The role of kidney diffusion tensor magnetic resonance ... · Original Article The role of kidney diffusion tensor magnetic resonance imaging in children Mehmet Burak Özkana,⇑,

The Egyptian Journal of Radiology and Nuclear Medicine 47 (2016) 1599–1611

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Original Article

The role of kidney diffusion tensor magnetic resonance imagingin children

http://dx.doi.org/10.1016/j.ejrnm.2016.08.0150378-603X/� 2016 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier.This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine.⇑ Corresponding author.

E-mail addresses: [email protected] (M.B. Özkan), [email protected] (R. Marterer), [email protected] (S. Tscheuner), oeblecom (U.M. Yildirim), [email protected] (E. Ozkan).

Mehmet Burak Özkan a,⇑, Robert Marterer b, Sebastian Tscheuner b, Utku Mahir Yildirim c,Elif Ozkan d

aDepartment of Pediatric Radiology, Dr. Sami Ulus Research and Training Hospital, Altindag, Ankara, TurkeybDepartment of Pediatric Radiology, Graz, AustriacDepartment of Radiology, Medikal Park Hospital, _Izmir, TurkeydDepartment of Pediatrics, Sami Ulus Hospital, Ankara, Turkey

a r t i c l e i n f o

Article history:Received 4 April 2016Accepted 19 August 2016Available online 28 September 2016

Keywords:Renal DTIPediatriceGFRRenal insufficiencyRadiology

a b s t r a c t

Background: Diffusion tensor imaging (DTI) in magnetic resonance imaging (MRI) providesinformation about the microstructure of renal tissue and is becoming increasingly useful inthe evaluation of relationship between renal structure and function.Objectives: To investigate, whether DTI allows assessment of renal impairment and pathol-ogy in pediatric patients with decreased renal functions.Materials and methods: Thirty-two pediatric patients and seventeen healthy children wereincluded in this prospective study. For DTI, a respiratory-triggered coronal echo planarimaging (EPI) sequence was performed. Cortical and medullary mean axial and radial dif-fusivity and fractional anisotropy (FA) were analyzed.Results: In healthy subjects, the cortical FA values were significantly lower than the medul-lary FA values (p < 0.001). Cortical and medullary ADC values showed positive correlations(r = 0.499, p = 0.041) and a negative correlation with cortical FA values(r = �0.533,p = 0.028). The eGFR values were negatively correlated with the medullary ADC values(r = �0.484, p = 0.049) in healthy subjects and positively correlated with the k medullaryvalues (r = 0.385, p = 0.027). Additionally in the patient group, the age was positively cor-related with FA cortex values (r = 0.411, p = 0.018) and with the medullary ADC values(r = 0.461, p = 0.007). However, the medullary FA values were negatively correlated withthe medullary ADC values (r = �0.363, p = 0.038). Tractography of healthy volunteersshowed a radial arrangement which converged into the pyramids, whereas renal insuffi-ciency patients had irregular arrangement patterns and architectural distortions in theobserved areas.Conclusions: Renal DTI is a promising diagnostic tool in the assessment of microstructuralrenal changes and correlates with the eGFR. Therefore, it is possible to estimate thearrangement of the tracks which emanate from the renal medulla. Furthermore, diffusionof the water molecules could be carried out. This study demonstrates the usage of DTI inrenal pediatric kidneys. Validations in larger cohort groups with histopathological biopsiesare needed.� 2016 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting byElsevier. This is an open access article under the CC BY-NC-ND license (http://creativecom-

mons.org/licenses/by-nc-nd/4.0/).

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1. Introduction

The major function of the kidneys is to balance thewater and solute concentration. Kidneys do this physiolog-ically by the help of glomeruli and tubules, which enablefiltration and reabsorption of water and solutes [1–4].Understanding the basic mechanisms of water diffusionin the kidneys could help to improve the understandingof kidney pathologies. Laboratory parameters, such asserum creatinine or estimated glomerular filtration rate(eGFR), are commonly used for the evaluation of renaltubular function [5–7].

