Clinical Radiology xxx (2014) 1e10
Contents lists available at ScienceDirect
Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Review
Diffusion-weighted imaging in urinary tract lesions V. Baliyan, C.J. Das*, S. Sharma, A.K. Gupta All India Institute of Medical Sciences, Ansari Nagar, New Delhi, India
art icl e i nformat ion Article history: Received 7 October 2013 Received in revised form 9 January 2014 Accepted 14 January 2014
Diffusion-weighted imaging (DWI) utilizes the signal contrast provided by the regional differences in the Brownian motion of water molecules, which is a direct reflection of the cellular micro-environment. DWI emerged as a revolutionary magnetic resonance imaging (MRI) technique in the field of stroke imaging. As far as body imaging is concerned, DWI has come a long way from being an experimental technique to an essential element of almost all abdominal MRI examinations. This progress has been made possible by technical advancements in MRI systems, as well as a better understanding of MRI physics. DWI is quick to perform and has the potential to provide crucial information about the disease process without adding much to the total imaging time. This article provides a brief review of the basic principles of DWI with insights to the information that DWI provides in the evaluation of various diseases of the urinary tract at both 1.5 and 3 T. DWI is helpful for differentiation of various histopathological subtypes of renal cell carcinoma (RCC). Prediction of histopathological grade of RCC is also becoming possible solely based on DWI. Assessment of response to chemotherapeutic agents is possible based on the change in the ADC (apparent diffusion coefficient) value. DWI performed with high b-values increases the confidence in diagnosing prostatic carcinoma. This article highlights the emerging role of DWI in the evaluation of urinary tract lesions. Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Diffusion is the random molecular motion on a microscopic scale. The randomness of this motion is due to a very high rate of collisions of moving molecules among themselves or against cell membranes. Diffusion-weighted signal contrast depends on a complex interaction between the Brownian motion of water molecules and biological membranes (natural barriers to the Brownian motion). Brownian motion occurs more freely in an environment with a lesser degree of compartmentalization compared to a highly cellular arrangement with tightly packed cells.
Malignancies, lymphomas, and abscesses have highly cellular arrangements; hence, they show restricted diffusion. The diffusion characteristics can be measured objectively and are represented in form of apparent diffusion coefficient (ADC) values. So tissue diffusivity and, hence, diffusion-weighted imaging (DWI) can provide crucial diagnostic information regarding the architecture of various tissues and organs. Recently, DWI has moved a step further, as it has been shown that the degree of diffusion restriction correlates with tumour grade, and ADC values can be used as a biomarker to evaluate the response to chemotherapy.
DWI: basic physics * Guarantor and correspondent: C.J. Das, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India. Tel.: þ91 1126593628. E-mail address: [email protected] (C.J. Das).
To understand the basis of DWI, let us consider that there are two water molecules that are diffusing along a magnetic
0009-9260/$ e see front matter Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2014.01.011
Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
2
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
field gradient. As time goes on, the molecules alter their paths and begin to experience slightly different field strengths, which in turn affect their precession frequencies and phase. The phase differences generated as a result of motion diminish the magnitude of the final echo depending on the strength and duration of the field gradients. DWI is a modification of the T2-weighted sequence with the application of a special type of gradient known as the diffusionlabelling gradient. Diffusion-labelling gradients are coupled equal and opposite gradients that are applied on either side of a 180 refocusing pulse (Fig 1), which make the moving molecules lose signal. Static molecules experience equal and opposite phase shift under the influence of these gradients. However, these phase shifts are not equal and, hence, do not cancel each other out in the case of freely diffusing molecules. If water is free to diffuse in any direction, it is called isotropic diffusion. Due to its random nature, diffusion is inherently isotropic (meaning equal probability in all directions). However, in certain instances, it may have a directionality due to the anisotropy of the medium, e.g., elongated cellular processes of neurons (axons and dendrites) and because diffusion-labelling gradients are applied only along one direction at a time. If a diffusion-labelling gradient is applied perpendicular to the axis of the fibres, these will show restricted diffusion. So the sequence is repeated with the labelling gradients along the x, y, and z-axes and the signal is averaged. This removes the directional effect.
ADC and ADC map The ADC is an objective measure of diffusion expressed in square millimetre per second. ADC map is a voxel-byvoxel representation of the ADC values. DWI has some amount of T2 weighting, and the signal depends on both diffusion and tissue T2 properties. This makes areas with longer T2 relaxation times appear brighter, which may mimic restricted diffusion. This effect (T2 shine-through effect) can be avoided by using a sequence with a shorter echo time, a higher b-value, and by interpreting the DWI in conjunction with the ADC map, as in cases of T2 shinethrough, the ADC will be normal or high signal.1 T2 shinethrough occurs because of the long T2 decay time in some normal tissues. The formula for calculating ADC1,2 is
ADC ¼ log½ðS0=S1Þ=ðb1 b0Þ where S0 is the signal intensity on the b0 image (without diffusion sensitising gradient); S1 is the signal intensity on the DWI image (with a higher b-value); and the b-value is the gradient factor of the diffusion-sensitizing gradient in seconds per square millimetre. Areas of restricted diffusion will appear as bright areas at DWI and as dark areas on the corresponding ADC map. However, an area with a longer T2 relaxation time (e.g., fluid) will be bright on both.
Imaging technique The DWI protocol for abdominal magnetic resonance imaging (MRI) used at our institute is shown in Table 1. A commonly used technique for abdominal DWI is breathhold, fat-suppressed, single shot spin-echo echo-planer imaging (EPI) using a parallel imaging technique.3 Fat suppression is necessary to avoid chemical shift artefacts. The use of a breath-hold technique limits the number of bvalues and the signal-to-noise ratio (SNR) is low. The SNR can be improved with the use of higher field strengths (3 T) and parallel imaging.5 Parallel imaging permits a shorter echo time, which increases the SNR and reduces susceptibility artefacts.6
Field strength: 1.5 versus 3 T Most of the experience on DWI that has been reported in the literature is with the use of 1.5 T systems. However, experience with the use of 3 T magnets for DWI is growing. Therefore, it is imperative for radiologists to be familiar with the advantages and pitfalls of DWI at 3 T. Inherent high SNR at 3 T allows faster imaging. This combined with the advantages of parallel imaging allows acquisition of the DWI sequence during a single breathhold. Three Tesla allows high b-value diffusion imaging. A greater incidence of susceptibility artefacts is the only major pitfall.7
Table 1 Diffusion-weighted imaging protocol for 1.5 and 3 T systems. Parameter
3 Tesla
1.5 Tesla
Sequence
2D single-shot spin echo EPI 16 channels 3657.5 SPIR 124 100 36 5/1
2D single-shot spin echo EPI 16 channels 3654 SPIR 100 124 36 5/1
SENSE (sensitivity encoding) 3
SENSE
0, 400, 800
0, 400, 800
Coils Bandwidth, Hz/pixel Fat-suppression technique Image matrix Number of sections Section thickness/ intersection gap, mm Parallel imaging technique
Figure 1 Application of diffusion-labelling gradients of equal strength but opposite polarity, on either side of 180 pulse.
