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Metabolic Brain Disease

, Volume 31, Issue 4, pp 929–936 | Cite as

Cerebral blood flow changes in hemodialysis and peritoneal dialysis patients: an arterial-spin labeling MR imaging

  • Xiao Lu Jiang
  • Ji Qiu Wen
  • Long Jiang Zhang
  • Gang Zheng
  • Xue Li
  • Zhe Zhang
  • Ya Liu
  • Li Juan Zheng
  • Long Wu
  • Hui Juan Chen
  • Xiang Kong
  • Song Luo
  • Guang Ming Lu
  • Xue Man Ji
  • Zong Jun Zhang
Original Article

Abstract

We used arterial-spin labeling (ASL) MR imaging, a non-invasive technique to evaluate cerebral blood flow (CBF) changes in patients with end-stage renal disease (ESRD) undergoing peritoneal dialysis (PD) and hemodialysis (HD), and nondialysis ESRD patients compared with healthy cohort. Ninety seven ESRD patients including 32 PD patients (20 male, 12 female; mean age 33 ± 8 years), 33 HD patients (22 male, 11 female; mean age 33 ± 8 years) and 32 nondialysis patients (20 male, 12 female; mean age 35 ± 7 years) and 31 age- and gender-matched healthy controls (20 male, 11 female; mean age 32 ± 8 years) were included in this study. All subjects underwent ASL MR imaging, neuropsychologic tests, and ESRD patients underwent laboratory testing. CBF values were compared among PD, HD, nondialysis patients and control groups. Correlation analysis and multiple regression analysis were performed to investigate the association between CBF values and hemoglobin, neuropsychologic test results, serum creatinine, urea levels, disease duration, and dialysis duration. Elevated CBFs of whole brain region, gray matter, and white matter were found in all ESRD patient groups compared with healthy controls (all P < 0.001). However, compared with non-dialysis ESRD patients, both PD and HD patients had widespread regional CBF decline mainly in bilateral frontal and anterior cingulate cortices. There were no differences for CBF between PD and HD patient groups. Negative correlations were observed between mean CBFs of whole brain region, gray matter, and white matter and the hemoglobin level in all ESRD patients. Multiple linear regression showed elevated CBF of multiple brain areas correlated with some neuropsychological tests in ESRD patients (all P < 0.001, AlphaSim corrected), but the association was not present or shrank after adjusting hemoglobin level. This study found that mean CBF was predominantly increased in patients with ESRD, which correlated with their hemoglobin level and neurocognitive disorders. There were no differences of CBF change and cognitive function between PD and HD ESRD patients with long-term treatment. The degree of anemia may be a predominant risk factor for cognitive impairment in these ESRD patients.

Keywords

End-stage renal disease (ESRD) Cerebral blood flow (CBF) Peritoneal dialysis (PD) Hemodialysis (HD) Arterial-spin labeling (ASL) 

Abbreviations

ASL

Arterial-spin labeling

CBF

Cerebral blood flow

DST

Digit-symbol test

ESRD

End-stage renal disease

NCT-A

Number connecting-A

PD

Peritoneal dialysis

HD

Hemodialysis

Notes

Compliance with ethical standards

Conflict of interest

None.

Grants

Supported by grants from National Natural Science Foundation of China (grant Nos. 81,471,644 and 81,101,039 to G.Z., grants Nos. 81,322,020, 81,230,032, and 81,171,313 to L.J.Z.), the Program for New Century Excellent Talents in the University (NCET-12-0260 to L.J.Z.), and the Grants from the China Postdoctoral Science Foundation (grant Nos. 2014 T71014 and 2015 M570436 to G.Z.)

