Multiparametric MRI of solid renal masses: pearls and pitfalls

Clinical Radiology xxx (2014) e1ee13

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Pictorial Review

Multiparametric MRI of solid renal masses: pearls and pitfalls N.K. Ramamurthy a, B. Moosavi a, M.D.F. McInnes a, T.A. Flood b, N. Schieda a, * a

Department of Radiology, The Ottawa Hospital, The University of Ottawa, Civic Campus C1 1053 Carling Avenue, Ottawa, Ontario, Canada, K1Y 4E9 b Division of Anatomical Pathology, The Ottawa Hospital, The University of Ottawa, 501 Smyth Road, 4th Floor CCW, Room 4278, Ottawa, Ontario, Canada, K1Y 4E9

art icl e i nformat ion Article history: Received 24 August 2014 Received in revised form 4 October 2014 Accepted 8 October 2014

Functional imaging [diffusion-weighted imaging (DWI) and dynamic contrast enhancement (DCE)] techniques combined with T2-weighted (T2W) and chemical-shift imaging (CSI), with or without urography, constitutes a comprehensive multiparametric (MP) MRI protocol of the kidneys. MP-MRI of the kidneys can be performed in a time-efficient manner. Breath-hold sequences and parallel imaging should be used to reduce examination time and improve image quality. Increased T2 signal intensity (SI) in a solid renal nodule is specific for renal cell carcinoma (RCC); whereas, low T2 SI can be seen in RCC, angiomyolipoma (AML), and haemorrhagic cysts. Low b-value DWI can replace conventional fat-suppressed T2W. DWI can be performed free-breathing (FB) with two b-values to reduce acquisition time without compromising imaging quality. RCC demonstrates restricted diffusion; however, restricted diffusion is commonly seen in AML and in chronic haemorrhage. CSI must be performed using the correct echo combination at 3 T or T2* effects can mimic intra-lesional fat. Twodimensional (2D)-CSI has better image quality compared to three-dimensional (3D)-CSI, but volume averaging in small lesions can simulate intra-lesional fat using 2D techniques. SI decrease on CSI is present in both AML and clear cell RCC. Verification of internal enhancement with MRI can be challenging and is improved with image subtraction. Subtraction imaging is prone to errors related to spatial misregistration, which is ameliorated with expiratory phase imaging. SI ratios can be used to confirm subtle internal enhancement and enhancement curves are predictive of RCC subtype. MR urography using conventional extracellular gadolinium must account for T2* effects; however, gadoxetic acid enhanced urography is an alternative. The purpose of this review it to highlight important technical and interpretive pearls and pitfalls encountered with MP-MRI of solid renal masses. Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Introduction * Guarantor and correspondent: N. Schieda, Department of Radiology, The Ottawa Hospital, The University of Ottawa, 1053 Carling Avenue, Ottawa, Ontario, Canada, K1Y 4E9. Tel.: þ1 613 759 0958; fax: þ1 613 737 8830. E-mail address: [email protected] (N. Schieda).

CT remains the most widely used technique for the characterization of renal masses1,2 and is considered “the most important technique” for evaluating the indeterminate renal mass by the American College of Radiology (ACR).2 MRI

http://dx.doi.org/10.1016/j.crad.2014.10.006 0009-9260/Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Ramamurthy NK, et al., Multiparametric MRI of solid renal masses: pearls and pitfalls, Clinical Radiology (2014), http://dx.doi.org/10.1016/j.crad.2014.10.006

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Table 1 Multiparametric MRI protocol performed at both 1.5 and 3 T.a Half-Fourier single-shot turbo spin echob

Chemical shift (IP þ OP)

Diffusion-weighted imagingc

FS 3D gradient-recalled echo (GRE)d

Post-gadoliniume dynamic FS 3D GRE

Imaging plane Fat suppression

Coronal, sagittal, axial N/a

Axial N/a

Physiologyf Volumetryg Section thickness (mm) Matrix Field of view (mm)

Breath-hold 2D or 3D 3e5h 128  128 400  400

Axial Spectral adiabatic inversion recovery Breath-hold 3D 4 224  204 400  400

Axial, coronal þ sagittal delay Spectral adiabatic inversion recovery Breath-hold 3D 4 224  204 400  400

