Skip to main content
Top
Published in: BMC Nephrology 1/2018

Open Access 01-12-2018 | Technical advance

Blood oxygen level dependent magnetic resonance imaging for detecting pathological patterns in lupus nephritis patients: a preliminary study using a decision tree model

Authors: Huilan Shi, Junya Jia, Dong Li, Li Wei, Wenya Shang, Zhenfeng Zheng

Published in: BMC Nephrology | Issue 1/2018

Login to get access

Abstract

Background

Precise renal histopathological diagnosis will guide therapy strategy in patients with lupus nephritis. Blood oxygen level dependent (BOLD) magnetic resonance imaging (MRI) has been applicable noninvasive technique in renal disease. This current study was performed to explore whether BOLD MRI could contribute to diagnose renal pathological pattern.

Methods

Adult patients with lupus nephritis renal pathological diagnosis were recruited for this study. Renal biopsy tissues were assessed based on the lupus nephritis ISN/RPS 2003 classification. The Blood oxygen level dependent magnetic resonance imaging (BOLD-MRI) was used to obtain functional magnetic resonance parameter, R2* values. Several functions of R2* values were calculated and used to construct algorithmic models for renal pathological patterns. In addition, the algorithmic models were compared as to their diagnostic capability.

Results

Both Histopathology and BOLD MRI were used to examine a total of twelve patients. Renal pathological patterns included five classes III (including 3 as class III + V) and seven classes IV (including 4 as class IV + V). Three algorithmic models, including decision tree, line discriminant, and logistic regression, were constructed to distinguish the renal pathological pattern of class III and class IV. The sensitivity of the decision tree model was better than that of the line discriminant model (71.87% vs 59.48%, P < 0.001) and inferior to that of the Logistic regression model (71.87% vs 78.71%, P < 0.001). The specificity of decision tree model was equivalent to that of the line discriminant model (63.87% vs 63.73%, P = 0.939) and higher than that of the logistic regression model (63.87% vs 38.0%, P < 0.001). The Area under the ROC curve (AUROCC) of the decision tree model was greater than that of the line discriminant model (0.765 vs 0.629, P < 0.001) and logistic regression model (0.765 vs 0.662, P < 0.001).