Direction of diffusion gradients b-Values, s/mm2
3
SPIR, spectral inversion recovery.
Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
3
Figure 2 Simple renal cyst showing gradual decline in signal on increasing b-values and losing almost all signal on b ¼ 800 s/mm2 image (c). ADC map (d) shows high ADC value. Corresponding (e) T1 and (f) T2-weighted images of the cyst.
Normal diffusion characteristics of kidneys The kidney has the highest ADC values among the solid abdominal organs.8 It shows regional differences in ADC values. The renal cortex has a higher ADC than the medulla, and diffusion is anisotropic in the medulla.9 It is important to mention here that ADC values of the cortex and medulla are identical in transplanted kidneys.
lesions. However, there is considerable overlap between the ADC values of complicated cysts and cystic renal cell carcinomas (RCCs).10
Infection In pyelonephritis, the renal cortical and medullary ADC values are significantly lower (Fig 4) than the normal contralateral kidney.10
Neoplasms
Evaluation of disease Renal Simple and complicated cysts The signal intensity of most simple cysts drops at a higher b-value (>500 s/mm2) and disappears completely at b-values of approximately 1000 s/mm2 (Fig 2). The presence of blood products and proteinaceous material makes complicated cysts appear bright on T1-weighted images, hypointense on T2-weighted and b0 images, and show lower ADC values than simple cysts (Fig 3). Simple and even complicated cysts have higher ADC values than solid renal
Benign and malignant lesions show significantly different ADC values. Benign lesions lose signal at higher b-value images and show high ADC values.11 Conversely, retention of signal at higher b-value images and low ADC values indicate hypercellular tissue or malignancy (Figs 5 and 6). In the case of renal vein or inferior vena cava (IVC) invasion by RCC, the tumour thrombus can be evaluated as the tumour thrombus shows restricted diffusion with ADC values comparable to the renal mass (Fig 7). DWI helps to differentiate between RCC and transitional cell carcinoma (TCC) and among various subtypes of RCC. The ADC value is significantly higher in RCC than in TCC. Among various subtypes of RCC, clear cell RCC shows higher ADC values than non-clear cell RCC.12 Prediction
Figure 3 Complicated haemorrhagic renal cyst shows bright signal on T1-weighted image (a) and lower signal on T2-weighted (b) images. It shows restriction of diffusion (c) and low ADC value on the ADC map (d). Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
4
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
Figure 4 A patient with pyelonephritis shows restriction of diffusion at b ¼ 800 s/mm2 (arrow) and corresponding areas of low ADC in the left kidney (arrow).
Figure 5 There is a small T2 hyperintense (a) and T1 hypointense (b) mass at the lower pole of left kidney, which shows peripheral bright signal at DWI (c) and corresponding low signal on the ADC map (d). Histopathology showed it to be a clear cell carcinoma.
of histopathological grade is also possible solely based on DWI. A recent MRI study of renal tumours using DWI at 3 T, demonstrated an inverse linear relationship with the cellularity in renal malignancies.13 Whole-body DWI with background suppression (DWIBS; Fig 8) can be used to evaluate metastatic spread of RCC.4 However, as there is significant overlap between these ADC values, one cannot be confident in distinguishing benign from malignant renal neoplasm based on ADC values alone.14 Therefore, conventional MRI is still necessary for the optimal characterization of indeterminate renal masses and biopsy is often the final solution for this challenging question. DWI also helps to differentiate viable from necrotic areas within tumours.15 Therefore, it aids the selection of optimal target sites for biopsy and in the detection of response following radiation therapy, chemotherapy, or local ablative therapies.16 An increase in ADC values after therapy is considered a marker of response, whereas persistence of low ADC values is a sign of non-response.16 An important aspect of increase in ADC following treatment with chemotherapy and/or radiation is that this change may predate other morphological changes detected by conventional
MRI parameters, e.g., size, T2 signal. Therefore, it may serve as a useful biomarker to predict changes ahead of morphological RECIST criteria to assess treatment response.
Angiomyolipoma (AML). Among all renal neoplasms, angiomyolipomas (Fig 16) show minimum ADC values. This has been attributed to the muscle and fat component of AMLs.
Chronic renal failure (CRF) ADC values of renal parenchyma in patients with CRF are significantly lower (both cortex and medulla) than the ADC values of normal renal parenchyma (Fig 9). This has the potential to evolve as a tool for qualitative assessment of renal function and as a method for monitoring early renal allograft rejection.17,18
Other renal diseases The ADC of the renal cortex is lower in patients with renal artery stenosis.17 DWI also has the potential to recognize renal infarcts.19
Figure 6 Case of a renal TCC showing hydronephrosis (a) and surrounding soft-tissue mass with restricted diffusion (b) and low signal on the ADC map (c). Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
5
Figure 7 A T2 isointense tumour thrombus in the left renal vein branches (a; arrow) with high signal at b ¼ 800 s/mm2 (b) and hypointense signal on the ADC map (c), suggestive of restricted diffusion. Another patient with RCC shows tumour thrombus in IVC reaching up to the right atrium (d and g; arrows) and a metastatic lesion in the liver. The primary mass, thrombus in the IVC, and metastatic lesion all show restricted diffusion (eef).
Pelvicalyceal and ureter Hydronephrosis versus pyonephrosis The ADC value of the renal pelvis in pyonephrosis is lower than the values in hydronephrosis20 (Figs 10 and 11). Sometimes a large necrotic renal mass with pelvicalyceal extension may be mistaken for pyonephrosis at ultrasound, computed tomography (CT), or conventional MRI (Fig 10), but these can be differentiated based on DWI as such
tumours show peripheral restricted diffusion (Fig 12), whereas pyonephrosis shows a different pattern with restriction of diffusion in the entire renal pelvis or an appearance of fluidefluid level with restriction in dependent areas (Fig 12).