TE/TR (msec)

Breath-hold 2D 6, 6, 5 384  256 400  400 coronal; 350  350 axial 90/1250e1500

Axial Spectral adiabatic inversion recovery Free-breathing 2D 5 128  128 400  400

Flip angle (degrees) Bandwidth (Hz) Acceleration Number of signals averaged

90 325 2 1

1.3e2.5/4.2; 1.1e2.3/4.1; 2.3e4.5/170i 70

4.8/3400

1.7/3.8

1.7/3.8

70

2 1

2 1,4,6j

12 1100 2 1

12 1100 2 1

FS, fat-suppressed; IP, in phase; OP, opposed phase; 3D, three-dimensional 2D, two-dimensional; TE/TR, echo time/repetition time. a MRI performed on four clinical MR systems including at 1.5 T (Symphony, Siemens Medical, Malvern PA, USA) and at 3 T (TRIO, Siemens Medical, and Discovery 750W, General Electric Health Care, Milwaukee, WI, USA). Combined surface (four channels for Symphony, six channels for TRIO, eight channels for Discovery) with activated spine array. b HASTE (Siemens Medical) and ssFSE (General Electric Medical). c Diffusion-weighted imaging performed with spectral fat suppression echo planar imaging with tri-directional motion probing gradients and b-values of 0, 600 mm2/sec with automatic apparent diffusion coefficient map generation using mono-exponential curve fitting. d VIBE (Siemens Medical) and LAVA (General Electric Medical). e Four phases acquired dynamically starting with the cortico-medullary phase timed empirically at 35 s, followed by the nephrographic phase at 120 s postinjection. Axial, coronal, and sagittal delayed sequences are also performed. Gadolinium injected at a concentration of 0.1 mmol/kg using gadobutrol (Gadovist, Bayer, Toronto, ON, Canada) at a rate of 3 ml/s. f All breath-holds performed with end expiration. g 3D sequences (VIBE or LAVA), 2D sequences are fast low-angled shot (FLASH, Siemens Medical) or spoiled GRE (spGRE, General Electric Medical). h 3 mm for three-dimensional and 5 mm for two-dimensional acquisition. i TE/TR times for TRIO; Discovery 750W and Symphony respectively. j Number of signals averaged partitioned by b-value on 3 T Discovery 750 W (one for b ¼ 0, six for b ¼ 600 mm2/sec) and a standard of four signals used for b ¼ 0 and 600 mm2/sec on 3 T TRIO and 1.5 T Symphony scanners.

is considered comparable to CT by the ACR2 and offers several advantages over CT including: improved contrast resolution, functional imaging techniques, and the lack of ionizing radiation, which is of particular significance due to growing concerns over cumulative radiation exposure from multi-phase and repeat CT examinations. The non-ionizing property of MRI is critical for patients who undergo frequent repeat imaging examinations screening for renal cell carcinoma (RCC) including those patients with tuberous sclerosis (TS) and Von HippeleLindau disease. Furthermore, in a recent study, Willatt et al. demonstrated that MRI further characterized a large proportion of renal masses that were considered indeterminate at CT.3 Conventional renal MRI protocols include T2-weighted (T2W), chemical shift imaging [CSI; in and opposed phase (IP þ OP)], and fat-suppressed (FS) T1W sequences before and after gadolinium injection.4e7 Combining this protocol with dynamic contrast enhancement (DCE) and diffusion-weighted imaging (DWI) constitutes a multiparametric (MP) MRI protocol (Table 1). MP-MRI is rapidly becoming the reference standard for renal MRI.4e7 For depiction of the urothelium, MP-MRI is combined with MR urography (MRU). MP-MRI can be performed in a timeefficient manner and provides important information that is not available with standard renal MRI. The purpose of this review is to highlight important pearls and pitfalls of

Figure 1 A 74-year-old male patient with Fuhrman grade 3 cc-RCC. Coronal T2W HASTE image demonstrates a well-circumscribed mass arising from the lower pole of the left kidney (white arrow). The mass is heterogeneously hyperintense to the adjacent renal cortical parenchyma, a specific imaging finding of RCC. Marked CM phase enhancement with washout on the NG phase was observed on DCE imaging (not shown) and combined with heterogeneously increased T2W SI is specific for cc-RCC subtype.

