Advertisement

European Radiology

, Volume 26, Issue 6, pp 1732–1741 | Cite as

Elevated global cerebral blood flow, oxygen extraction fraction and unchanged metabolic rate of oxygen in young adults with end-stage renal disease: an MRI study

  • Gang Zheng
  • Jiqiu Wen
  • Hanzhang Lu
  • Yaxian Lou
  • Zhiying Pan
  • Wei Liu
  • Hui Liu
  • Xue Li
  • Zhe Zhang
  • Huijuan Chen
  • Xiang Kong
  • Song Luo
  • Xiaolu Jiang
  • Ya Liu
  • Zongjun Zhang
  • Long Jiang ZhangEmail author
  • Guang Ming LuEmail author
Neuro

Abstract

Objectives

To noninvasively assess global cerebral blood flow (CBF), oxygen extraction fraction (OEF) and cerebral metabolic rate of oxygen (CMRO2) in young adults with end-stage renal disease (ESRD).

Methods

Thirty-six patients and 38 healthy volunteers were included and took part in MR examinations, blood and neuropsychological tests. CBF and OEF were measured by phase-contrast and T2-relaxation-under-spin-tagging MRI techniques, respectively. CMRO2 was computed from CBF, OEF and hematocrit according to Fick’s principle. Correlations were performed between MR measurements, blood biochemistry measurements and neuropsychological test scores.

Results

Compared with controls, ESRD patients had elevated CBF (72.9 ± 12.5 vs. 63.8 ± 8.5 ml min−1 100 g−1, P < 0.001), elevated OEF (47.2 ± 10.2 vs. 35.8 ± 5.4 %, P < 0.001), but unaffected CMRO2 (199.5 ± 36.4 vs. 193.8 ± 28.6 μmol O2 min−1 100 g−1, P = 0.879). Hematocrit negatively correlated with CBF (r = −0.640, P < 0.001) and OEF (r = −0.701, P < 0.001), but not with CMRO2. Altered neuropsychological test scores of ESRD patients were associated with OEF and CBF, but not with CMRO2. There were weak relationships between eGFR and hematocrit (r = 0.308, P = 0.068) or CBF (r = 0.318, P = 0.059).

Conclusion

Our findings suggested that anaemic young adults with ESRD may afford higher CBF and OEF to maintain a normal CMRO2. Despite this compensatory process, however, cognitive function was still impaired and its severity was correlated with their CBF and OEF abnormality.

Key Points

• Anaemic young adults with ESRD may afford higher CBF and OEF.

• Anaemic young adults with ESRD maintain a normal CMRO 2 .

• Cognitive function was still impaired in young ESRD adults.

• The severity of cognitive dysfunction correlated with CBF and OEF changes.

Keywords

End-stage renal disease Cerebral blood flow Oxygen extract fraction Cerebral metabolic rate of oxygen Uremic encephalopathy 

Abbreviations

CBF

Cerebral blood flow

CMRO2

Cerebral metabolic rate of oxygen

DST

Digit symbol test

ESRD

End-stage renal disease

LTT

Line-tracing test

MoCA

Montreal cognitive assessment

MMSE

Mini mental state examination

NCT-A

Number connection test type A

SAS

Self-rating anxiety scale

SDS

Self-rating depression scale

SDT

Serial-dotting test

TRUST

T2-relaxation-under-spin-tagging

OEF

Oxygen extraction fraction

Notes

Acknowledgments

The scientific guarantor of this publication is Guang Ming Lu. This study has received funding by grants from National Natural Science Foundation of China (grant Nos. 81471644 and 81101039 to G.Z., grants Nos. 81322020, 81230032, and 81171313 to L.J.Z.), the Program for New Century Excellent Talents in the University (NCET-12-0260 to L.J.Z.), and the Special Grant from the China Postdoctoral Science Foundation (grant No. 2014 T71014 to G.Z.). No complex statistical methods were necessary for this paper.

Institutional review board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. No study subjects or cohorts have been previously reported. Methodology:prospective, observable study, performed at one centre.