Diffusion weighted imaging (DWI) visualizes watermotion at the molecular level and provides useful informa-tion on parenchyma microstructure and function, basicallydepending on the Brownian motion [5–7]. The apparentdiffusion coefficient (ADC) is a quantitative parameter cal-culated from DWI [1]. It was shown that ADC values tendto decrease in chronic kidney diseases, depending uponthe degree of renal impairment [5,8].

Kidneys have a well-defined anatomical structure withtubules, collecting ducts and vessels radially orientedtoward the pelvis and in which molecules move in a pref-erential direction [9,10]. To investigate molecular diffusionin kidneys, the direction should be evaluated. In healthykidney vessels, tubules and collecting ducts are involvedin water reabsorption and urine formation. These struc-tures have a highly perfectly organized radial arrangement.This kind of arrangement enables motion of water mole-cules to move in different directions, such as right to leftor superior to inferior. Therefore, this is the reason forthe anisotropic manner of the molecular diffusion in renalparenchyma [9]. This highly perfectly designed structuralorganization gets damaged in pathological processes. Thisrelationship was demonstrated by previous studies[5,6,9,11].

DTI enables to measure the diffusion of the water mole-cules in at least six vectoral ways. The diffusion anisotropycould be used to understand the microstructure of therenal parenchyma. The fractional anisotropy (FA) describesthe degree of anisotropy of a diffusion process whereasADC describes only the averaged diffusivity in the direc-tional way. Therefore, DTI enables to estimate and to mea-sure the vectoral way of least restricted diffusion [3,12,13].

In the literature, the correlation between age-dependent changes and the ability of DTI to estimate renaltissue injuries due to tumors, pyelonephritis and renalartery stenosis was demonstrated. Additionally, it isknown that the renal medulla has higher FA values thanthe cortex [5,9,14].

Studies in adults have demonstrated the ability to showmicrostructural changes correlating with functionalparameters by utilizing DTI [3,4,9,15–16]. This prospectivestudy’s purpose was to examine the value of renal DTI inchildren and adolescents.

2. Material and methods

Divided into two cohorts (normal eGFR of P60 ml/min/1.73 m2, and reduced eGFR between P25 ml/

min/1.73 m2 and <60 ml/min/1.73 m2), a total of 50 chil-dren were included in this prospective single center study.A healthy control group consisted of 17 volunteers, thestudy group of 33 children. The control group consistedof nine males and eight females with a mean age of8 ± 0.9 years (3.09–14.7 years). The mean age in the studygroup was 8.5 years ± 0.7 years (3.02–15.3 years), consist-ing of 20 male and 12 female children. One patient hadto be excluded from this study group, as corticomedullarydifferentiation (CMD) had not been reported.

All of them underwent renal DTI, as further described inthe renal MRI acquisition section. The duration of the studywas one and half year. To be certain about the absence ofrenal parenchymal disease, volunteer patients additionallyunderwent a renal ultrasound examination.

Exclusion criteria were MRI contraindications such asferromagnetic implants or claustrophobia. Because of apossible risk of nephrogenic systemic fibrosis [17], patientswith GFRs lower than 25 were not included in the study.

The dimensions and corticomedullar differentiationwere controlled before the renal MRI examination. All thevalues regarding these parameters were within normalvalues. Regarding the b:0 image values differentiationbetween the cortex and the medulla could be easily evalu-ated and able to be understood the object regions andedges.

A study group sub-group, representing patients withrenal impairment (eGFRP 25 and equal or lower 40),was defined. eGFRs were calculated from serum creatininemeasurements for all subjects based on the revisedSchwarz formula for children and adolescent [18]. Thepatients were sedated under the age of eight. They weresedated by local anesthesiological products.

The study was approved by the institutional reviewboard and written consent was obtained from the parentsof all children.

3. Renal MRI acquisition

All subjects were scanned in supine position in anAvanto 1.5 T (T) MRI scanner (Siemens Medical Systems,Erlangen, Germany). Spine array (posterior) and body array(anterior) receiver coils were used to maximize image uni-formity. The imaging protocol consisted of a respiratory-gated (axial 2D, 3D) echo-planar fast spin echo sequence(HASTE) and a coronal T2-weighted sequence. After theHASTE sequence, a respiratory-gated, single-shot diffusiontensor imaging – echo planar imaging (DTI-EPI) acquisitionwas performed on one kidney (b = 0 and 400 s/mm2, 6directions + null, TR/TE = 2000 ms/75 ms, imaging slice thick-ness = 3 mm, 10 imaging slices/subject). In order to achievea better resolution and higher SNR values, either the leftor right kidney was evaluated. Only single renal evaluationwas enough for the determination.