Please cite this article in press as: Ramamurthy NK, et al., Multiparametric MRI of solid renal masses: pearls and pitfalls, Clinical Radiology (2014), http://dx.doi.org/10.1016/j.crad.2014.10.006

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Figure 2 (a) A 37-year-old female patient with minimal-fat AML; (b) a 64-year-old man with p-RCC; and (c) a 53-year-old woman with a haemorrhagic cyst illustrating the differential diagnosis of low T2W signal intensity (SI) renal lesions. Axial T2W ssFSE (top) and axial fat only image [derived from T1W gradient recalled echo (GRE) two-point DIXON IP and OP imaging; bottom] in (a) demonstrate a small homogeneously low T2W SI nodule arising from the medial interpolar region of the left kidney (white arrow) with intralesional fat (white arrowhead). The nodule enhanced rapidly on CM phase imaging (not shown) and RCC was suggested. Diagnosis of minimal-fat AML was confirmed after partial nephrectomy. In retrospect, the diagnosis of minimal-fat AML may have been suggested given that the combination of homogeneously low T2W SI and microscopic fat has not been described in RCC. Axial T2W ssFSE (top) and axial pre-contrast CM and NG phase contrast-enhanced T1W FS GRE images (bottom) in (b) demonstrate typical imaging features of p-RCC arising from the medial interpolar region of the left kidney. The tumour is homogeneously hypointense on T2W imaging (long white arrow) and is haemorrhagic with minimal delayed enhancement (short white arrows). Also note large parapelvic cyst in (b). Axial T2W ssFSE (top), axial pre-contrast FS T1W GRE and CE subtraction image (left to right, bottom) demonstrates a typical haemorrhagic cyst in the right kidney. The cyst is of low T2W SI (long white arrow), increased T1W SI precontrast and is non-enhancing (short white arrows). Also note a complex Bosniak type IIF cyst in the anterior right kidney with thin enhancing septa for which the patient was being imaged.

renal MP-MRI using a sequence-based approach. As illustrated in this review, MP-MRI provides new insights into the nature of renal masses; however, it may also result in technical and interpretive errors in less experienced users.

T2W imaging T2W imaging is essential to differentiate solid from cystic renal masses and can also help to characterize indeterminate solid renal masses. A solid renal mass that is

Figure 3 A 34-year-old man with small p-RCC, 5  9  6 mm (anterioreposterior  transverse  craniocaudal) homogeneously low T2W SI nodule is barely perceptible on axial T2W ssFSE image (curved arrow in a) and much more apparent on sagittal T2W ssFSE image (white arrow in b). Multiplanar imaging is recommended for renal masses, because small renal nodules may be better depicted in a particular imaging plane due to the orientation of the kidneys. Please cite this article in press as: Ramamurthy NK, et al., Multiparametric MRI of solid renal masses: pearls and pitfalls, Clinical Radiology (2014), http://dx.doi.org/10.1016/j.crad.2014.10.006

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Figure 4 A 78-year-old female patient with large Fuhrman grade 3 cc-RCC in the left kidney. Axial (a) IP, (b) OP T1W GRE, and (c) axial subtraction (IP-OP) image demonstrates a large renal mass in the left kidney with intralesional fat (white arrowheads). A significant (>25%) SI drop on OP compared to IP imaging in RCC is specific for clear cell subtype and is due to the presence of intracytoplasmic lipid within clear cells. The presence of adipocytes in RCC is rare.

