Skip to main content
Top
Published in: European Radiology 5/2021

01-05-2021 | Kidney Transplantation | Urogenital

Early detection of subclinical pathology in patients with stable kidney graft function by arterial spin labeling

Authors: Wei Wang, Yuanmeng Yu, Xue Li, Jinsong Chen, Yong Zhang, Longjiang Zhang, Jiqiu Wen

Published in: European Radiology | Issue 5/2021

Login to get access

Abstract

Objectives

To evaluate the utility of arterial spin labeling (ASL) for the identification of kidney allografts with underlying pathologies, particularly those with stable graft function.

Methods

A total of 75 patients, including 18 stable grafts with normal histology (normal group), 21 stable grafts with biopsy-proven pathology (subclinical pathology group), and 36 with unstable graft function (unstable graft group), were prospectively examined by ASL magnetic resonance imaging. Receiver operating characteristic curves were generated to calculate the area under the curve (AUC), sensitivity, and specificity.

Results

Patient demographics among the 3 groups were comparable. Compared with the normal group, kidney allograft cortical ASL values decreased in the subclinical pathology group and the unstable graft group (204.7 ± 44.9 ml/min/100 g vs 152.5 ± 38.9 ml/min/100 g vs 92.3 ± 37.4 ml/min/100 g, p < 0.001). The AUC, sensitivity, and specificity for discriminating allografts with pathologic changes from normal allografts were 0.92 (95% CI, 0.83–0.97), 71.9%, and 100% respectively by cortical ASL and 0.82 (95% CI, 0.72–0.90), 54.4%, and 100% respectively by serum creatinine. The cortical ASL identified allografts with subclinical pathology among patients with stable graft function with an AUC of 0.80 (95% CI, 0.64–0.91), sensitivity of 57.1%, and specificity of 88.9%. Combined use of proteinuria and cortical ASL could improve the sensitivity and specificity to 76.2% and 100% respectively for distinguishing the subclinical pathology group from the normal group.

Conclusions

Cortical ASL is useful for the identification of allografts with underlying pathologies. More importantly, ASL showed promise as a non-invasive tool for the clinical translation of identifying kidney allografts with subclinical pathology.