Conclusions

BOLD MRI is a useful non-invasive imaging technique for the evaluation of lupus nephritis. Decision tree models constructed using functions of R2* values may facilitate the prediction of renal pathological patterns.
Appendix
Available only for authorised users
Literature
1.
go back to reference Austin HA 3rd, Boumpas DT, Vaughan EM, Balow JE. Predicting renal outcomes in severe lupus nephritis: contributions of clinical and histologic data. Kidney Int. 1994;45(2):544–50.CrossRefPubMed Austin HA 3rd, Boumpas DT, Vaughan EM, Balow JE. Predicting renal outcomes in severe lupus nephritis: contributions of clinical and histologic data. Kidney Int. 1994;45(2):544–50.CrossRefPubMed
2.
go back to reference Bihl GR, Petri M, Fine DM. Kidney biopsy in lupus nephritis: look before you leap. Nephrol Dial Transplant. 2006;21(7):1749–52.CrossRefPubMed Bihl GR, Petri M, Fine DM. Kidney biopsy in lupus nephritis: look before you leap. Nephrol Dial Transplant. 2006;21(7):1749–52.CrossRefPubMed
3.
go back to reference Malvezzi P, Bricault I, Terrier N, Bayle F. Evaluation of intrarenal oxygenation by blood oxygen level-dependent magnetic resonance imaging in living kidney donors and their recipients: preliminary results. Transplant Proc. 2009;41(2):641–4.CrossRefPubMed Malvezzi P, Bricault I, Terrier N, Bayle F. Evaluation of intrarenal oxygenation by blood oxygen level-dependent magnetic resonance imaging in living kidney donors and their recipients: preliminary results. Transplant Proc. 2009;41(2):641–4.CrossRefPubMed
4.
go back to reference Chandarana H, Lee VS. Renal functional MRI: are we ready for clinical application? AJR Am J Roentgenol. 2009;192(6):1550–7.CrossRefPubMed Chandarana H, Lee VS. Renal functional MRI: are we ready for clinical application? AJR Am J Roentgenol. 2009;192(6):1550–7.CrossRefPubMed
5.
go back to reference Herget-Rosenthal S. Imaging techniques in the management of chronic kidney disease: current developments and future perspectives. Semin Nephrol. 2011;31(3):283–90.CrossRefPubMed Herget-Rosenthal S. Imaging techniques in the management of chronic kidney disease: current developments and future perspectives. Semin Nephrol. 2011;31(3):283–90.CrossRefPubMed
6.
go back to reference Ebrahimi B, Textor SC, Lerman LO. Renal relevant radiology: renal functional magnetic resonance imaging. Clin J Am Soc Nephrol. 2014;9(2):395–405.CrossRefPubMed Ebrahimi B, Textor SC, Lerman LO. Renal relevant radiology: renal functional magnetic resonance imaging. Clin J Am Soc Nephrol. 2014;9(2):395–405.CrossRefPubMed
7.
go back to reference Prasad PV, Edelman RR, Epstein FH. Noninvasive evaluation of intrarenal oxygenation with BOLD MRI. Circulation. 1996;94(12):3271–5.CrossRefPubMed Prasad PV, Edelman RR, Epstein FH. Noninvasive evaluation of intrarenal oxygenation with BOLD MRI. Circulation. 1996;94(12):3271–5.CrossRefPubMed
8.
go back to reference Chrysochou C, Mendichovszky IA, Buckley DL, Cheung CM, Jackson A, Kalra PA. BOLD imaging: a potential predictive biomarker of renal functional outcome following revascularization in atheromatous renovascular disease. Nephrol Dial Transplant. 2012;27(3):1013–9.CrossRefPubMed Chrysochou C, Mendichovszky IA, Buckley DL, Cheung CM, Jackson A, Kalra PA. BOLD imaging: a potential predictive biomarker of renal functional outcome following revascularization in atheromatous renovascular disease. Nephrol Dial Transplant. 2012;27(3):1013–9.CrossRefPubMed
9.
go back to reference Thoeny HC, Kessler TM, Simon-Zoula S, De Keyzer F, Mohaupt M, Studer UE, Vermathen P. Renal oxygenation changes during acute unilateral ureteral obstruction: assessment with blood oxygen level-dependent mr imaging--initial experience. Radiology. 2008;247(3):754–61.CrossRefPubMed Thoeny HC, Kessler TM, Simon-Zoula S, De Keyzer F, Mohaupt M, Studer UE, Vermathen P. Renal oxygenation changes during acute unilateral ureteral obstruction: assessment with blood oxygen level-dependent mr imaging--initial experience. Radiology. 2008;247(3):754–61.CrossRefPubMed
10.
go back to reference Wang ZJ, Kumar R, Banerjee S, Hsu CY. Blood oxygen level-dependent (BOLD) MRI of diabetic nephropathy: preliminary experience. J Magn Reson Imaging. 2011;33(3):655–60.CrossRefPubMedPubMedCentral Wang ZJ, Kumar R, Banerjee S, Hsu CY. Blood oxygen level-dependent (BOLD) MRI of diabetic nephropathy: preliminary experience. J Magn Reson Imaging. 2011;33(3):655–60.CrossRefPubMedPubMedCentral