heterogeneously hyperintense to the renal cortex on T2W imaging is most likely a RCC,8 and usually of clear cell subtype7 (cc-RCC; Fig 1). T2W lesion-to-renal parenchyma signal intensity (SI) ratios can discriminate RCC from benign angiomyolipoma (AML) with high degrees of accuracy.8 Although low T2W SI is considered typical for AML,8e10 low T2W SI is also commonly present in both papillary RCC (p-RCC) and haemorrhagic cysts11e13 (Fig 2). The overlap in T2W SI between p-RCCs and AMLs without visible fat often necessitates histological confirmation. Haemorrhagic cysts rarely pose a diagnostic dilemma, as their increased T1W SI and lack of enhancement will readily differentiate them from solid neoplasms14 (Fig 2). T2W imaging is performed as breath-hold (BH) halfFourier single-shot turbo spin-echo (ss-TSE) with parallel imaging (PI; Table 1).15 Compared to standard TSE, ss-TSE provides improved spatial and contrast resolution, less

artefacts, and time efficiency.15 Three-plane acquisition is advised because the visibility of small renal lesions may depend on renal orientation (Fig 3). Image blur with ss-TSE is ameliorated with PI.16 ss-TSE can be performed with FB or respiratory-triggered (RT) techniques in non-cooperative patients.17

CS (IP D OP) imaging In 1997, Outwater et al.18 reported that cc-RCC demonstrates a SI decrease on CS-MRI due to the intracellular or intracytoplasmic lipid18,19 (Fig 4). Intracellular lipid is defined as fat molecules within the cytoplasm of cells, which differs from the presence of adipocytes (fat cells), which are only rarely present in RCC.20e24 A significant SI drop (CSI SI index > 25%) in RCC is characteristic of cc-RCC subtype,12,18,25 whereas other RCC only rarely demonstrate

Figure 5 A 42-year-old woman with classic (triphasic) AML in the right kidney. Axial T2W ssFSE image (a) demonstrates a large mass in the medial interpolar region of the right kidney (white arrow) that is iso-intense to the adjacent perinephric fat. Axial FS b ¼ 0 mm2/sec EPI image demonstrated homogeneous suppression of SI within the mass (white arrow in b) features consistent with bulk fat and the diagnosis of AML. Note that fat is of increased SI on FSE imaging related to J-coupling effects and that the low b-value FS EPI can serve as a surrogate for conventional FS T2W FSE imaging as a time-saving measure. Also note right parapelvic cyst (arrowheads) which is nearly isointense to renal pelvis in both (a) and (b). Please cite this article in press as: Ramamurthy NK, et al., Multiparametric MRI of solid renal masses: pearls and pitfalls, Clinical Radiology (2014), http://dx.doi.org/10.1016/j.crad.2014.10.006

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minimal SI drop on CS-MRI.25 AML are composed of variable amounts of smooth muscle, blood vessels, and adipocytes.26 The depiction of gross fat at CT or with FS MRI is considered diagnostic of AML27e30 (Fig 6). Only rarely do RCC demonstrate gross internal fat content from various causes, including osseous metaplasia and engulfing of the renal sinus fat, which is a known pitfall for the diagnosis of AML. In these rare cases, the presence of synchronous calcification and fat within a renal mass favours the diagnosis of RCC.31 Less concentrated areas of fat cells within AML result in a SI drop on CS-MRI and are referred to as areas of microscopic fat. Microscopic fat is also variably detected in the 5% of AML that do not contain sufficient amounts of fat to be characterized with conventional MRI (minimal fat or

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fat poor AML)10,13,32 (Fig 2). Although intracellular lipid and microscopic fat are readily differentiated at histopathology, they both result in SI drop at CS-MRI. Therefore, the presence of SI drop on CS-MRI is non-specific, as it can be seen in both RCC and AML.10,33 Fortunately, CS-MRI in combination with other MRI findings is typically characteristic. In a mass that contains both SI-drop on CS-MRI and bulk fat, the diagnosis of classic AML is established.28,29 SI drop in a mass that is heterogeneously hyperintense on T2W imaging and hyperenhancing is virtually pathognomonic for cc-RCC7,12,13 (Fig 4). Conversely, a significant SI drop on CS-MRI in a solid renal mass that is homogeneously hypointense on T2W imaging may represent a minimal-fat or fat-poor AML,