References

  1. 1.
    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 67:216–223CrossRefPubMedGoogle Scholar
  2. 2.
    Feng L, Yap KB, Ng TP (2013) Depressive symptoms in older adults with chronic kidney disease: mortality, quality of life outcomes, and correlates. Am J Geriatr Psychiatr 21:570–579CrossRefGoogle Scholar
  3. 3.
    United States Renal Data System (2014) 2014 annual data report: an overview of the epidemiology of kidney disease in the United States. National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, BethesdaGoogle Scholar
  4. 4.
    Liu ZH (2013) Nephrology in China. Nat Rev Nephrol 9:523–528CrossRefPubMedGoogle Scholar
  5. 5.
    Li LS (1996) End-stage renal disease in China. Kidney Int 49:287–301CrossRefPubMedGoogle Scholar
  6. 6.
    Mathew RJ, Rabin P, Stone WJ, Wilson WH (1985) Regional cerebral blood flow in dialysis encephalopathy and primary degenerative dementia. Kidney Int 28:64–68CrossRefPubMedGoogle Scholar
  7. 7.
    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 Physiol 262(5 Pt 2):F737–F743PubMedGoogle Scholar
  8. 8.
    Kanai H, Hirakata H, Nakane H, Fujii K, Hirakata E, Ibayashi S, Kuwabara Y (2001) Depressed cerebral oxygen metabolism in patients with chronic renal failure: a positron emission tomography study. Am J Kidney Dis 38(4 Suppl 1):S129–S133CrossRefPubMedGoogle Scholar
  9. 9.
    Papoiu AD, Emerson NM, Patel TS, Kraft RA, Valdes-Rodriguez R, Nattkemper LA, Coghill RC, Yosipovitch G (2014) Voxel-Based morphometry and arterial spin labeling fMRI reveal neuropathic and neuroplastic features of brain processing of itch in end-stage renal-disease. J Neurophysiol 112:1729–1738CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Farhoudi M, Abedi Azar S, Abdi R (2012) Brain hemodynamics in patients with end-stage renal disease between hemodialysis sessions. Iran J Kidney Dis 6:110–113PubMedGoogle Scholar
  11. 11.
    Lu H, Ge Y (2008) Quantitative evaluation of oxygenation in venous vessels using T2-relaxation-under-spin-tagging MRI. Magn Reson Med 60:357–363CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Lu H, Xu F, Grgac K, Liu P, Qin Q, van Zijl P (2012) Calibration and validation of TRUST MRI for the estimation of cerebral blood oxygenation. Magn Reson Med 67:42–49CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Xu F, Uh J, Liu P, Lu H (2012) On improving the speed and reliability of T2-relaxation-under-spin-tagging (TRUST) MRI. Magn Reson Med 68:198–204CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Liu P, Xu F, Lu H (2013) Test-retest reproducibility of a rapid method to measure brain oxygen metabolism. Magn Reson Med 69:675–681CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Bonomini M, Sirolli V (2003) Uremic toxicity and anemia. J Nephrol 16:21–28PubMedGoogle Scholar
  16. 16.
    Fisher JW (1980) Mechanism of the anemia of chronic renal failure. Nephron 25:106–111CrossRefPubMedGoogle Scholar
  17. 17.
    Rodriguez L, Tighiouart H, Scott T, Lou K, Giang L, Sorensen E, Weiner DE, Sarnak MJ (2013) Association of sleep disturbances with cognitive impairment and depression in maintenance hemodialysis patients. J Nephrol 26:101–110CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    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 28:647–654CrossRefPubMedGoogle Scholar
  19. 19.
    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 29:777–786CrossRefPubMedGoogle Scholar
  20. 20.
    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
  21. 21.
    Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state: a practical method for grading the cognitive state of patients for the clinicians. J Psychiatr Res 12:189–198CrossRefPubMedGoogle Scholar
  22. 22.
    Bossola M, Antocicco M, Di Stasio E, Ciciarelli C, Luciani G, Tazza L, Rosa F, Onder G (2011) Mini Mental State Examination over time in chronic hemodialysis patients. J Psychosom Res 71:50–54CrossRefPubMedGoogle Scholar
  23. 23.
    Murray AM, Knopman DS (2010) Cognitive impairment in CKD: no longer an occult burden. Am J Kidney Dis 56:615–618CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Martin SZ, Madai VI, von Samson-Himmelstjerna FC, Mutke MA, Bauer M, Herzig CX, Hetzer S, Günther M5, Sobesky J (2015) 3D GRASE pulsed arterial spin labeling at multiple inflow times in patients with long arterial transit times: comparison with dynamic susceptibility-weighted contrast-enhanced MRI at 3 Tesla. J Cereb Blood Flow Metab 35:392–401CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Fan AP, Benner T, Bolar DS, Rosen BR, Adalsteinsson E (2012) Phase-based regional oxygen metabolism (PROM) using MRI. Magn Reson Med 67:669–678CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Zheng G, Zhang LJ, Cao Y, Lu GM (2013) Venous blood ammonia can be associated with cerebral blood flow in hepatic encephalopathy. Hepatology 58:832–833CrossRefPubMedGoogle Scholar
  27. 27.
    Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K, Blei AT (2002) Hepatic encephalopathy– definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 35:716–721CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2015

Authors and Affiliations

  • Gang Zheng
    • 1
    • 2
  • Jiqiu Wen
    • 3
  • Hanzhang Lu
    • 4
  • Yaxian Lou
    • 1
    • 2
  • Zhiying Pan
    • 1
    • 2
  • Wei Liu
    • 5
  • Hui Liu
    • 6
  • Xue Li
    • 3
  • Zhe Zhang
    • 3
  • Huijuan Chen
    • 1
  • Xiang Kong
    • 1
  • Song Luo
    • 1
  • Xiaolu Jiang
    • 1
  • Ya Liu
    • 1
    • 2
  • Zongjun Zhang
    • 1
  • Long Jiang Zhang
    • 1
    Email author
  • Guang Ming Lu
    • 1
    Email author
  1. 1.Department of Medical Imaging, Jinling HospitalMedical School of Nanjing UniversityNanjingChina
  2. 2.College of Aivil AviationNanjing University of Aeronautics and AstronauticsNanjingChina
  3. 3.National Clinical Research Center of Kidney Diseases, Jinling HospitalMedical School of Nanjing UniversityNanjingChina
  4. 4.Advanced Imaging Research CenterUniversity of Texas Southwestern Medical CenterDallasUSA
  5. 5.Siemens Shenzhen Magnetic Resonance Ltd.ShenzhenChina
  6. 6.Siemens MR NEA Collaboration, Siemens Ltd.ShanghaiChina

Personalised recommendations