In all children diffusion MR images were acquired priorto the administration of gadolinium. As a routine part ofthis renal MRI imaging, we had to use the gadoliniumadministration in order to get the sufficient renal diagnosisexcept those under eGFR under 25. Although we had to usegadolinium as a part of imaging technique, the renal DTIwas evaluated separately in another work station and the

M.B. Özkan et al. / The Egyptian Journal of Radiology and Nuclear Medicine 47 (2016) 1599–1611 1601

renal MRI determination did not affect the renal DTIresults.

4. Imaging post-processing

Image post-processing was performed with DiffusionToolkit software package (www.trackvis.org, version 0.5).

Fig. 1a. Shows the descriptive charac

Fig. 1b. Demonstrates the correlations of par

Tractography was reconstructed using a deterministicstreamline algorithm. This algorithm was based on auser-defined region of interest. To be continuous andhomogenous within the previous studies, thresholds wereset for minimum fractional anisotropy (FA). A region ofinterest (ROI) analysis of the ADC and FA maps was per-formed to obtain measures of mean cortical and medullary

teristics of healthy volunteers.

ameters that are statically significant.

http://www.trackvis.org

Fig. 2. (a) Shows the correlations of parameters in the study group patients.

Fig. 2 (continued)


ADC and FA for each subject. At least three coronal imageslices in proximity to the renal hilum were selected forthe ROI analysis. Medullary and cortical ROI selectionswere obtained in the HASTE images with high cor-ticomedullary contrast and high anatomical detail. The ROIsselected in the HASTE images were directly applied to the cor-

responding (and co-registered) ADC and FA maps to obtaincortical and medullary ADC and FA values. Afterward, themean of all resulting ADC and FA values was calculated. A Dif-fusion Ellipsoid is completely represented by the DiffusionTensor, D. FA is calculated from the eigenvalues (k k1, k 2, kk3) of the diffusion tensors [1] The eigenvectors (�) give the

Fig. 2 (continued)

Table 1aThe DTI results of t-test for the healthy group.

Paired samples test tPaired differences

Mean Std. deviation Std. error mean 95% confidence interval of thedifference

Lower Upper

Pair 1 medullarFA - adcmedulla �1.646212 0.045.584 0.007935 �1.662375 �1.630049 �207.460

Pair 2 facortex - adccortex �1.993091 0.094447 0.016441 �2.026580 �1.959602 �121.226

Pair 3 k1korteks - k1medulla 0.823939 0.137862 0.023999 0.775056 0.872823 34.333



Pair 6 facortex - medullarFA �0.235364 0.023817 0.004146 �0.243809 �0.226919 �56.769

df Sig. (2-tailed)Pair 1 medullarFA - adcmedulla 32 0.000

Pair 2 facortex - adccortex 32 0.000

Pair 3 k1korteks - k1medulla 32 0.000



Pair 6 facortex - medullarFA 32 0.000


directions in which the ellipsoid has major axes, and the cor-responding eigenvalues give the magnitude of the peak in thatdirection.

5. Statistical analysis

Among both cohorts, mean medullary and cortical dif-fusion parameters (ADC, FA) as well as eGFRs were com-pared using two-tailed Student’s t tests. Mean cortical

and medullary ADC and FA were also plotted as a functionof eGFR for all subjects and Pearson’s correlation coeffi-cients (R) were determined. Multivariable regression wasused to analyze the dependence of whole-kidney region-of-interest tractography volume on FA, eigenvectors andrenal function diagnosis.

As statistical software (SPSS Statistics 21, IBM, USA) wasused, P-values lower than 0.05 were assumed to be statis-tically significant.

Table 1bThe DTI results of t-test for the patient group.