Figure 6 A 64-year-old male patient with p-RCC depicted in Fig 2(b). The tumour is heterogeneously hyperintense on axial IP T1W GRE imaging in (a) with internal SI drop (white arrow) on the corresponding axial OP image in (b). This finding is confirmed (arrowhead) on the fat-only image in (c) and suggests the presence of intralesional fat. The combination of intralesional fat and homogeneously low T2W SI (see Fig 2b) is typical of minimal-fat AML and has not been described in p-RCC. The spurious SI drop on OP compared to IP imaging in this patient is related to erroneous selection of echo times (TEs) for CSI at 3 T. Note that IP echo (TE ¼ 2.5 ms in a) was recorded before the OP echo (TE ¼ 3.7 ms in b) and that using this echo combination, a SI drop on OP image becomes ambiguous and can be due to intralesional fat or T2* effects. In this example, the p-RCC demonstrates calcification on the corresponding unenhanced CT image (curved arrow in d) and haemorrhage on precontrast FS T1W GRE imaging (see Fig 2b) and susceptibility effects on the later TE OP image mimic the presence of intralesional fat. Because the fat-only image obtained from a two-point DIXON technique displays the difference between the IP and OP echoes, the susceptibility artefact is erroneously displayed as fat. The diagnosis of haemorrhagic p-RCC with calcifications was confirmed after partial nephrectomy. Please cite this article in press as: Ramamurthy NK, et al., Multiparametric MRI of solid renal masses: pearls and pitfalls, Clinical Radiology (2014), http://dx.doi.org/10.1016/j.crad.2014.10.006

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CS-MRI should be performed by sampling the first echo pair during the same BH and in the correct order (OP before IP echo).34 At 3 T, because the first OP echo occurs at 1.1 ms, sampling the first echo pair is challenging and requires high receiver bandwidths.34e36 This technical limitation can be overcome34; however, sampling the first IP and later OP echoes should not be performed because SI drop on the OP images could be due to either intralesional fat or susceptibility (T2*) effects34,37 (Fig 6). CS-MRI can be performed using a two-dimensional (2D) or three-dimensional (3D) technique. 3D techniques improve spatial resolution and signal-to-noise ratio (SNR) and 2D acquisitions are more resistant to motion artefact. Slight improvements in image quality occur with 2D compared to 3D CS-MRI at both 1.5 and 3 T38e40; however, volume averaging at 2D is problematic when India-ink artefact can be confused for intralesional fat. This occurs when lesion size is less than two-times the section thickness (Fig 7).

DWI

Figure 7 A 34-year-old man with small p-RCC depicted in Fig 3. Axial 2D IPeOP images (a) and 3D IPeOP images (b) were obtained at section thicknesses of 5 and 3 mm, respectively. On the 2D images there is internal SI drop on the OP image compared to the IP image (white arrow in a). The combination of homogeneously low T2W SI (see Fig 3) and intralesional fat resulted in a diagnosis of a minimal-fat AML and targeted biopsy, which was performed using ultrasound guidance. A diagnosis of p-RCC was confirmed at histopathology. In retrospect, the SI drop observed using 2D imaging in (a) is not present on the 3D imaging (white arrow in b) and is due to a volume-averaging artefact from India-ink artefact at the interface of the nodule and the retroperitoneal fat. Although 2D CSI provides slightly better imaging quality compared to 3D techniques, volume averaging (which occurs when lesion size is less that two-times the section thickness) can mimic intralesional fat. In this example, the tumour measured 6 mm in the craniocaudal dimension.

as this combination of findings has not been reported in RCC10 (Fig 2). In our practice, we recommend surveillance or histological sampling for the latter because the diagnosis of minimal-fat AML is likely.