Key Points

• Cortical ASL values were decreased in kidney allografts with subclinical pathologic changes as compared with normal allografts (152.5 ± 38.9 ml/min/100 g vs 204.7 ± 44.9 ml/min/100 g, p < 0.001).
• Cortical ASL differentiated allografts with pathologic changes and subclinical pathology group from normal group with an AUC of 0.92 (95% CI, 0.83–0.97) and 0.80 (95% CI, 0.64–0.91) respectively.
• Cortical ASL discriminated allografts with underlying pathologic changes from normal allografts with a specificity of 100%, and combined use of proteinuria and cortical ASL values could also achieve 100% specificity for discriminating allografts with subclinical pathology from normal allografts.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kaballo MA, Canney M, O’Kelly P, Williams Y, O’Seaghdha CM, Conlon PJ (2018) A comparative analysis of survival of patients on dialysis and after kidney transplantation. Clin Kidney J 11:389–393CrossRef Kaballo MA, Canney M, O’Kelly P, Williams Y, O’Seaghdha CM, Conlon PJ (2018) A comparative analysis of survival of patients on dialysis and after kidney transplantation. Clin Kidney J 11:389–393CrossRef
2.
go back to reference Parajuli S, Joachim E, Alagusundaramoorthy S et al (2019) Subclinical antibody-mediated rejection after kidney transplantation: treatment outcomes. Transplantation 103:1722–1729CrossRef Parajuli S, Joachim E, Alagusundaramoorthy S et al (2019) Subclinical antibody-mediated rejection after kidney transplantation: treatment outcomes. Transplantation 103:1722–1729CrossRef
3.
go back to reference Moreso F, Ibernon M, Gomà M et al (2006) Subclinical rejection associated with chronic allograft nephropathy in protocol biopsies as a risk factor for late graft loss. Am J Transplant 6:747–752CrossRef Moreso F, Ibernon M, Gomà M et al (2006) Subclinical rejection associated with chronic allograft nephropathy in protocol biopsies as a risk factor for late graft loss. Am J Transplant 6:747–752CrossRef
4.
go back to reference Moledina DG, Luciano RL, Kukova L et al (2018) Kidney biopsy-related complications in hospitalized patients with acute kidney disease. Clin J Am Soc Nephrol 13:1633–1640CrossRef Moledina DG, Luciano RL, Kukova L et al (2018) Kidney biopsy-related complications in hospitalized patients with acute kidney disease. Clin J Am Soc Nephrol 13:1633–1640CrossRef
5.
go back to reference Odudu A, Nery F, Harteveld AA et al (2018) Arterial spin labelling MRI to measure renal perfusion: a systematic review and statement paper. Nephrol Dial Transplant 33:ii15–ii21CrossRef Odudu A, Nery F, Harteveld AA et al (2018) Arterial spin labelling MRI to measure renal perfusion: a systematic review and statement paper. Nephrol Dial Transplant 33:ii15–ii21CrossRef
6.
go back to reference Kim DW, Shim WH, Yoon SK et al (2017) Measurement of arterial transit time and renal blood flow using pseudocontinuous ASL MRI with multiple post-labeling delays: feasibility, reproducibility, and variation. J Magn Reson Imaging 46:813–819CrossRef Kim DW, Shim WH, Yoon SK et al (2017) Measurement of arterial transit time and renal blood flow using pseudocontinuous ASL MRI with multiple post-labeling delays: feasibility, reproducibility, and variation. J Magn Reson Imaging 46:813–819CrossRef
7.
go back to reference Ritt M, Janka R, Schneider MP et al (2010) Measurement of kidney perfusion by magnetic resonance imaging: comparison of MRI with arterial spin labeling to para-aminohippuric acid plasma clearance in male subjects with metabolic syndrome. Nephrol Dial Transplant 25:1126–1133CrossRef Ritt M, Janka R, Schneider MP et al (2010) Measurement of kidney perfusion by magnetic resonance imaging: comparison of MRI with arterial spin labeling to para-aminohippuric acid plasma clearance in male subjects with metabolic syndrome. Nephrol Dial Transplant 25:1126–1133CrossRef
8.
go back to reference Cai YZ, Li ZC, Zuo PL et al (2017) Diagnostic value of renal perfusion in patients with chronic kidney disease using 3D arterial spin labeling. J Magn Reson Imaging 46:589–594CrossRef Cai YZ, Li ZC, Zuo PL et al (2017) Diagnostic value of renal perfusion in patients with chronic kidney disease using 3D arterial spin labeling. J Magn Reson Imaging 46:589–594CrossRef
9.
go back to reference Hueper K, Gutberlet M, Rong S et al (2014) Acute kidney injury: arterial spin labeling to monitor renal perfusion impairment in mice-comparison with histopathologic results and renal function. Radiology 270:117–124CrossRef Hueper K, Gutberlet M, Rong S et al (2014) Acute kidney injury: arterial spin labeling to monitor renal perfusion impairment in mice-comparison with histopathologic results and renal function. Radiology 270:117–124CrossRef
10.
go back to reference Wiebe C, Gibson IW, Blydt-Hansen TD et al (2012) Evolution and clinical pathologic correlations of de novo donor-specific HLA antibody post kidney transplant. Am J Transplant 12:1157–1167CrossRef Wiebe C, Gibson IW, Blydt-Hansen TD et al (2012) Evolution and clinical pathologic correlations of de novo donor-specific HLA antibody post kidney transplant. Am J Transplant 12:1157–1167CrossRef