Paired samples test t df Sig. (2-tailed)Paired differences

Mean Std. deviation Std. error mean 95% confidence interval ofthe difference

Lower Upper

Pair 1 medullarFA - adcmedulla �1.646212 0.045584 0.007935 �1.662375 �1.630049 �207.460 32 0.000

Pair 2 facortex - adccortex �1.993091 0.094447 0.016441 �2.026580 �1.959602 �121.226 32 0.000

Pair 3 k1korteks - k1medulla 0.823939 0.137862 0.023999 0.775056 0.872823 34.333 32 0.000



Pair 6 facortex - medullarFA �0.235364 0.023817 0.004146 �0.243809 �0.226919 �56.769 32 0.000

Table 1cThe DTI correlation values of t-test for the patient group.

Correlations

adccortex medullatractlength adcmedulla facortex k1korteks k1medulla k2korteks

aage Pearson’s Correlation 0.461Sig. (2-tailed) 0.007

medullatractlength Pearson’s Correlation �0.527 0.495Sig. (2-tailed) 0.002 0.003

adcmedulla Pearson’s Correlation �0.527 1 0.345 �0.461Sig. (2-tailed) 0.002 0.049 0.007

k2korteks Pearson’s Correlation �0.461Sig. (2-tailed) 0.007

k2medulla Pearson’s Correlation 0.392Sig. (2-tailed) 0.024

k3korteks Pearson’s Correlation 0.476 �0.346 0.644Sig. (2-tailed) 0.005 0.048 0.000

k3medulla Pearson’s Correlation 0.440Sig. (2-tailed) 0.010

eGFR Pearson’s Correlation 0.385Sig. (2-tailed) 0.027


6. Results

Comparison between the two groups showed that theFA values in the medulla were significantly lower(p < 0.001) in the study group than in the control group.Additionally, the ADC cortex, ADC medulla, and FA cortexwere statistically significant lower values (p = 0.049,0.001, and 0.001 respectively) in the study group comparedto the control group. However the k values did not showstatistically significant differences between the corticalvalues in both groups (p = 0.121). (Compare Table 2a.)

Within the stepwise regression analysis result medullartract length showed linear regression with ADC of themedulla (p = 0.015) in study group population. Addition-ally medullar FA results showed partial regression withADC medulla when eGFR was less than 60 in the studygroup (p = 0.029).

7. Control group

The mean value of the eGFR in the control group wasmeasured to be 84 mL/min (range 72–119 mL/min)(Fig. 1a).

The ADC value was significantly (p < 0.001) higher inthe cortex than in the medulla; the FA value was signifi-cantly (p < 0.001) higher in the medulla than in the cortex.Additionally, the k1, 2, 3 medulla values were higher thanin the cortex (p < 0.001, 0.0013, and 0.0002 respectively).

In healthy subjects there was negative correlation ofeGFR with ADC medulla values (r = �0.484, p = 0.049).For the cortex evaluation, there was negative correlationbetween ADC cortex values and FA values (r = �0.533,p = 0.028) (Fig. 1b).

8. Study group

In the cortical regions, ADC values were significantly(p < 0.001) higher than in the medulla. In opposite, theFA values were significantly (p < 0.001) higher in themedulla than in the cortex. (Fig. 2a and b) (Tables 1a–1c).

Multivariate stepwise regressions in the impaired renalfunction subgroup (eGFR 6 40) showed statistically differ-ing FA values (p = 0.04), when compared to the controlgroup. (The graphics of the detailed analysis are shownin Fig. 3.)

Table2a

TheDTI

resu

ltsof

t-test

betw

eenthegrou

psinclud

ingco

rtex

andmed

ulla.

Inde

pende

ntsamples

test

Leve

ne’stest

for

equalityof

varian

ces

t-test

foreq

ualityof

mea

ns

FSig.

tdf

Sig.