DWI has revolutionized abdominal MRI. A detailed explanation of DWI is beyond the scope of this manuscript but is described elsewhere.41,42 Briefly, DWI exploits the random motion of water molecules in differing environments to determine tissue cellularity.41 Although techniques vary, a FS single-shot spin-echo echo-planar imaging (EPI) sequence is typically performed.43,44 EPI can be performed as a BH; however, FB or RT techniques are preferred to improve image quality and sample multiple bvalues.42,45,46 RT reduces motion artefact but results in prolonged acquisition times compared to FB, and FB DWI demonstrates comparable image quality to RT.45 Increasing the number of excitations (NEX) overcomes many of the artefacts observed with EPI.42,44 Choice of b-value and number of b-values is variable. A minimum of two b-values is required to generate an apparent diffusion coefficient (ADC) map.41 Typically strategies involve either two [short (<200) and long (>500) mm2/sec] or three or more bvalues; the more b-values (particularly when >500 mm2/ sec) selected, the longer the acquisition time. We perform DWI with two b-values to reduce scan time (Table 1); a

Figure 8 A 34-year-old man with small p-RCC depicted in Figs. 3 and 7. (a) Axial b0 mm2/sec, (b) b ¼ 600 mm2/sec, and (c) ADC map illustrates the utility of DWI in renal mass imaging. On the long b-value EPI image (b) the nodule is much more apparent compared to the short b value EPI image (a) improving lesion detection (white arrows). The nodule demonstrates restricted diffusion with low SI on ADC map (c), a finding that is suggestive of malignancy. Please cite this article in press as: Ramamurthy NK, et al., Multiparametric MRI of solid renal masses: pearls and pitfalls, Clinical Radiology (2014), http://dx.doi.org/10.1016/j.crad.2014.10.006

Figure 9 A 78-year-old female patient with chronic renal failure on haemodialysis and a p-RCC in the right kidney. (a) Coronal T2W ssFSE image demonstrates atrophic kidneys with multiple tiny cysts in both kidneys, typical findings in chronic renal failure with dialysis-induced cystic disease. There is a homogeneously low T2W SI mass in the lower pole of the right kidney (white arrow). Axial b ¼ 0 mm2/sec, b800 mm2/sec and ADC map (left to right in b) demonstrates restricted diffusion within the mass (curved arrows). The mass was isointense on T1W imaging (not shown), which excluded a haemorrhagic cyst. No internal fat was present and the mass developed de novo when compared to a baseline CT performed 5 years earlier (not shown), which effectively excluded AML as a potential cause. Therefore, the diagnosis of p-RCC was suggested and confirmed after total nephrectomy.

Figure 10 An 87-year-old woman with classic (triphasic) AML. (a) Axial IP, (b) OP, and (c) FS 3D T1W GRE images demonstrate a nodule arising from the posterior interpolar region of the right kidney. The nodule contains minute foci of bulk fat (arrowheads) that are of increased T1W SI in (a), demonstrate etching artefact with the adjacent kidney in (b) and lose SI on the FS image in (c). The diagnosis of AML was readily established. Corresponding axial b ¼ 0 mm2/sec (d), b ¼ 600 mm2/sec (e) and ADC map (f) demonstrates restricted diffusion in the AML (open white arrows).

Figure 11 A 53-year-old woman with a haemorrhagic cyst in the right kidney (Fig 2c). The cyst is of low T2W SI on coronal T2W ssFSE image (white arrow in a). Also note bilateral renal cysts in (a). There is restricted diffusion on b ¼ 0 mm2/sec, b ¼ 600 mm2/sec EPI and ADC map (left to right in b) in the haemorrhagic cyst. Note that the haemorrhagic cyst demonstrates preserved SI on the b ¼ 600 mm2/sec (white arrow) compared to the b ¼ 0 mm2/sec (arrowhead) EPI and is of low SI on ADC map (curved arrow). Conversely, a simple cyst in the anterior interpolar region of the right kidney demonstrates a loss of SI on the b ¼ 600 mm2/sec compared to the b ¼ 0 mm2/sec EPI and T2 shine-through on the ADC map at the same level. Haemorrhagic cysts may demonstrate restricted diffusion due to internal viscosity but can be readily differentiated from solid renal masses by increased T1W SI on pre-contrast imaging and lack of enhancement (see Fig 2c). Please cite this article in press as: Ramamurthy NK, et al., Multiparametric MRI of solid renal masses: pearls and pitfalls, Clinical Radiology (2014), http://dx.doi.org/10.1016/j.crad.2014.10.006