11.
go back to reference Levey AS, Stevens LA, Schmid CH et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612CrossRef Levey AS, Stevens LA, Schmid CH et al (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612CrossRef
12.
go back to reference Loupy A, Haas M, Solez K et al (2017) The Banff 2015 kidney meeting report: current challenges in rejection classification and prospects for adopting molecular pathology. Am J Transplant 17:28–41CrossRef Loupy A, Haas M, Solez K et al (2017) The Banff 2015 kidney meeting report: current challenges in rejection classification and prospects for adopting molecular pathology. Am J Transplant 17:28–41CrossRef
13.
go back to reference Ni X, Wang W, Li X et al (2020) Utility of diffusion-weighted imaging for guiding clinical management of patients with kidney transplant: a prospective study. J Magn Reson Imaging 52:565–574CrossRef Ni X, Wang W, Li X et al (2020) Utility of diffusion-weighted imaging for guiding clinical management of patients with kidney transplant: a prospective study. J Magn Reson Imaging 52:565–574CrossRef
14.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRef DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRef
15.
go back to reference Nery F, Buchanan CE, Harteveld AA et al (2020) Consensus-based technical recommendations for clinical translation of renal ASL MRI. MAGMA 33:141–161CrossRef Nery F, Buchanan CE, Harteveld AA et al (2020) Consensus-based technical recommendations for clinical translation of renal ASL MRI. MAGMA 33:141–161CrossRef
16.
go back to reference Zhang JL, Rusinek H, Chandarana H, Lee VS (2013) Functional MRI of the kidneys. J Magn Reson Imaging 37:282–293CrossRef Zhang JL, Rusinek H, Chandarana H, Lee VS (2013) Functional MRI of the kidneys. J Magn Reson Imaging 37:282–293CrossRef
17.
go back to reference Li LP, Tan H, Thacker JM et al (2017) Evaluation of renal blood flow in chronic kidney disease using arterial spin labeling perfusion magnetic resonance imaging. Kidney Int Rep 2:36–43CrossRef Li LP, Tan H, Thacker JM et al (2017) Evaluation of renal blood flow in chronic kidney disease using arterial spin labeling perfusion magnetic resonance imaging. Kidney Int Rep 2:36–43CrossRef
18.
go back to reference Artz NS, Sadowski EA, Wentland AL et al (2011) Arterial spin labeling MRI for assessment of perfusion in native and transplanted kidneys. Magn Reson Imaging 29:74–82CrossRef Artz NS, Sadowski EA, Wentland AL et al (2011) Arterial spin labeling MRI for assessment of perfusion in native and transplanted kidneys. Magn Reson Imaging 29:74–82CrossRef
19.
go back to reference Heusch P, Wittsack HJ, Blondin D et al (2014) Functional evaluation of transplanted kidneys using arterial spin labeling MRI. J Magn Reson Imaging 40:84–89CrossRef Heusch P, Wittsack HJ, Blondin D et al (2014) Functional evaluation of transplanted kidneys using arterial spin labeling MRI. J Magn Reson Imaging 40:84–89CrossRef
20.
go back to reference Ren T, Wen CL, Chen LH et al (2016) Evaluation of renal allografts function early after transplantation using intravoxel incoherent motion and arterial spin labeling MRI. Magn Reson Imaging 34:908–914CrossRef Ren T, Wen CL, Chen LH et al (2016) Evaluation of renal allografts function early after transplantation using intravoxel incoherent motion and arterial spin labeling MRI. Magn Reson Imaging 34:908–914CrossRef
21.
go back to reference Scholbach T, Wang HK, Yang AH, Loong CC, Wu TH (2013) Correlation of histopathologic and dynamic tissue perfusion measurement findings in transplanted kidneys. BMC Nephrol 14:143–152CrossRef Scholbach T, Wang HK, Yang AH, Loong CC, Wu TH (2013) Correlation of histopathologic and dynamic tissue perfusion measurement findings in transplanted kidneys. BMC Nephrol 14:143–152CrossRef
22.
go back to reference Hueper K, Schmidbauer M, Thorenz A et al (2017) Longitudinal evaluation of perfusion changes in acute and chronic renal allograft rejection using arterial spin labeling in translational mouse models. J Magn Reson Imaging 46:1664–1672CrossRef Hueper K, Schmidbauer M, Thorenz A et al (2017) Longitudinal evaluation of perfusion changes in acute and chronic renal allograft rejection using arterial spin labeling in translational mouse models. J Magn Reson Imaging 46:1664–1672CrossRef
23.
go back to reference Wang W, Yu Y, Wen J et al (2019) Combination of functional magnetic resonance imaging and histopathologic analysis to evaluate interstitial fibrosis in kidney allografts. Clin J Am Soc Nephrol 14:1372–1380CrossRef Wang W, Yu Y, Wen J et al (2019) Combination of functional magnetic resonance imaging and histopathologic analysis to evaluate interstitial fibrosis in kidney allografts. Clin J Am Soc Nephrol 14:1372–1380CrossRef
24.