References

  1. Arieff AI (1985) Aluminum and the pathogenesis of dialysis encephalopathy. Am J Kidney Dis 6(5):317–321CrossRefPubMedGoogle Scholar
  2. Bajaj JS, Wade JB, Sanyal AJ (2009) Spectrum of neurocognitive impairment in cirrhosis: implications for the assessment of hepatic encephalopathy. Hepatology 50(6):2014–2021CrossRefPubMedGoogle Scholar
  3. Buoncristiani U, Alberti A, Gubbiotti G, Mazzotta G, Gallai V, Quintaliani G, Gaburri M (1993) Better preservation of cognitive faculty in continuous ambulatory peritoneal dialysis. Perit Dial Int 13:S202–S205PubMedGoogle Scholar
  4. Bush G, Luu P, Posner ,MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4(6):215–222CrossRefPubMedGoogle Scholar
  5. Chai C, Zhang M, Long M, Chu Z, Wang T, Wang L, Guo Y, Yan S, Haacke EM, Shen W, Xia S (2015) Increased brain iron deposition is a risk factor for brain atrophy in patients with haemodialysis: a combined study of quantitative susceptibility mapping and whole brain volume analysis. Metab Brain Dis 30(4):1009–1016CrossRefPubMedGoogle Scholar
  6. Eknoyan G, Lameire N, Barsoum R, Eckardt KU, Levin A, Levin N, Locatelli F, MacLeod A, Vanholder R, Walker R, Wang H (2004) The burden of kidney disease: improving global outcomes. Kidney Int 66:1310–1314CrossRefPubMedGoogle Scholar
  7. Fazekas G, Fazekas F, Schmidt R, Flooh E, Valetitsch H, Kapeller P, Krejs GJ (1996) Pattern of cerebral blood flow and cognition in patients undergoing chronic haemodialysis treatment. Nucl Med Commun 17(7):603–608CrossRefPubMedGoogle Scholar
  8. Günal AI, Ilkay E, Kirciman E, Karaca I, Dogukan A (2003) Celiker H (2003) blood pressure control and left ventricular hypertrophy in long-term CAPD and hemodialysis patients: a cross-sectional study. Perit Dial Int 23(6):563–567PubMedGoogle Scholar
  9. Hata R, Matsumoto M, Handa N, Terakawa H, Sugitani Y, Kamada T (1994) Effects of hemodialysis on cerebral circulation evaluated by transcranial Doppler ultrasonography. Stroke 25(2):408–412CrossRefPubMedGoogle Scholar
  10. Hirakata H, Yao H, Osato S, Ibayashi S, Onoyama K, Otsuka M, Ichiya Y, Kuwabara Y, Masuda Y, Fujishima M (1992) CBF and oxygen metabolism in hemodialysis patients: effects of anemia correction with recombinant human EPO. Am J Phys 262(5 Pt 2):F737–F743Google Scholar
  11. Horina JH, Fazekas F, Niederkorn K, Payer F, Valetitsch H, Winkler HM, Horner S, Freidl W, Pogglitsch H, Krejs GJ (1991) Cerebral hemodynamic changesfollowing treatment with erythropoietin. Nephron 58(4):407–412Google Scholar
  12. Iseki K, Fukiyama K (1996) Predictors of stroke in patients receiving chronic hemodialysis. Kidney Int 50(5):1672–1675CrossRefPubMedGoogle Scholar
  13. Isshiki R, Kobayashi S, Iwagami M, Tsutumi D, Mochida Y, Ishioka K, Oka M, Maesato K, Moriya H, Ohtake T, Hidaka S (2014) Cerebral blood flow in patients with peritoneal dialysis by an easy Z-score imaging system for brain perfusion single-photon emission tomography. Ther Apher Dial 18(3):291–296CrossRefPubMedGoogle Scholar
  14. Kalirao P, Pederson S, Foley RN, Kolste A, Tupper D, Zaun D, Buot V, Murray AM (2011) Cognitive impairment in peritoneal dialysis patients. Am J Kidney Dis 57(4):612–620CrossRefPubMedPubMedCentralGoogle Scholar
  15. Kambova L (1998) Recombinant erythropoietin improves cognitive function in chronic haemodialysis patients. Nephrol Dial Transplant 13(1):229–230CrossRefPubMedGoogle Scholar
  16. Knopman D, Boland ,LL, Mosley T, Howard G, Liao D, Szklo M, McGovern P, AR F, Atherosclerosis Risk in Communities (ARIC) Study Investigators (2001) Cardiovascular risk factors and cognitive decline in middle-aged adults. Neurology 56:42–48CrossRefPubMedGoogle Scholar