(2-tailed)

Mea

ndifferen

ceStd.

errordifferen

ce95

%co

nfide

nce

interval

ofthedifferen

ce

Lower

Upp

er

med

ullarFA

Equal

varian

cesassu

med

2.96

70.09

26.92

745

0.00

00.05

6998

0.00

8229

0.04

0424

0.07

3572

Equal

varian

cesnot

assu

med

6.01

620

.150

0.00

00.05

6998

0.00

9474

0.03

7244

0.07

6752

adccortex

Equal

varian

cesassu

med

4.32

40.04

32.01

945

0.04

90.05

0833

0.02

5178

0.00

0123

0.10

1544

Equal

varian

cesnot

assu

med

2.53

244

.771

0.01

50.05

0833

0.02

0076

0.01

0393

0.09

1274

adcm

edulla

Equal

varian

cesassu

med

0.32

50.57

16.02

145

0.00

00.08

6000

0.01

4283

0.05

7232

0.11

4768

Equal

varian

cesnot

assu

med

5.66

823

.811

0.00

00.08

6000

0.01

5174

0.05

4669

0.11

7331

faco

rtex

Equal

varian

cesassu

med

6.36

50.01

57.51

545

0.00

00.02

2273

0.00

2964

0.01

6303

0.02

8243

Equal

varian

cesnot

assu

med

6.36

319

.225

0.00

00.02

2273

0.00

3500

0.01

4952

0.02

9593

k1k

orteks

Equal

varian

cesassu

med

2.08

90.15

5�1

.580

450.12

1�0

.025

400.01

607

�0.057

770.00

698

Equal

varian

cesnot

assu

med

�1.717

34.013

0.09

5�0

.025

400.01

479

�0.055

450.00

466

k1m

edulla

Equal

varian

cesassu

med

0.27

90.60

02.64

345

0.01

10.09

578

0.03

624

0.02

279

0.16

878

Equal

varian

cesnot

assu

med

2.63

927

.378

0.01

40.09

578

0.03

629

0.02

136

0.17

020


In contrast to the control group, tractography in thestudy group did not demonstrate astrict radial arrange-ment of the fibers extending from the proximal portionto the Henle loop. The tracks were loosely arranged alongthe displaced parenchyma in the study group. This resultedin hollow spaces without tracts in the location of thedilated renal calyces or parts of the renal pelvices, espe-cially in the patients with diagnosed ureteropelvic junction(UPJ) obstruction (Figs. 4a and 4b).

9. Discussion

The main objective of the study was to assess the feasi-bility and potential benefits of diffusion tensor imaging inpediatric kidney diseases. We acquired diffusion MRimages of sufficient quality to perform DTI tractographyin a cohort of children with normal and abnormal renalfunctional parameters based on the eGFR values.

The renal parenchyma is divided into cortex andmedulla which is totally different in a histological andmorphological point of view. Mainly the cortex part isresponsible for the ultrafiltration of plasma. This ultrafil-trate moves through the medullary pyramids. Betweenthe medullary pyramids there are also vessels which passtransverse and parallel to the tubules, enabling activesecretion and reabsorption of solutes. In the renal pelvicregion, the ultrafiltration moves to the renal papillas end-ing into minor and major calyx forming the urine [1,2,9].The formation of urine and ultrafiltration of the kidneyneeds a nearly perfectly designed microstructural arrange-ment, in both the cortex and the medulla. In the cortex,there are randomly arranged fibers extending from proxi-mal portions of the glomerule to the distal parts of the con-voluted tubules. The fiber network system in the medullaconsisted of a parallel vascular network design. The tubu-lous structures, including the ascending and descendingportions of the Henle loop are also found in this paralleldesigned portion system. In this volumetric design withinthe comparison of medulla with the cortical region, thefibers found in the medulla were thinner than the corticaltubules [1,9,13,16].

In a previous study with a small population, fibersextending throughout the whole kidney did not show sig-nificant differences between kidneys with normal orabnormal function [9]. Our study’s results support thisfinding, although whole renal fiber tracts were signifi-cantly higher in the study group than in the control group.This is most likely due to increasing number of fibers withpatient age and was not statistically significant in the mul-tivariate regression analysis. Similar findings have beenreported in other previous studies [5,6,8,9]. On the otherhand, based on the regression analysis, the medullar FAcould have a critical role in the determination and estima-tion of the renal parenchymal injury.