TCC In a study by Nishizawa et al.,21 renal pelvic and ureteric tumours (except carcinoma in situ) were shown clearly with
Figure 8 DWIBS shows metastatic lesions in the scalp, ribs, and lumbar vertebrae. Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
6
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
Figure 9 Upper panel shows a rejected transplant kidney in the right iliac fossa. Lower panel shows native kidney of a patient with CRF. Note is made of marked restriction of diffusion in both cases.
Figure 10 T2-weighted image (a) shows fluid signal inside a dilated pelvicalyceal system, which loses signal on the b ¼ 800 s/mm2 image (b) and the ADC map shows free diffusion, suggestive of simple hydronephrosis.
Figure 11 (a) Coronal half-Fourier axial single-shot fast spin-echo (HASTE), (b) T1 axial and (c) T2 FS axial images show fluid signal in the bilateral dilated pelvicalyceal system and staghorn calculus in left renal pelvis. (d) DWI image at b ¼ 800 s/mm2 and (e) the ADC map show fluidefluid levels with restriction of diffusion in dependent areas, suggestive of pyonephrosis. Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
7
Figure 12 (a) Axial T2-weighted image shows fluid signal inside the dilated pelvicalyceal system with peripheral enhancement on gadoliniumenhanced images (b, c). (d, e) DWI and ADC map show peripheral restriction, suggestive of necrotic RCC rather than pyonephrosis.
DWI (Fig 7). In addition, the infiltrating tumour had lower ADC values than that of papillary tumour.
Urinary bladder and prostate TCC
Lymphomas It is well established that lymphoma shows restricted diffusion, which is attributed to its high cellularity. We encountered a case of diffuse large B-cell lymphoma (DLBCL) with retroperitoneal lymph nodes and contiguous infiltration of the renal pelvis and circumferential ureteric wall thickening suggestive of infiltration. At DWI, it showed restricted diffusion in the soft tissue in the renal pelvis and in the soft tissue along the left ureter wall (Fig 13).
TCC is the major histological type of bladder cancer, which is further subdivided into the various histological grades. The histological grade of TCC is the most important factor that determines tumour progression and recurrence. There is a significant correlation between ADC values and histopathological grades,22 so ADC value has the potential to predict the biological behaviour of bladder cancer and tumour recurrence (Fig 14). However, the interpretation of DWI may be challenging due to the frequent occurrence of bladder clots in the vicinity, which may also show restricted diffusion.
Figure 13 A patient with recurrent diffuse large B-cell lymphoma shows left para-aortic lymph node with infiltrative T2 isointense (a) soft tissue in the left renal sinus showing restricted diffusion (b, c). The images in the lower panel show soft-tissue along the ureter (d), which also shows restricted diffusion (e, f). Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
8
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
Figure 14 (a) Axial T2-weighted image shows irregular bladder wall thickening showing restricted diffusion (bec) in a patient with carcinoma of urinary bladder.
Prostate carcinoma
Pitfalls
The majority of prostatic carcinomas arise from the peripheral zone, which are usually easy to diagnose due to their T2 hypointense signal on the background of the bright T2 signal of the normal peripheral zone (Fig 15aec). A significant minority of prostatic carcinomas arises in the transition zone, but a high prevalence of BPH makes it difficult to diagnose.23 There is growing evidence to show that DWI might help to detect carcinoma in the transition zone (Fig 15dee) and also to detect skeletal metastasis.24e26 However, it has its own limitations of poor spatial resolution, artefacts due to biopsy-related haemorrhage, and the overlapping ADC values.
Currently, DWI images have low spatial resolution; however, contrast resolution is good. It is also important to note that DWI does not work for lesions with a low intrinsic T2 signal (T2 blackout effect, Fig 16). DWI is also vulnerable to susceptibility effects. One such example is the effect of gadolinium: as gadolinium has significant susceptibility effects at higher concentration it can significantly decrease the T2 signal in the renal parenchyma and the collecting system due to high concentration at these sites (Fig 17). It can be avoided easily by simply performing DWI prior to the administration of gadolinium.
Figure 15 (a) Axial T2-weighted image shows subtle signal changes with hypointensity in the peripheral zone on left side. (bec) DWI shows restriction of diffusion at the corresponding location. (d, e) Lesion with restricted diffusion in the transition zone. Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
9
Figure 16 A case of angiomyolipoma showing bright signal on T1-weighted imaging (aeb) due to fat, and shows low signal on the fat-saturated T2weighted image (c). Lower panel shows that the signal at DWI (all b-values) and ADC is low due to lack of enough water protons (T2 blackout effect).
Future trends Predicting tumour perfusion (intravoxel incoherent motion) DWI was introduced in the 1980s and, initially, it was considered that only random Brownian motion was responsible for the generation of contrast in DWI. However, it
soon became clear that the motion of water through microvasculature also influences the signal at DWI.1 Because of the random orientation of the capillary network, motion of water molecules driven by perfusion mimics the properties of molecular diffusion, also called pseudo-diffusion. Therefore, DWI contrast is a result of phase dispersion under the combined effect of molecular diffusion and microvascular perfusion, known as intravoxel incoherent motion (IVIM). The influence of pseudo-diffusion is one order higher in magnitude due to the greater distances covered by the protons under its influence. As a result, the drop in signal at lower b-values (e.g., 0e100 s/mm2) is predominantly a result of perfusion effects and at higher b-values Brownian molecular diffusion dominates. As a result, the plot of signal intensity versus b-value is a bi-exponential function, and it is possible to calculate the perfusion fraction of tissue using IVIM analysis.27e30 However, this has its own limitations, because the diffusion fraction is subject to contamination from other tubular flow phenomena, such as the collecting tubular flow of the kidneys (31e33).
Summary
Figure 17 T1-weighted gadolinium-enhanced image shows loss of signal at the dependent location within the urinary bladder due to T2 effects (susceptibility).
DWI provides useful information about the local microenvironment of the diffusivity of water molecules in tissues, which is quantified using the ADC. In general, normal tissues show relatively free diffusion compared to malignant tumours, which show restricted diffusion because of high cell densities and a high nuclear-to-cytoplasmic ratio. Initially, the application of DWI in routine clinical practice was limited to stroke imaging, but during the past few years, its use has also been extended to body imaging. Initially DWI was seldom applied in body imaging because of technical difficulties; however, these difficulties have been overcome with the introduction of parallel imaging techniques, stronger gradient systems, and multi-channel coils. Consequently, it has now become an essential element of almost all abdominal MRI examinations. Currently, DWI has the
Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
10
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
potential for tumour detection and characterization for several organs, including the kidney, prostate, and urinary bladder. In future, it is likely that the ADC will be used as an imaging biomarker to assess treatment response following chemo-radiotherapy.
17.
18.