  17. Kong X, Wen JQ, Qi RF, Luo S, Zhong JH, Chen HJ, Ji GJ, Lu GM, Zhang LJ (2014) Diffuse interstitial brain edema in patients with end-stage renal disease undergoing hemodialysis: a tract-based spatial statistics study. Medicine (Baltimore) 93(28):e313CrossRefGoogle Scholar
  18. Kuwabara Y, Sasaki M, Hirakata H, Koga H, Nakagawa M, Chen T, Kaneko K, Masuda K, Fujishima M (2002) Cerebral blood flow and vasodilatory capacity in anemia secondary to chronic renal failure. Kidney Int 61(2):564–569CrossRefPubMedGoogle Scholar
  19. Luo S, Qi RF, Wen JQ, Zhong JH, Kong X, Liang X, Xu Q, Zheng G, Zhang Z, Zhang LJ, Lu GM (2015) Abnormal intrinsic brain activity patterns in patients with end-stage renal disease undergoing peritoneal dialysis: a resting-state functional MR imaging study. Radiology 8:141913Google Scholar
  20. Madan P, Kalra OP, Agarwal S, Tandon OP (2007) Cognitive impairment in chronic kidney disease. Nephrol Dial Transplant 22(2):440–444CrossRefPubMedGoogle Scholar
  21. Marsh JT, Brown WS, Wolcott D, Landsverk J, Nissenson AR (1986) Electrophysiological indices of CNS function in hemodialysis and CAPD. Kidney Int 30(6):957–963CrossRefPubMedGoogle Scholar
  22. Marsh JT, Brown WS, Wolcott D, Carr CR, Harper R, Schweitzer SV, Nissenson AR (1991) rHuEPO treatment improves brain and cognitive function of anemic dialysis patients. Kidney Int 39(1):155–163CrossRefPubMedGoogle Scholar
  23. Mathew RJ, Rabin P, Stone WJ, Wilson WH (1985) Regional cerebral blood flow in dialysis encephalopathy and primary degenerative dementia. Kidney Int 28(1):64–68CrossRefPubMedGoogle Scholar
  24. McIntyre CW (2011) Hemodynamic effects of peritoneal dialysis. Perit Dial Int 31(Suppl 2):S73–S76CrossRefPubMedGoogle Scholar
  25. Metry G, Spittle M, Rahmati S, Giller C, Giller A, Kaufman A, Schneditz D, Manno E, Brener Z, Boniece I, Ronco F, Ronco C, Levin NW (2002) Online monitoring of cerebral hemodynamics during hemodialysis. Am J Kidney Dis 40(5):996–1004CrossRefPubMedGoogle Scholar
  26. Murray AM, Tupper DE, Knopman DS, Gilbertson DT, Pederson SL, Li S, Smith GE, Hochhalter AK, Collins AJ, Kane RL (2006) Cognitive impairment in hemodialysis patients is common. Neurology 67(2):216–223CrossRefPubMedGoogle Scholar
  27. Nakatani T, Naganuma T, Uchida J, Masuda C, Wada S, Sugimura T, Sugimura K (2003) Silent cerebral infarction in hemodialysis patients. Am J Nephrol 23(2):86–90CrossRefPubMedGoogle Scholar
  28. Ni L, Wen J, Zhang LJ, Zhu T, Qi R, Xu Q, Liang X, Zhong J, Zheng G, Lu GM (2014) Aberrant default-mode functional connectivity in patients with end-stage renal disease: a resting-state functional MR imaging study. Radiology 271(2):543–552CrossRefPubMedGoogle Scholar
  29. Nugent RA, Fathima SF, Feigl AB, Chyung D (2011) The burden of chronic kidney disease on developing nations: a 21st century challenge in global health. Nephron Clin Pract 118:c269–c277CrossRefPubMedGoogle Scholar
  30. Paulson OB, Parving HH, Olesen J, Skinhoj E (1973) Influence of carbon monoxide and of hemodilution on cerebral blood flow and blood gases in man. J Appl Physiol 35(1):111–116PubMedGoogle Scholar
  31. Pickett JL, Theberge DC, Brown WS, Schweitzer SU, Nissenson AR (1999) Normalizing hematocrit in dialysis patients improves brain function. Am J Kidney Dis 33(6):1122–1130CrossRefPubMedGoogle Scholar
  32. Prohovnik I, Post J, Uribarri J, Lee H, Sandu O, Langhoff E (2007) Cerebrovascular effects of hemodialysis in chronic kidney disease. J Cereb Blood Flow Metab 27(11):1861–1869CrossRefPubMedGoogle Scholar
  33. Radić J, Ljutić D, Radić M, Kovaĉić V, Sain M, Curković KD (2010) The possible impact of dialysis modality on cognitive function in chronic dialysis patients. Neth J Med 68(4):153–157PubMedGoogle Scholar