In the evaluation of the fractional anisotropy maps, cor-ticomedullary differentiation detected in the study groupwas fairly poor when compared with the healthy volun-teers. The insufficient resolution of the FA maps betweenthe regions could be as a result of the injury to the lossof fiber tract organization. This could also be due to the

Fig. 3. (a–f) Figures are enabled from the regression plot of the test of multiwise step logistic regression test. In this graphics the selected cases representthe study group who is less than or equal to eGFR of 40. The number of selected cases is seventeen kidneys.The unselected cases are the children who haveeGFR greater than 40. (a) Shows the relationship of medullar trace length with age. (b) Shows the relationship of ADC medulla with medullar trace length.(c) Shows thepartialregressionplot of medullar FA and age. (d) Shows the scatter plot of medullar FA. (e) Shows the partial regression plot of medullar FAand ADC medulla values. (f) Shows the histogram of selected histogram in the relationship of frequency.


capacity of detecting DTI in the thinner fibers, which couldbe related to the Tesla magnitude. On the other hand,Jaimes et al. did a study with a 3T machine reporting sim-ilar results [9].

Regarding the patient group, there is a decrease in diffu-sion anisotropy obtained. This could be caused within thestructural parenchymal alterations, such as interstitialfibrosis, tubular atrophy and cellular infiltration, basicallyinvolving pathologies the medullar part of the renal sys-tem. Previously particularly including the small groupstudies presenting the reduction in the medullary frac-tional anisotropy values was reported [4–6,8,9]. In ourstudy group, there were seventeen patients with eGFR lessthan 40 ml/min/1.73 m2. In this group we identified thatonly medullary FA could be a promising diagnostic toolin the assessment of radial fiber arrangement and its corre-lation with eGFR. Based on our study report, we could usethe medullary FA as a marker of renal structural integrityalteration, potentially useful index for the diagnosis andoutcome of kidney disease.

Hueper et al. [11], hypothesize that the majority ofchronic diseases affecting the renal parenchyma probablyalter directed diffusion (FA) before free diffusion (ADC).Previous studies mention that ADC and FA are also influ-enced by different several factors as in the renal medulla.In think age of the water molecules and physiology there

could be high alterations during the movement of thetransportation [6,9]. ADC is mainly influenced by perfu-sion, whereas the FA is related to the water molecule trans-port in the collecting tubules.

These comments also suggested that DTI is the mostappropriate technique for functionally evaluating thekidney as compared to DWI, and the medullary FA repre-sents the most sensitive parameter in detecting renal dam-age in different diseases.

The limitations of the study include a small study pop-ulation of 49 children. There were no patients with aneGFR lower than 25 ml/min/1.73 m2 and only seventeenwith an eGFR between 25 ml/min/1.73 m2 and 40 ml/min/1.73 m2. We avoided inclusion of patients with a eGFRlower than 25 ml/min/1.73 m2 because of potentiallyharmful MRI contrast agent effects [17]. Due to therestricted study population, age-dependencies in renal dif-fusion parameters were no assessed explicitly. Regardingthis, we noticed similar results as in the literature [9].Additionally, we did not consider or compare different bvalues in the evaluation of DTI imaging, which possiblycould help to optimize acquisition technique. Previousstudies demonstrated the effects of different b values[19–21], that influence the FA values regarding the limita-tions for the specific chronic kidney diseases should beevaluated.

Fig. 3b (continued)

Fig. 3c (continued)


Fig. 3e (continued)

Fig. 3d (continued)


Fig. 3f (continued)

Fig. 4a. Shows the DTI evaluation of a seven years old boy with eGFR diagnosed with 30 after TrackVis program reformat technique: The long green renalfibers show the extension of from proximal tubules to the Henle Loop. The proximal portion of the fibers getting thinner represents the tubule pathology inmedulla region.This image was obtained with a view of 55�.


10. Conclusions

Our prospective study showed the capability of renalDTI in the usage of alterations induced by variouschronic kidney diseases. DTI enables to understand the

renal anisotropy based on physiology without contrastmedia administration. Medullary FA values seem to bethe best promising tool in the association within thecomplementary of laboratory and morphologicalparameters.

Fig. 4b. Shows the anterior-posterior view of the 3-D tractography. The upperportion of the green fibers get thinner and shows loss of connection ofnetwork in the radial arrangement at the medullar region. The red fibers shows the crossing of left to right direction. (For interpretation of the references tocolor in this figure legend, the reader is referred to the web version of this article.)


Conflict of interest

The authors declare that there are no conflict ofinterests.

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http://dx.doi.org/10.1002/jmri.2087

http://dx.doi.org/10.1002/jmri.2087

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