References 1. Le Bihan D, Breton E, Lallemand D, et al. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 1988;168:497e505. 2. Charles-Edwards EM, deSouza NM. Diffusion-weighted magnetic resonance imaging and its application to cancer. Cancer Imaging 2006;6:135e43. 3. Yamashita Y, Tang Y, Takahashi M. Ultrafast MR imaging of the abdomen: echo planar imaging and diffusion-weighted imaging. J Magn Reson Imaging 1998;8:367e74. € ller MF, Prasad P, Siewert B, et al. Abdominal diffusion mapping with 4. Mu use of a whole-body echo-planar system. Radiology 1994;190:475e8. € rtz P, Krautmacher C, Tra €ber F, et al. Diffusion-weighted whole- body 5. Mu MR imaging with background body signal suppression: a feasibility study at 3.0 Tesla. Eur Radiol 2007;17:3031e7. 6. Skare S, Newbould RD, Clayton DB, et al. Clinical multishot DW-EPI through parallel imaging with considerations of susceptibility, motion, and noise. Magn Reson Med 2007;57:881e90. 7. Akisik FM, Sandrasegaran K, Aisen AM, et al. Abdominal MR imaging at 3.0 T. RadioGraphics 2007;27:1433e44. 8. Kilickesmez O, Yirik G, Bayramoglu S, et al. Non-breath-hold high bvalue diffusion-weighted MRI with parallel imaging technique: apparent diffusion coefficient in normal abdominal organs. Diagn Interv Radiol 2008;14:83e7. 9. Ries M, Jones RA, Basseau F, et al. Diffusion tensor MRI of the human kidney. J Magn Reson Imaging 2001;14:42e9. 10. Cova M, Squillaci E, Stacul F, et al. Diffusion weighted MRI in the evaluation of renal lesions: preliminary results. Br J Radiol 2004;77:851e7. 11. Thoeny HC, De Keyzer F, Oyen RH, et al. Diffusion-weighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience. Radiology 2005;235:911e7. 12. Notohamiprodjo M, Staehler M, Steiner N, et al. Combined diffusionweighted, blood oxygen level-dependent, and dynamic contrastenhanced MRI for characterization and differentiation of renal cell carcinoma. Acad Radiol 2013;20:685e93. 13. Manenti G, Di Roma M, Mancino S, et al. Malignant renal neoplasms: correlation between ADC values and cellularity in diffusion weighted magnetic resonance imaging at 3 T. Radiol Med 2008;113:199e213. 14. Zhang J, Tehrani YM, Wang L, et al. Renal masses: characterization with diffusion-weighted MR imagingda preliminary experience. Radiology 2008;247:458e64. 15. Razek AA, Megahed AS, Denewer A, et al. Role of diffusion-weighted magnetic resonance imaging in differentiation between the viable and necrotic parts of head and neck tumors. Acta Radiol 2008;49:364e70. 16. Buijs M, Kamel IR, Vossen JA, et al. Assessment of metastatic breast cancer response to chemoembolization with contrast agent enhanced
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29. 30. 31.
32.
33.
and diffusion-weighted MR imaging. J Vasc Interv Radiol 2007;18:957e63. Namimoto T, Yamashita Y, Mitsuzaki K, et al. Measurement of the apparent diffusion coefficient in diffuse renal disease by diffusionweighted echo-planar MR imaging. J Magn Reson Imaging 1999;9:832e7. Thoeny HC, Zumstein D, Simon-Zoula S, et al. Functional evaluation of transplanted kidneys with diffusion-weighted and BOLD MR imaging: initial experience. Radiology 2006;241:812e21. Yamanouchi Y, Yamamoto K, Noda K, et al. Renal infarction in a patient with spontaneous dissection of segmental arteries: diffusion- weighted magnetic resonance imaging. Am J Kidney Dis 2008;52:788e91. Merkle EM, Nour SG, Lewin JS. MR imaging follow-up after percutaneous radiofrequency ablation of renal cell carcinoma: findings in 18 patients during first 6 months. Radiology 2005;235:1065e71. Nishizawa S, Imai S, Okaneya T, et al. Diffusion weighted imaging in the detection of upper urinary tract urothelial tumors. Int Braz J Urol 2010;36:18e28. Kanazawa S, Matsuki M, Inada Y, et al. Diffusion-weighted MR imaging for urinary bladder carcinoma: ADC values among tumor histologic grades. Bull Osaka Med Coll 2008;54:1e6. McNeal JE, Redwine EA, Freiha FS, et al. Zonal distribution of prostatic adenocarcinoma: correlation with histologic pattern and direction of spread. Am J Surg Pathol 1988;12:897e906. Hosseinzadeh K, Schwarz SD. Endorectal diffusion-weighted imaging in prostate cancer to differentiate malignant and benign peripheral zone tissue. J Magn Reson Imaging 2004;20:654e61. Kim CK, Park BK, Lee HM, et al. Value of diffusion-weighted imaging for the prediction of prostate cancer location at 3 T using a phased-array coil: preliminary results. Invest Radiol 2007;42:842e7. € fer R, Blumstein N, et al. Prostate carcinoma: diffusionLuboldt W, Ku weighted imaging as potential alternative to conventional MR and 11 C-choline PET/CT for detection of bone metastases. Radiology 2008;249:1017e25. Le Bihan D, Breton E, Lallemand D, et al. MR imaging of intra-voxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986;161:401e7. Le Bihan D, Turner R, Moonen CT, et al. Imaging of diffusion and microcirculation with gradient sensitization: design, strategy, and significance. J Magn Reson Imaging 1991;1:7e28. Le Bihan D. IVIM method measures diffusion and perfusion. Diagn Imaging (San Franc) 1990;12. 133, 136. Le Bihan D. Intravoxel incoherent motion perfusion MR imaging: a wake-up call. Radiology 2008;249:748e52. Yoshino N, Yamada I, Ohbayashi N, et al. Salivary glands and lesions: evaluation of apparent diffusion coefficients with split-echo diffusionweighted MR imagingdinitial results. Radiology 2001;221:837e42. Zhang L, Murata Y, Ishida R, et al. Functional evaluation with intra- voxel incoherent motion echo-planar MRI in irradiated salivary glands: a correlative study with salivary gland scintigraphy. J Magn Reson Imaging 2001;14:223e9. Muller MF, Prasad PV, Edelman RR. Can the IVIM model be used for renal perfusion imaging? Eur J Radiol 1998;26:297e303.
Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
Contents lists available at ScienceDirect
Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Review
Diffusion-weighted imaging in urinary tract lesions V. Baliyan, C.J. Das*, S. Sharma, A.K. Gupta All India Institute of Medical Sciences, Ansari Nagar, New Delhi, India
art icl e i nformat ion Article history: Received 7 October 2013 Received in revised form 9 January 2014 Accepted 14 January 2014
Diffusion-weighted imaging (DWI) utilizes the signal contrast provided by the regional differences in the Brownian motion of water molecules, which is a direct reflection of the cellular micro-environment. DWI emerged as a revolutionary magnetic resonance imaging (MRI) technique in the field of stroke imaging. As far as body imaging is concerned, DWI has come a long way from being an experimental technique to an essential element of almost all abdominal MRI examinations. This progress has been made possible by technical advancements in MRI systems, as well as a better understanding of MRI physics. DWI is quick to perform and has the potential to provide crucial information about the disease process without adding much to the total imaging time. This article provides a brief review of the basic principles of DWI with insights to the information that DWI provides in the evaluation of various diseases of the urinary tract at both 1.5 and 3 T. DWI is helpful for differentiation of various histopathological subtypes of renal cell carcinoma (RCC). Prediction of histopathological grade of RCC is also becoming possible solely based on DWI. Assessment of response to chemotherapeutic agents is possible based on the change in the ADC (apparent diffusion coefficient) value. DWI performed with high b-values increases the confidence in diagnosing prostatic carcinoma. This article highlights the emerging role of DWI in the evaluation of urinary tract lesions. Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Diffusion is the random molecular motion on a microscopic scale. The randomness of this motion is due to a very high rate of collisions of moving molecules among themselves or against cell membranes. Diffusion-weighted signal contrast depends on a complex interaction between the Brownian motion of water molecules and biological membranes (natural barriers to the Brownian motion). Brownian motion occurs more freely in an environment with a lesser degree of compartmentalization compared to a highly cellular arrangement with tightly packed cells.
Malignancies, lymphomas, and abscesses have highly cellular arrangements; hence, they show restricted diffusion. The diffusion characteristics can be measured objectively and are represented in form of apparent diffusion coefficient (ADC) values. So tissue diffusivity and, hence, diffusion-weighted imaging (DWI) can provide crucial diagnostic information regarding the architecture of various tissues and organs. Recently, DWI has moved a step further, as it has been shown that the degree of diffusion restriction correlates with tumour grade, and ADC values can be used as a biomarker to evaluate the response to chemotherapy.
DWI: basic physics * Guarantor and correspondent: C.J. Das, All India Institute of Medical Sciences, Ansari Nagar, New Delhi 110029, India. Tel.: þ91 1126593628. E-mail address: [email protected] (C.J. Das).
To understand the basis of DWI, let us consider that there are two water molecules that are diffusing along a magnetic
0009-9260/$ e see front matter Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2014.01.011
Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
2
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
field gradient. As time goes on, the molecules alter their paths and begin to experience slightly different field strengths, which in turn affect their precession frequencies and phase. The phase differences generated as a result of motion diminish the magnitude of the final echo depending on the strength and duration of the field gradients. DWI is a modification of the T2-weighted sequence with the application of a special type of gradient known as the diffusionlabelling gradient. Diffusion-labelling gradients are coupled equal and opposite gradients that are applied on either side of a 180 refocusing pulse (Fig 1), which make the moving molecules lose signal. Static molecules experience equal and opposite phase shift under the influence of these gradients. However, these phase shifts are not equal and, hence, do not cancel each other out in the case of freely diffusing molecules. If water is free to diffuse in any direction, it is called isotropic diffusion. Due to its random nature, diffusion is inherently isotropic (meaning equal probability in all directions). However, in certain instances, it may have a directionality due to the anisotropy of the medium, e.g., elongated cellular processes of neurons (axons and dendrites) and because diffusion-labelling gradients are applied only along one direction at a time. If a diffusion-labelling gradient is applied perpendicular to the axis of the fibres, these will show restricted diffusion. So the sequence is repeated with the labelling gradients along the x, y, and z-axes and the signal is averaged. This removes the directional effect.
ADC and ADC map The ADC is an objective measure of diffusion expressed in square millimetre per second. ADC map is a voxel-byvoxel representation of the ADC values. DWI has some amount of T2 weighting, and the signal depends on both diffusion and tissue T2 properties. This makes areas with longer T2 relaxation times appear brighter, which may mimic restricted diffusion. This effect (T2 shine-through effect) can be avoided by using a sequence with a shorter echo time, a higher b-value, and by interpreting the DWI in conjunction with the ADC map, as in cases of T2 shinethrough, the ADC will be normal or high signal.1 T2 shinethrough occurs because of the long T2 decay time in some normal tissues. The formula for calculating ADC1,2 is
ADC ¼ log½ðS0=S1Þ=ðb1 b0Þ where S0 is the signal intensity on the b0 image (without diffusion sensitising gradient); S1 is the signal intensity on the DWI image (with a higher b-value); and the b-value is the gradient factor of the diffusion-sensitizing gradient in seconds per square millimetre. Areas of restricted diffusion will appear as bright areas at DWI and as dark areas on the corresponding ADC map. However, an area with a longer T2 relaxation time (e.g., fluid) will be bright on both.
Imaging technique The DWI protocol for abdominal magnetic resonance imaging (MRI) used at our institute is shown in Table 1. A commonly used technique for abdominal DWI is breathhold, fat-suppressed, single shot spin-echo echo-planer imaging (EPI) using a parallel imaging technique.3 Fat suppression is necessary to avoid chemical shift artefacts. The use of a breath-hold technique limits the number of bvalues and the signal-to-noise ratio (SNR) is low. The SNR can be improved with the use of higher field strengths (3 T) and parallel imaging.5 Parallel imaging permits a shorter echo time, which increases the SNR and reduces susceptibility artefacts.6
Field strength: 1.5 versus 3 T Most of the experience on DWI that has been reported in the literature is with the use of 1.5 T systems. However, experience with the use of 3 T magnets for DWI is growing. Therefore, it is imperative for radiologists to be familiar with the advantages and pitfalls of DWI at 3 T. Inherent high SNR at 3 T allows faster imaging. This combined with the advantages of parallel imaging allows acquisition of the DWI sequence during a single breathhold. Three Tesla allows high b-value diffusion imaging. A greater incidence of susceptibility artefacts is the only major pitfall.7
Table 1 Diffusion-weighted imaging protocol for 1.5 and 3 T systems. Parameter
3 Tesla
1.5 Tesla
Sequence
2D single-shot spin echo EPI 16 channels 3657.5 SPIR 124 100 36 5/1
2D single-shot spin echo EPI 16 channels 3654 SPIR 100 124 36 5/1
SENSE (sensitivity encoding) 3
SENSE
0, 400, 800
0, 400, 800
Coils Bandwidth, Hz/pixel Fat-suppression technique Image matrix Number of sections Section thickness/ intersection gap, mm Parallel imaging technique
Figure 1 Application of diffusion-labelling gradients of equal strength but opposite polarity, on either side of 180 pulse.