  34. Radić J, Ljutić D, Radić M, Kovačić V, Sain M, Dodig-Ćurković K (2011) Is there differences in cognitive and motor functioning between hemodialysis and peritoneal dialysis patients? Ren Fail 33(6):641–649CrossRefPubMedGoogle Scholar
  35. Seliger SL, Gillen DL, Longstreth WT Jr, Kestenbaum B, Stehman-Breen CO (2003) Elevated risk of stroke among patients with end-stage renal disease. Kidney Int 64(2):603–609CrossRefPubMedGoogle Scholar
  36. Temple RM, Deary IJ, Winney RJ (1995) Recombinant erythropoietin improves cognitive function in patients maintained on chronic ambulatory peritoneal dialysis. Nephrol Dial Transplant 10(9):1733–1738PubMedGoogle Scholar
  37. Tilki HE, Akpolat T, Tunali G, Kara A, Onar MK (2004) Effects of hemodialysis and continuous ambulatory peritoneal dialysis on P300 cognitive potentials in uraemic patients. Ups J Med Sci 109:43–48CrossRefPubMedGoogle Scholar
  38. Toyoda K, Fujii K, Fujimi S, Kumai Y, Tsuchimochi H, Ibayashi S, Iida M (2005) Stroke in patients on maintenance hemodialysis: a 22-year single-center study. Am J Kidney Dis 45(6):1058–1066CrossRefPubMedGoogle Scholar
  39. Venkateshappa C, Harish G, Mahadevan A, SrinivasBharath MM, Shankar SK (2012) Elevated oxidative stress and decreased antioxidant function in the human hippocampus and frontal cortex with increasing age: implications for neurodegeneration in Alzheimer’s disease. Neurochem Res 37(8):1601–1614CrossRefPubMedGoogle Scholar
  40. Vorstrup S, Lass P, Waldemar G, Brandi L, Schmidt JF, Johnsen A, Paulson OB (1992) Increased cerebral blood flow in anemic patients on long-term hemodialytic treatment. J Cereb Blood Flow Metab 12(5):745–749CrossRefPubMedGoogle Scholar
  41. Wang J, Zhang Y, Wolf RL, Roc AC, Alsop DC, Detre JA (2005) Amplitude modulated continuous arterial spin labeling perfusion MR with single coil at 3 T: feasibility study. Radiology 235(1):218–228CrossRefPubMedGoogle Scholar
  42. Wang HH, Hung SY, Sung JM, Hung KY, Wang JD (2014) Risk of stroke in long-term dialysis patients compared with the general population. Am J Kidney Dis 63(4):604–611CrossRefPubMedGoogle Scholar
  43. Wolcott DL, Wellisch DK, Marsh JT, Schaeffer J, Landsverk J, Nissenson AR (1988) Relationship of dialysis modality and other factors to cognitive function in chronic dialysis patients. Am J Kidney Dis 12:275–284CrossRefPubMedGoogle Scholar
  44. Yao Q, Zhang W, Qian J (2009) Dialysis status in China: a report from the Shanghai Dialysis Registry (2000–2005). Ethn Dis 19(1 Suppl 1):S1–23-26.Google Scholar
  45. Zhang LJ, Wen J, Ni L, Zhong J, Liang X, Zheng G, Lu GM (2013) Predominant gray matter volume loss in patients with end-stage renal disease: a voxel-based morphometry study. Metab Brain Dis 28(4):647–654CrossRefPubMedGoogle Scholar
  46. Zheng G, Wen J, Zhang L, Zhong J, Liang X, Ke W, Kong X, Zhao T, He Y, Zuo X, Luo S, Zhang LJ, Lu GM (2014) Altered brain functional connectivity in hemodialysis patients with end-stage renal disease: a resting-state functional MR imaging study. Metab Brain Dis 29(3):777–786CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Xiao Lu Jiang
    • 1
  • Ji Qiu Wen
    • 2
  • Long Jiang Zhang
    • 1
  • Gang Zheng
    • 1
    • 3
  • Xue Li
    • 2
  • Zhe Zhang
    • 2
  • Ya Liu
    • 1
    • 3
  • Li Juan Zheng
    • 1
  • Long Wu
    • 1
  • Hui Juan Chen
    • 1
  • Xiang Kong
    • 1
  • Song Luo
    • 1
  • Guang Ming Lu
    • 1
  • Xue Man Ji
    • 1
  • Zong Jun Zhang
    • 1
  1. 1.Department of Medical ImagingJingling Hospital, Medical School of Nanjing UniversityNanjingChina
  2. 2.National Clinical Research Center of Kidney DiseasesJingling Hospital, Medical School of Nanjing UniversityNanjingChina
  3. 3.College of Civil AviationNanjing University of Aeronautics and AstronauticsNanjingChina

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