go back to reference Prasad PV, Li LP, Thacker JM et al (2019) Cortical perfusion and tubular function as evaluated by magnetic resonance imaging correlates with annual loss in renal function in moderate chronic kidney disease. Am J Nephrol 49:114–124CrossRef Prasad PV, Li LP, Thacker JM et al (2019) Cortical perfusion and tubular function as evaluated by magnetic resonance imaging correlates with annual loss in renal function in moderate chronic kidney disease. Am J Nephrol 49:114–124CrossRef
25.
go back to reference Mora-Gutiérrez JM, Garcia-Fernandez N, Slon Roblero MF et al (2017) Arterial spin labeling MRI is able to detect early hemodynamic changes in diabetic nephropathy. J Magn Reson Imaging 46:1810–1817CrossRef Mora-Gutiérrez JM, Garcia-Fernandez N, Slon Roblero MF et al (2017) Arterial spin labeling MRI is able to detect early hemodynamic changes in diabetic nephropathy. J Magn Reson Imaging 46:1810–1817CrossRef
26.
go back to reference Nery F, De Vita E, Clark CA, Gordon I, Thomas DL (2019) Robust kidney perfusion mapping in pediatric chronic kidney disease using single-shot 3D-GRASE ASL with optimized retrospective motion correction. Magn Reson Med 81:2972–2984PubMed Nery F, De Vita E, Clark CA, Gordon I, Thomas DL (2019) Robust kidney perfusion mapping in pediatric chronic kidney disease using single-shot 3D-GRASE ASL with optimized retrospective motion correction. Magn Reson Med 81:2972–2984PubMed
27.
go back to reference Lanzman RS, Wittsack HJ, Martirosian P et al (2010) Quantification of renal allograft perfusion using arterial spin labeling MRI: initial results. Eur Radiol 20:1485–1491CrossRef Lanzman RS, Wittsack HJ, Martirosian P et al (2010) Quantification of renal allograft perfusion using arterial spin labeling MRI: initial results. Eur Radiol 20:1485–1491CrossRef
28.
go back to reference Hu G, Yang Z, Liang W et al (2019) Intravoxel incoherent motion and arterial spin labeling MRI analysis of reversible unilateral ureteral obstruction in rats. J Magn Reson Imaging 50:288–296CrossRef Hu G, Yang Z, Liang W et al (2019) Intravoxel incoherent motion and arterial spin labeling MRI analysis of reversible unilateral ureteral obstruction in rats. J Magn Reson Imaging 50:288–296CrossRef
29.
go back to reference Liang L, Chen WB, Chan KW et al (2016) Using intravoxel incoherent motion MR imaging to study the renal pathophysiological process of contrast-induced acute kidney injury in rats: comparison with conventional DWI and arterial spin labelling. Eur Radiol 26:1597–1605CrossRef Liang L, Chen WB, Chan KW et al (2016) Using intravoxel incoherent motion MR imaging to study the renal pathophysiological process of contrast-induced acute kidney injury in rats: comparison with conventional DWI and arterial spin labelling. Eur Radiol 26:1597–1605CrossRef
30.
go back to reference Zimmer F, Klotz S, Hoeger S et al (2017) Quantitative arterial spin labelling perfusion measurements in rat models of renal transplantation and acute kidney injury at 3 T. Z Med Phys 27:39–48CrossRef Zimmer F, Klotz S, Hoeger S et al (2017) Quantitative arterial spin labelling perfusion measurements in rat models of renal transplantation and acute kidney injury at 3 T. Z Med Phys 27:39–48CrossRef
31.
go back to reference Hueper K, Gueler F, Bräsen JH et al (2015) Functional MRI detects perfusion impairment in renal allografts with delayed graft function. Am J Physiol Renal Physiol 308:F1444–F1451CrossRef Hueper K, Gueler F, Bräsen JH et al (2015) Functional MRI detects perfusion impairment in renal allografts with delayed graft function. Am J Physiol Renal Physiol 308:F1444–F1451CrossRef
32.
go back to reference Hueper K, Hensen B, Gutberlet M et al (2016) Kidney transplantation: multiparametric functional magnetic resonance imaging for assessment of renal allograft pathophysiology in mice. Invest Radiol 51:58–65CrossRef Hueper K, Hensen B, Gutberlet M et al (2016) Kidney transplantation: multiparametric functional magnetic resonance imaging for assessment of renal allograft pathophysiology in mice. Invest Radiol 51:58–65CrossRef
33.
go back to reference Shirvani S, Tokarczuk P, Statton B et al (2019) Motion-corrected multiparametric renal arterial spin labelling at 3 T: reproducibility and effect of vasodilator challenge. Eur Radiol 29:232–240CrossRef Shirvani S, Tokarczuk P, Statton B et al (2019) Motion-corrected multiparametric renal arterial spin labelling at 3 T: reproducibility and effect of vasodilator challenge. Eur Radiol 29:232–240CrossRef
35.
go back to reference Edwards A, Silldforff EP, Pallone TL (2000) The renal medullary microcirculation. Front Biosci 5:E36–E52CrossRef Edwards A, Silldforff EP, Pallone TL (2000) The renal medullary microcirculation. Front Biosci 5:E36–E52CrossRef
Metadata
Title
Early detection of subclinical pathology in patients with stable kidney graft function by arterial spin labeling
Authors
Wei Wang
Yuanmeng Yu
Xue Li
Jinsong Chen
Yong Zhang
Longjiang Zhang
Jiqiu Wen
Publication date
01-05-2021
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 5/2021
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-020-07369-5

Other articles of this Issue 5/2021

European Radiology 5/2021 Go to the issue