model of diabetes. J Int Med Res 46(4): 1391-1403. https://doi.org/10.1177/0300060517743826

    Article  PubMed  PubMed Central  Google Scholar 

  43. Ding J, Chen J, Jiang Z, Zhou H, Di J, Xing S, Xing W (2016) Is low b-factors-based apparent diffusion coefficient helpful in assessing renal dysfunction? Radiol Med 121 (1):6-11. https://doi.org/10.1007/s11547-015-0577-2

    Article  PubMed  Google Scholar 

  44. Ljimani A, Caroli A, Laustsen C, Francis S, Mendichovszky IA, Bane O, Nery F, Sharma K, Pohlmann A, Dekkers IA, Vallee JP, Derlin K, Notohamiprodjo M, Lim RP, Palmucci S, Serai SD, Periquito J, Wang ZJ, Froeling M, Thoeny HC, Prasad P, Schneider M, Niendorf T, Pullens P, Sourbron S, Sigmund EE (2020) Consensus-based technical recommendations for clinical translation of renal diffusion-weighted MRI. MAGMA 33(1):177-195. https://doi.org/10.1007/s10334-019-00790-y

    Article  CAS  PubMed  Google Scholar 

  45. Mendichovszky I, Pullens P, Dekkers I, Nery F, Bane O, Pohlmann A, de Boer A, Ljimani A, Odudu A, Buchanan C, Sharma K, Laustsen C, Harteveld A, Golay X, Pedrosa I, Alsop D, Fain S, Caroli A, Prasad P, Francis S, Sigmund E, Fernández-Seara M, Sourbron S (2020) Technical recommendations for clinical translation of renal MRI: a consensus project of the Cooperation in Science and Technology Action PARENCHIMA. MAGMA 33(1):131-140. https://doi.org/10.1007/s10334-019-00784-w

    Article  CAS  PubMed  Google Scholar 

  46. Bane O, Mendichovszky IA, Milani B, Dekkers IA, Deux JF, Eckerbom P, Grenier N, Hall ME, Inoue T, Laustsen C, Lerman LO, Liu C, Morrell G, Pedersen M, Pruijm M, Sadowski EA, Seeliger E, Sharma K, Thoeny H, Vermathen P, Wang ZJ, Serafin Z, Zhang JL, Francis ST, Sourbron S, Pohlmann A, Fain SB, Prasad PV (2020) Consensus-based technical recommendations for clinical translation of renal BOLD MRI. MAGMA. 33(1):199-215. https://doi.org/10.1007/s10334-019-00802-x

    Article  PubMed  Google Scholar 

  47. Christen T, Lemasson B, Pannetier N, Farion R, Remy C, Zaharchuk G, Barbier EL (2012) Is T2* enough to assess oxygenation? Quantitative blood oxygen level-dependent analysis in brain tumor. Radiology 262(2):495-502. https://doi.org/10.1148/radiol.11110518

    Article  PubMed  PubMed Central  Google Scholar 

  48. Bryan RN (2012) Science to practice: is T2* enough to assess oxygenation? Radiology 262(2):375-377. https://doi.org/10.1148/radiol.11112449

    Article  PubMed  Google Scholar 

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Funding

This study was funded by Beijing Municipal Administration of Hospitals’ Ascent Plan (Code: DFL20180802).

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Authors and Affiliations

  1. Department of Radiology, Xuanwu Hospital, Capital Medical University, Beijing, 100053, China

    Shuang-Shuang Zheng & Jie Lu

  2. Department of Radiology, Fuxing Hospital, Capital Medical University, Beijing, 100038, China

    Shuang-Shuang Zheng & Yue-Ming He

  3. Department of Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing, 100053, China

    Jie Lu

  4. Beijing Key Laboratory of Magnetic Resonance Imaging and Brain Informatics, Beijing, 100053, China

    Jie Lu

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Correspondence to Jie Lu.

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Zheng, SS., He, YM. & Lu, J. Noninvasive evaluation of diabetic patients with high fasting blood glucose using DWI and BOLD MRI. Abdom Radiol 46, 1659–1669 (2021). https://doi.org/10.1007/s00261-020-02780-4

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