11.
go back to reference Pruijm M, Hofmann L, Zanchi A, Maillard M, Forni V, Muller ME, Wuerzner G, Vogt B, Stuber M, Burnier M. 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. 2013;99(2):136–44.CrossRefPubMed Pruijm M, Hofmann L, Zanchi A, Maillard M, Forni V, Muller ME, Wuerzner G, Vogt B, Stuber M, Burnier M. 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. 2013;99(2):136–44.CrossRefPubMed
12.
go back to reference Park SY, Kim CK, Park BK, Huh W, Kim SJ, Kim B. Evaluation of transplanted kidneys using blood oxygenation level-dependent MRI at 3 T: a preliminary study. AJR Am J Roentgenol. 2013;198(5):1108–14.CrossRef Park SY, Kim CK, Park BK, Huh W, Kim SJ, Kim B. Evaluation of transplanted kidneys using blood oxygenation level-dependent MRI at 3 T: a preliminary study. AJR Am J Roentgenol. 2013;198(5):1108–14.CrossRef
13.
go back to reference Khatir DS, Pedersen M, Jespersen B, Buus NH. Reproducibility of MRI renal artery blood flow and BOLD measurements in patients with chronic kidney disease and healthy controls. J Magn Reson Imaging. 2014;40(5):1091–8.CrossRefPubMed Khatir DS, Pedersen M, Jespersen B, Buus NH. Reproducibility of MRI renal artery blood flow and BOLD measurements in patients with chronic kidney disease and healthy controls. J Magn Reson Imaging. 2014;40(5):1091–8.CrossRefPubMed
14.
go back to reference Xin-Long P, Jing-Xia X, Jian-Yu L, Song W, Xin-Kui T. A preliminary study of blood-oxygen-level-dependent MRI in patients with chronic kidney disease. Magn Reson Imaging. 2012;30(3):330–5.CrossRefPubMed Xin-Long P, Jing-Xia X, Jian-Yu L, Song W, Xin-Kui T. A preliminary study of blood-oxygen-level-dependent MRI in patients with chronic kidney disease. Magn Reson Imaging. 2012;30(3):330–5.CrossRefPubMed
15.
go back to reference Petri M, Orbai AM, Alarcón GS, Gordon C, Merrill JT, Fortin PR, Bruce IN, Isenberg D, Wallace DJ, Nived O, et al. Derivation and validation of the systemic lupus international collaborating clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 2012;64(8):2677–86.CrossRefPubMedPubMedCentral Petri M, Orbai AM, Alarcón GS, Gordon C, Merrill JT, Fortin PR, Bruce IN, Isenberg D, Wallace DJ, Nived O, et al. Derivation and validation of the systemic lupus international collaborating clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 2012;64(8):2677–86.CrossRefPubMedPubMedCentral
16.
go back to reference Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH. Derivation of the SLEDAI. A disease activity index for lupus patients. Arthritis Rheum. 1992;35(6):630–40.CrossRefPubMed Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH. Derivation of the SLEDAI. A disease activity index for lupus patients. Arthritis Rheum. 1992;35(6):630–40.CrossRefPubMed
17.
go back to reference Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150(9):604–12.CrossRefPubMedPubMedCentral Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150(9):604–12.CrossRefPubMedPubMedCentral
18.
go back to reference Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol. 2004;15(2):241–50.CrossRefPubMed Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol. 2004;15(2):241–50.CrossRefPubMed
19.
go back to reference Austin HA 3rd, Muenz LR, Joyce KM, Antonovych TT, Balow JE. Diffuse proliferative lupus nephritis: identification of specific pathologic features affecting renal outcome. Kidney Int. 1984;25(4):689–95.CrossRefPubMed Austin HA 3rd, Muenz LR, Joyce KM, Antonovych TT, Balow JE. Diffuse proliferative lupus nephritis: identification of specific pathologic features affecting renal outcome. Kidney Int. 1984;25(4):689–95.CrossRefPubMed
20.
go back to reference Marshall RJ. The use of classification and regression trees in clinical epidemiology. J Clin Epidemiol. 2001;54(6):603–9.CrossRefPubMed Marshall RJ. The use of classification and regression trees in clinical epidemiology. J Clin Epidemiol. 2001;54(6):603–9.CrossRefPubMed
21.
go back to reference Fisher RA. The use of multiple measurements in taxonomic problems. Ann Eugenics. 1936;7:179–88.CrossRef Fisher RA. The use of multiple measurements in taxonomic problems. Ann Eugenics. 1936;7:179–88.CrossRef
22.