Direction of diffusion gradients b-Values, s/mm2
3
SPIR, spectral inversion recovery.
Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
3
Figure 2 Simple renal cyst showing gradual decline in signal on increasing b-values and losing almost all signal on b ¼ 800 s/mm2 image (c). ADC map (d) shows high ADC value. Corresponding (e) T1 and (f) T2-weighted images of the cyst.
Normal diffusion characteristics of kidneys The kidney has the highest ADC values among the solid abdominal organs.8 It shows regional differences in ADC values. The renal cortex has a higher ADC than the medulla, and diffusion is anisotropic in the medulla.9 It is important to mention here that ADC values of the cortex and medulla are identical in transplanted kidneys.
lesions. However, there is considerable overlap between the ADC values of complicated cysts and cystic renal cell carcinomas (RCCs).10
Infection In pyelonephritis, the renal cortical and medullary ADC values are significantly lower (Fig 4) than the normal contralateral kidney.10
Neoplasms
Evaluation of disease Renal Simple and complicated cysts The signal intensity of most simple cysts drops at a higher b-value (>500 s/mm2) and disappears completely at b-values of approximately 1000 s/mm2 (Fig 2). The presence of blood products and proteinaceous material makes complicated cysts appear bright on T1-weighted images, hypointense on T2-weighted and b0 images, and show lower ADC values than simple cysts (Fig 3). Simple and even complicated cysts have higher ADC values than solid renal
Benign and malignant lesions show significantly different ADC values. Benign lesions lose signal at higher b-value images and show high ADC values.11 Conversely, retention of signal at higher b-value images and low ADC values indicate hypercellular tissue or malignancy (Figs 5 and 6). In the case of renal vein or inferior vena cava (IVC) invasion by RCC, the tumour thrombus can be evaluated as the tumour thrombus shows restricted diffusion with ADC values comparable to the renal mass (Fig 7). DWI helps to differentiate between RCC and transitional cell carcinoma (TCC) and among various subtypes of RCC. The ADC value is significantly higher in RCC than in TCC. Among various subtypes of RCC, clear cell RCC shows higher ADC values than non-clear cell RCC.12 Prediction
Figure 3 Complicated haemorrhagic renal cyst shows bright signal on T1-weighted image (a) and lower signal on T2-weighted (b) images. It shows restriction of diffusion (c) and low ADC value on the ADC map (d). Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
4
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
Figure 4 A patient with pyelonephritis shows restriction of diffusion at b ¼ 800 s/mm2 (arrow) and corresponding areas of low ADC in the left kidney (arrow).
Figure 5 There is a small T2 hyperintense (a) and T1 hypointense (b) mass at the lower pole of left kidney, which shows peripheral bright signal at DWI (c) and corresponding low signal on the ADC map (d). Histopathology showed it to be a clear cell carcinoma.
of histopathological grade is also possible solely based on DWI. A recent MRI study of renal tumours using DWI at 3 T, demonstrated an inverse linear relationship with the cellularity in renal malignancies.13 Whole-body DWI with background suppression (DWIBS; Fig 8) can be used to evaluate metastatic spread of RCC.4 However, as there is significant overlap between these ADC values, one cannot be confident in distinguishing benign from malignant renal neoplasm based on ADC values alone.14 Therefore, conventional MRI is still necessary for the optimal characterization of indeterminate renal masses and biopsy is often the final solution for this challenging question. DWI also helps to differentiate viable from necrotic areas within tumours.15 Therefore, it aids the selection of optimal target sites for biopsy and in the detection of response following radiation therapy, chemotherapy, or local ablative therapies.16 An increase in ADC values after therapy is considered a marker of response, whereas persistence of low ADC values is a sign of non-response.16 An important aspect of increase in ADC following treatment with chemotherapy and/or radiation is that this change may predate other morphological changes detected by conventional
MRI parameters, e.g., size, T2 signal. Therefore, it may serve as a useful biomarker to predict changes ahead of morphological RECIST criteria to assess treatment response.
Angiomyolipoma (AML). Among all renal neoplasms, angiomyolipomas (Fig 16) show minimum ADC values. This has been attributed to the muscle and fat component of AMLs.
Chronic renal failure (CRF) ADC values of renal parenchyma in patients with CRF are significantly lower (both cortex and medulla) than the ADC values of normal renal parenchyma (Fig 9). This has the potential to evolve as a tool for qualitative assessment of renal function and as a method for monitoring early renal allograft rejection.17,18
Other renal diseases The ADC of the renal cortex is lower in patients with renal artery stenosis.17 DWI also has the potential to recognize renal infarcts.19
Figure 6 Case of a renal TCC showing hydronephrosis (a) and surrounding soft-tissue mass with restricted diffusion (b) and low signal on the ADC map (c). Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
5
Figure 7 A T2 isointense tumour thrombus in the left renal vein branches (a; arrow) with high signal at b ¼ 800 s/mm2 (b) and hypointense signal on the ADC map (c), suggestive of restricted diffusion. Another patient with RCC shows tumour thrombus in IVC reaching up to the right atrium (d and g; arrows) and a metastatic lesion in the liver. The primary mass, thrombus in the IVC, and metastatic lesion all show restricted diffusion (eef).
Pelvicalyceal and ureter Hydronephrosis versus pyonephrosis The ADC value of the renal pelvis in pyonephrosis is lower than the values in hydronephrosis20 (Figs 10 and 11). Sometimes a large necrotic renal mass with pelvicalyceal extension may be mistaken for pyonephrosis at ultrasound, computed tomography (CT), or conventional MRI (Fig 10), but these can be differentiated based on DWI as such
tumours show peripheral restricted diffusion (Fig 12), whereas pyonephrosis shows a different pattern with restriction of diffusion in the entire renal pelvis or an appearance of fluidefluid level with restriction in dependent areas (Fig 12).
TCC In a study by Nishizawa et al.,21 renal pelvic and ureteric tumours (except carcinoma in situ) were shown clearly with
Figure 8 DWIBS shows metastatic lesions in the scalp, ribs, and lumbar vertebrae. Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
6
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
Figure 9 Upper panel shows a rejected transplant kidney in the right iliac fossa. Lower panel shows native kidney of a patient with CRF. Note is made of marked restriction of diffusion in both cases.