go back to reference Rao CR. The utilization of multiple measurements in problems of biological classification. J Royal Stat Soc SerB (Methodological). 1948;10:159–203. Rao CR. The utilization of multiple measurements in problems of biological classification. J Royal Stat Soc SerB (Methodological). 1948;10:159–203.
23.
go back to reference Alkarkhi AF, Easa AM. Comparing discriminant analysis and logistic regression model as a statistical assessment tools of arsenic and heavy metal contents in cockles. J Sustainable Dev. 2008;1:102–6. Alkarkhi AF, Easa AM. Comparing discriminant analysis and logistic regression model as a statistical assessment tools of arsenic and heavy metal contents in cockles. J Sustainable Dev. 2008;1:102–6.
24.
go back to reference Podgorelec V, Kokol P, Stiglic B, Rozman I. Decision trees: an overview and their use in medicine. J Med Syst. 2002;26(5):445–63.CrossRefPubMed Podgorelec V, Kokol P, Stiglic B, Rozman I. Decision trees: an overview and their use in medicine. J Med Syst. 2002;26(5):445–63.CrossRefPubMed
25.
go back to reference Gloviczki ML, Glockner JF, Lerman LO, McKusick MA, Misra S, Grande JP, Textor SC. Preserved oxygenation despite reduced blood flow in poststenotic kidneys in human atherosclerotic renal artery stenosis. Hypertension. 2010;55(4):961–6.CrossRefPubMedPubMedCentral Gloviczki ML, Glockner JF, Lerman LO, McKusick MA, Misra S, Grande JP, Textor SC. Preserved oxygenation despite reduced blood flow in poststenotic kidneys in human atherosclerotic renal artery stenosis. Hypertension. 2010;55(4):961–6.CrossRefPubMedPubMedCentral
26.
go back to reference Vermathen P, Binser T, Boesch C, Eisenberger U, Thoeny HC. Three-year follow-up of human transplanted kidneys by diffusion-weighted MRI and blood oxygenation level-dependent imaging. J Magn Reson Imaging. 2012;35(5):1133–8.CrossRefPubMed Vermathen P, Binser T, Boesch C, Eisenberger U, Thoeny HC. Three-year follow-up of human transplanted kidneys by diffusion-weighted MRI and blood oxygenation level-dependent imaging. J Magn Reson Imaging. 2012;35(5):1133–8.CrossRefPubMed
27.
go back to reference Li X, Xu X, Zhang Q, Ren H, Zhang W, Liu Y, Yan F, Chen N. Diffusion weighted imaging and blood oxygen level-dependent MR imaging of kidneys in patients with lupus nephritis. J Transl Med. 2014;12:295.CrossRefPubMedPubMedCentral Li X, Xu X, Zhang Q, Ren H, Zhang W, Liu Y, Yan F, Chen N. Diffusion weighted imaging and blood oxygen level-dependent MR imaging of kidneys in patients with lupus nephritis. J Transl Med. 2014;12:295.CrossRefPubMedPubMedCentral
28.
go back to reference O'Connor PM. Renal oxygen delivery: matching delivery to metabolic demand. Clin Exp Pharmacol Physiol. 2006;33(10):961–7.CrossRefPubMed O'Connor PM. Renal oxygen delivery: matching delivery to metabolic demand. Clin Exp Pharmacol Physiol. 2006;33(10):961–7.CrossRefPubMed
29.
go back to reference Gloviczki ML, Glockner J, Gomez SI, Romero JC, Lerman LO, McKusick M, Textor SC. Comparison of 1.5 and 3 T BOLD MR to study oxygenation of kidney cortex and medulla in human renovascular disease. Investig Radiol. 2009;44(9):566–71.CrossRef Gloviczki ML, Glockner J, Gomez SI, Romero JC, Lerman LO, McKusick M, Textor SC. Comparison of 1.5 and 3 T BOLD MR to study oxygenation of kidney cortex and medulla in human renovascular disease. Investig Radiol. 2009;44(9):566–71.CrossRef
30.
go back to reference Lübbers DW, Baumgärtl H. Heterogeneities and profiles of oxygen pressure in brain and kidney as examples of the pO2 distribution in the living tissue. Kidney Int. 1997;51(2):372–80.CrossRefPubMed Lübbers DW, Baumgärtl H. Heterogeneities and profiles of oxygen pressure in brain and kidney as examples of the pO2 distribution in the living tissue. Kidney Int. 1997;51(2):372–80.CrossRefPubMed
31.
go back to reference Ebrahimi B, Gloviczki M, Woollard JR, Crane JA, Textor SC, Lerman LO. Compartmental analysis of renal BOLD MRI data: introduction and validation. Investig Radiol. 2012;47(3):175–82. Ebrahimi B, Gloviczki M, Woollard JR, Crane JA, Textor SC, Lerman LO. Compartmental analysis of renal BOLD MRI data: introduction and validation. Investig Radiol. 2012;47(3):175–82.
32.