Figure 10 T2-weighted image (a) shows fluid signal inside a dilated pelvicalyceal system, which loses signal on the b ¼ 800 s/mm2 image (b) and the ADC map shows free diffusion, suggestive of simple hydronephrosis.
Figure 11 (a) Coronal half-Fourier axial single-shot fast spin-echo (HASTE), (b) T1 axial and (c) T2 FS axial images show fluid signal in the bilateral dilated pelvicalyceal system and staghorn calculus in left renal pelvis. (d) DWI image at b ¼ 800 s/mm2 and (e) the ADC map show fluidefluid levels with restriction of diffusion in dependent areas, suggestive of pyonephrosis. Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
7
Figure 12 (a) Axial T2-weighted image shows fluid signal inside the dilated pelvicalyceal system with peripheral enhancement on gadoliniumenhanced images (b, c). (d, e) DWI and ADC map show peripheral restriction, suggestive of necrotic RCC rather than pyonephrosis.
DWI (Fig 7). In addition, the infiltrating tumour had lower ADC values than that of papillary tumour.
Urinary bladder and prostate TCC
Lymphomas It is well established that lymphoma shows restricted diffusion, which is attributed to its high cellularity. We encountered a case of diffuse large B-cell lymphoma (DLBCL) with retroperitoneal lymph nodes and contiguous infiltration of the renal pelvis and circumferential ureteric wall thickening suggestive of infiltration. At DWI, it showed restricted diffusion in the soft tissue in the renal pelvis and in the soft tissue along the left ureter wall (Fig 13).
TCC is the major histological type of bladder cancer, which is further subdivided into the various histological grades. The histological grade of TCC is the most important factor that determines tumour progression and recurrence. There is a significant correlation between ADC values and histopathological grades,22 so ADC value has the potential to predict the biological behaviour of bladder cancer and tumour recurrence (Fig 14). However, the interpretation of DWI may be challenging due to the frequent occurrence of bladder clots in the vicinity, which may also show restricted diffusion.
Figure 13 A patient with recurrent diffuse large B-cell lymphoma shows left para-aortic lymph node with infiltrative T2 isointense (a) soft tissue in the left renal sinus showing restricted diffusion (b, c). The images in the lower panel show soft-tissue along the ureter (d), which also shows restricted diffusion (e, f). Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
8
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
Figure 14 (a) Axial T2-weighted image shows irregular bladder wall thickening showing restricted diffusion (bec) in a patient with carcinoma of urinary bladder.
Prostate carcinoma
Pitfalls
The majority of prostatic carcinomas arise from the peripheral zone, which are usually easy to diagnose due to their T2 hypointense signal on the background of the bright T2 signal of the normal peripheral zone (Fig 15aec). A significant minority of prostatic carcinomas arises in the transition zone, but a high prevalence of BPH makes it difficult to diagnose.23 There is growing evidence to show that DWI might help to detect carcinoma in the transition zone (Fig 15dee) and also to detect skeletal metastasis.24e26 However, it has its own limitations of poor spatial resolution, artefacts due to biopsy-related haemorrhage, and the overlapping ADC values.
Currently, DWI images have low spatial resolution; however, contrast resolution is good. It is also important to note that DWI does not work for lesions with a low intrinsic T2 signal (T2 blackout effect, Fig 16). DWI is also vulnerable to susceptibility effects. One such example is the effect of gadolinium: as gadolinium has significant susceptibility effects at higher concentration it can significantly decrease the T2 signal in the renal parenchyma and the collecting system due to high concentration at these sites (Fig 17). It can be avoided easily by simply performing DWI prior to the administration of gadolinium.
Figure 15 (a) Axial T2-weighted image shows subtle signal changes with hypointensity in the peripheral zone on left side. (bec) DWI shows restriction of diffusion at the corresponding location. (d, e) Lesion with restricted diffusion in the transition zone. Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
9
Figure 16 A case of angiomyolipoma showing bright signal on T1-weighted imaging (aeb) due to fat, and shows low signal on the fat-saturated T2weighted image (c). Lower panel shows that the signal at DWI (all b-values) and ADC is low due to lack of enough water protons (T2 blackout effect).
Future trends Predicting tumour perfusion (intravoxel incoherent motion) DWI was introduced in the 1980s and, initially, it was considered that only random Brownian motion was responsible for the generation of contrast in DWI. However, it
soon became clear that the motion of water through microvasculature also influences the signal at DWI.1 Because of the random orientation of the capillary network, motion of water molecules driven by perfusion mimics the properties of molecular diffusion, also called pseudo-diffusion. Therefore, DWI contrast is a result of phase dispersion under the combined effect of molecular diffusion and microvascular perfusion, known as intravoxel incoherent motion (IVIM). The influence of pseudo-diffusion is one order higher in magnitude due to the greater distances covered by the protons under its influence. As a result, the drop in signal at lower b-values (e.g., 0e100 s/mm2) is predominantly a result of perfusion effects and at higher b-values Brownian molecular diffusion dominates. As a result, the plot of signal intensity versus b-value is a bi-exponential function, and it is possible to calculate the perfusion fraction of tissue using IVIM analysis.27e30 However, this has its own limitations, because the diffusion fraction is subject to contamination from other tubular flow phenomena, such as the collecting tubular flow of the kidneys (31e33).
Summary
Figure 17 T1-weighted gadolinium-enhanced image shows loss of signal at the dependent location within the urinary bladder due to T2 effects (susceptibility).
DWI provides useful information about the local microenvironment of the diffusivity of water molecules in tissues, which is quantified using the ADC. In general, normal tissues show relatively free diffusion compared to malignant tumours, which show restricted diffusion because of high cell densities and a high nuclear-to-cytoplasmic ratio. Initially, the application of DWI in routine clinical practice was limited to stroke imaging, but during the past few years, its use has also been extended to body imaging. Initially DWI was seldom applied in body imaging because of technical difficulties; however, these difficulties have been overcome with the introduction of parallel imaging techniques, stronger gradient systems, and multi-channel coils. Consequently, it has now become an essential element of almost all abdominal MRI examinations. Currently, DWI has the
Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
10
V. Baliyan et al. / Clinical Radiology xxx (2014) 1e10
potential for tumour detection and characterization for several organs, including the kidney, prostate, and urinary bladder. In future, it is likely that the ADC will be used as an imaging biomarker to assess treatment response following chemo-radiotherapy.
17.
18.
References 1. Le Bihan D, Breton E, Lallemand D, et al. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 1988;168:497e505. 2. Charles-Edwards EM, deSouza NM. Diffusion-weighted magnetic resonance imaging and its application to cancer. Cancer Imaging 2006;6:135e43. 3. Yamashita Y, Tang Y, Takahashi M. Ultrafast MR imaging of the abdomen: echo planar imaging and diffusion-weighted imaging. J Magn Reson Imaging 1998;8:367e74. € ller MF, Prasad P, Siewert B, et al. Abdominal diffusion mapping with 4. Mu use of a whole-body echo-planar system. Radiology 1994;190:475e8. € rtz P, Krautmacher C, Tra €ber F, et al. Diffusion-weighted whole- body 5. Mu MR imaging with background body signal suppression: a feasibility study at 3.0 Tesla. Eur Radiol 2007;17:3031e7. 6. Skare S, Newbould RD, Clayton DB, et al. Clinical multishot DW-EPI through parallel imaging with considerations of susceptibility, motion, and noise. Magn Reson Med 2007;57:881e90. 7. Akisik FM, Sandrasegaran K, Aisen AM, et al. Abdominal MR imaging at 3.0 T. RadioGraphics 2007;27:1433e44. 8. Kilickesmez O, Yirik G, Bayramoglu S, et al. Non-breath-hold high bvalue diffusion-weighted MRI with parallel imaging technique: apparent diffusion coefficient in normal abdominal organs. Diagn Interv Radiol 2008;14:83e7. 9. Ries M, Jones RA, Basseau F, et al. Diffusion tensor MRI of the human kidney. J Magn Reson Imaging 2001;14:42e9. 10. Cova M, Squillaci E, Stacul F, et al. Diffusion weighted MRI in the evaluation of renal lesions: preliminary results. Br J Radiol 2004;77:851e7. 11. Thoeny HC, De Keyzer F, Oyen RH, et al. Diffusion-weighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience. Radiology 2005;235:911e7. 12. Notohamiprodjo M, Staehler M, Steiner N, et al. Combined diffusionweighted, blood oxygen level-dependent, and dynamic contrastenhanced MRI for characterization and differentiation of renal cell carcinoma. Acad Radiol 2013;20:685e93. 13. Manenti G, Di Roma M, Mancino S, et al. Malignant renal neoplasms: correlation between ADC values and cellularity in diffusion weighted magnetic resonance imaging at 3 T. Radiol Med 2008;113:199e213. 14. Zhang J, Tehrani YM, Wang L, et al. Renal masses: characterization with diffusion-weighted MR imagingda preliminary experience. Radiology 2008;247:458e64. 15. Razek AA, Megahed AS, Denewer A, et al. Role of diffusion-weighted magnetic resonance imaging in differentiation between the viable and necrotic parts of head and neck tumors. Acta Radiol 2008;49:364e70. 16. Buijs M, Kamel IR, Vossen JA, et al. Assessment of metastatic breast cancer response to chemoembolization with contrast agent enhanced
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29. 30. 31.
32.
33.
and diffusion-weighted MR imaging. J Vasc Interv Radiol 2007;18:957e63. Namimoto T, Yamashita Y, Mitsuzaki K, et al. Measurement of the apparent diffusion coefficient in diffuse renal disease by diffusionweighted echo-planar MR imaging. J Magn Reson Imaging 1999;9:832e7. Thoeny HC, Zumstein D, Simon-Zoula S, et al. Functional evaluation of transplanted kidneys with diffusion-weighted and BOLD MR imaging: initial experience. Radiology 2006;241:812e21. Yamanouchi Y, Yamamoto K, Noda K, et al. Renal infarction in a patient with spontaneous dissection of segmental arteries: diffusion- weighted magnetic resonance imaging. Am J Kidney Dis 2008;52:788e91. Merkle EM, Nour SG, Lewin JS. MR imaging follow-up after percutaneous radiofrequency ablation of renal cell carcinoma: findings in 18 patients during first 6 months. Radiology 2005;235:1065e71. Nishizawa S, Imai S, Okaneya T, et al. Diffusion weighted imaging in the detection of upper urinary tract urothelial tumors. Int Braz J Urol 2010;36:18e28. Kanazawa S, Matsuki M, Inada Y, et al. Diffusion-weighted MR imaging for urinary bladder carcinoma: ADC values among tumor histologic grades. Bull Osaka Med Coll 2008;54:1e6. McNeal JE, Redwine EA, Freiha FS, et al. Zonal distribution of prostatic adenocarcinoma: correlation with histologic pattern and direction of spread. Am J Surg Pathol 1988;12:897e906. Hosseinzadeh K, Schwarz SD. Endorectal diffusion-weighted imaging in prostate cancer to differentiate malignant and benign peripheral zone tissue. J Magn Reson Imaging 2004;20:654e61. Kim CK, Park BK, Lee HM, et al. Value of diffusion-weighted imaging for the prediction of prostate cancer location at 3 T using a phased-array coil: preliminary results. Invest Radiol 2007;42:842e7. € fer R, Blumstein N, et al. Prostate carcinoma: diffusionLuboldt W, Ku weighted imaging as potential alternative to conventional MR and 11 C-choline PET/CT for detection of bone metastases. Radiology 2008;249:1017e25. Le Bihan D, Breton E, Lallemand D, et al. MR imaging of intra-voxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986;161:401e7. Le Bihan D, Turner R, Moonen CT, et al. Imaging of diffusion and microcirculation with gradient sensitization: design, strategy, and significance. J Magn Reson Imaging 1991;1:7e28. Le Bihan D. IVIM method measures diffusion and perfusion. Diagn Imaging (San Franc) 1990;12. 133, 136. Le Bihan D. Intravoxel incoherent motion perfusion MR imaging: a wake-up call. Radiology 2008;249:748e52. Yoshino N, Yamada I, Ohbayashi N, et al. Salivary glands and lesions: evaluation of apparent diffusion coefficients with split-echo diffusionweighted MR imagingdinitial results. Radiology 2001;221:837e42. Zhang L, Murata Y, Ishida R, et al. Functional evaluation with intra- voxel incoherent motion echo-planar MRI in irradiated salivary glands: a correlative study with salivary gland scintigraphy. J Magn Reson Imaging 2001;14:223e9. Muller MF, Prasad PV, Edelman RR. Can the IVIM model be used for renal perfusion imaging? Eur J Radiol 1998;26:297e303.
Please cite this article in press as: Baliyan V, et al., Diffusion-weighted imaging in urinary tract lesions, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.011