go back to reference Rezaei-Darzi E, Farzadfar F, Hashemi-Meshkini A, Navidi I, Mahmoudi M, Varmaghani M, Mehdipour P, Soudi Alamdari M, Tayefi B, Naderimagham S, et al. Comparison of two data mining techniques in labeling diagnosis to Iranian pharmacy claim dataset: artificial neural network (ANN) versus decision tree model. Arch Iran Med. 2014;17(12):837–43.PubMed Rezaei-Darzi E, Farzadfar F, Hashemi-Meshkini A, Navidi I, Mahmoudi M, Varmaghani M, Mehdipour P, Soudi Alamdari M, Tayefi B, Naderimagham S, et al. Comparison of two data mining techniques in labeling diagnosis to Iranian pharmacy claim dataset: artificial neural network (ANN) versus decision tree model. Arch Iran Med. 2014;17(12):837–43.PubMed
33.
go back to reference Gladman DD, Ibanez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol. 2002;29(2):288–91.PubMed Gladman DD, Ibanez D, Urowitz MB. Systemic lupus erythematosus disease activity index 2000. J Rheumatol. 2002;29(2):288–91.PubMed
34.
go back to reference Yee CS, Farewell V, Isenberg DA, Prabu A, Sokoll K, Teh LS, Rahman A, Bruce IN, Griffiths B, Akil M, et al. Revised British isles lupus assessment group 2004 index: a reliable tool for assessment of systemic lupus erythematosus activity. Arthritis Rheum. 2006;54(10):3300–5.CrossRefPubMed Yee CS, Farewell V, Isenberg DA, Prabu A, Sokoll K, Teh LS, Rahman A, Bruce IN, Griffiths B, Akil M, et al. Revised British isles lupus assessment group 2004 index: a reliable tool for assessment of systemic lupus erythematosus activity. Arthritis Rheum. 2006;54(10):3300–5.CrossRefPubMed
35.
go back to reference Yu F, Wu LH, Tan Y, Li LH, Wang CL, Wang WK, Qu Z, Chen MH, Gao JJ, Li ZY, et al. Tubulointerstitial lesions of patients with lupus nephritis classified by the 2003 International Society of Nephrology and Renal Pathology Society system. Kidney Int. 2010;77(9):820–9.CrossRefPubMed Yu F, Wu LH, Tan Y, Li LH, Wang CL, Wang WK, Qu Z, Chen MH, Gao JJ, Li ZY, et al. Tubulointerstitial lesions of patients with lupus nephritis classified by the 2003 International Society of Nephrology and Renal Pathology Society system. Kidney Int. 2010;77(9):820–9.CrossRefPubMed
36.
go back to reference Bao H, Liu ZH, Xie HL, Hu WX, Zhang HT, Li LS. Successful treatment of class V+IV lupus nephritis with multitarget therapy. J Am Soc Nephrol : JASN. 2008;19(10):2001–10.CrossRefPubMedPubMedCentral Bao H, Liu ZH, Xie HL, Hu WX, Zhang HT, Li LS. Successful treatment of class V+IV lupus nephritis with multitarget therapy. J Am Soc Nephrol : JASN. 2008;19(10):2001–10.CrossRefPubMedPubMedCentral
37.
go back to reference Greloni G, Scolnik M, Marin J, Lancioni E, Quiroz C, Zacariaz J, De la Iglesia NP, Christiansen S, Pierangelo MA, Varela CF, et al. Value of repeat biopsy in lupus nephritis flares. Lupus Sci Med. 2014;1(1):e000004.CrossRefPubMedPubMedCentral Greloni G, Scolnik M, Marin J, Lancioni E, Quiroz C, Zacariaz J, De la Iglesia NP, Christiansen S, Pierangelo MA, Varela CF, et al. Value of repeat biopsy in lupus nephritis flares. Lupus Sci Med. 2014;1(1):e000004.CrossRefPubMedPubMedCentral
38.
go back to reference Shi H, Yan T, Li D, Jia J, Shang W, Wei L, Zheng Z. Detection of renal hypoxia in lupus nephritis using blood oxygen level-dependent MR imaging: a multiple correspondence analysis. Kidney Blood Press Res. 2017;42(1):123–35.CrossRefPubMed Shi H, Yan T, Li D, Jia J, Shang W, Wei L, Zheng Z. Detection of renal hypoxia in lupus nephritis using blood oxygen level-dependent MR imaging: a multiple correspondence analysis. Kidney Blood Press Res. 2017;42(1):123–35.CrossRefPubMed
39.
go back to reference Inoue T, Kozawa E, Okada H, Inukai K, Watanabe S, Kikuta T, Watanabe Y, Takenaka T, Katayama S, Tanaka J, et al. Noninvasive evaluation of kidney hypoxia and fibrosis using magnetic resonance imaging. J Am Soc Nephrol : JASN. 2011;22(8):1429–34.CrossRefPubMedPubMedCentral Inoue T, Kozawa E, Okada H, Inukai K, Watanabe S, Kikuta T, Watanabe Y, Takenaka T, Katayama S, Tanaka J, et al. Noninvasive evaluation of kidney hypoxia and fibrosis using magnetic resonance imaging. J Am Soc Nephrol : JASN. 2011;22(8):1429–34.CrossRefPubMedPubMedCentral
Metadata
Title
Blood oxygen level dependent magnetic resonance imaging for detecting pathological patterns in lupus nephritis patients: a preliminary study using a decision tree model
Authors
Huilan Shi
Junya Jia
Dong Li
Li Wei
Wenya Shang
Zhenfeng Zheng
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Nephrology / Issue 1/2018
Electronic ISSN: 1471-2369
DOI
https://doi.org/10.1186/s12882-017-0787-z

Other articles of this Issue 1/2018

BMC Nephrology 1/2018 Go to the issue