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single long b-value of 600 mm2/sec has been previously shown to be the best discriminator between benign and malignant tissues.47 There are three principle applications of DWI for renal imaging. First, low b-value trace EPI can serve as a surrogate for FS T2W imaging, decreasing total examination time48 (Fig 5). This strategy has been previously validated for hepatic imaging at 1.5 T48; however, image quality of EPI is limited at 3 T (due to artefact from cardiac motion and the lung bases).43,44 In our experience, because of decreased

motion and retroperitoneal location, image quality of EPI is satisfactory for the evaluation of the kidneys even at high field strength. Second, the long b-value trace EPI increases the conspicuity of renal lesions improving lesion detection (Fig 8). Lastly, the presence or absence of restricted diffusion can potentially characterize renal lesions.7,49,50 Preliminary results using DWI to characterize solid renal lesions as malignant are encouraging, and DWI can be particularly useful when gadolinium is contraindicated or when enhancement is equivocal (Fig 9). Taouli et al.51 initially demonstrated lower ADC values in renal neoplasms compared with benign lesions. In a recent metaanalysis, Lassel et al.52 demonstrated significantly lower ADC values in RCCs compared to oncocytomas and benign renal tissue. DWI can also potentially distinguish between RCC subtypes. Both p-RCC and chromophobe RCC demonstrate significantly lower ADC values when compared to ccRCC at both 3 T53 and 1.5 T.51 The utility of threshold ADC values for diagnosis is currently limited due to differences in acquisition parameters and intrinsic scanner variability.54 Lower ADC values have also been described in higher Fuhrman grade cc-RCC compared to lower Fuhrman grade cc-RCC55; suggesting that DWI may be useful in guiding patient selection for targeted molecular therapy or the active surveillance of small renal neoplasms. A potential pitfall of DWI in renal mass imaging is that benign lesions also exhibit restricted diffusion and may mimic neoplasia. Both classic triphasic AML and minimalfat AMLs may show profound diffusion restriction,56 with similar ADC values compared to p-RCC. In classic AML, the presence of macroscopic fat is diagnostic (Fig 10). Chronic haemorrhagic cysts may also demonstrate restricted diffusion due to internal viscosity and “T2 black-out” effects.57 T1W hyperintensity, lack of enhancement, rim calcification and stability over multiple imaging studies is diagnostic14 (Fig 11). Infection, including pyelonephritis and abscess, also commonly results in restricted diffusion, although diagnosis is usually readily established by clinical history and laboratory analysis.58

Gadolinium-enhanced sequences Figure 12 A 62-year-old male patient with p-RCC illustrates the challenges of confirming enhancement in minimal-enhancing lesions at MRI. A subtraction image (a) which was obtained from pre-contrast and 4 min post-contrast delayed-phase FS T1W GRE (left to right in b) demonstrates increased SI within a renal nodule in the anterior interpolar region of the right kidney suggestive of internal enhancement, which could not be readily established by visually comparing the pre- and post-contrast images in (b). However, when comparing the quality of the image subtraction, it is apparent that spatial misregistration has occurred because the pre-contrast image and post-contrast image were obtained at different levels within the tumour (left to right in c) identified by cross-reference lines on sagittal T2W images in (c). This commonly occurs when BH is not identical between acquisitions. The use of a SI ratio [(Post-contrast SI e Pre-contrast SI)/Pre-contrast SI  100%] can be used to confirm enhancement when subtraction imaging fails. In this tumour, SI ratio [(534e420)/420  100] is 27% which confirms enhancement.

FS T1W GRE sequences, before and after gadolinium, are necessary for renal MRI and should be performed unless there is a contraindication to gadolinium. In patients at risk for nephrogenic systemic fibrosis (NSF) due to renal impairment (estimated glomerular filtration rate <30 ml/ min), the use of gadolinium can now be considered if iodinated contrast medium is contraindicated; however, extreme caution should be exercised, and gadopentetate dimeglumine (Magnevist), gadoversetamide (Optimark), and gadodiamide (Omniscan) should be avoided.59,60 Gadolinium is particularly beneficial in patients who have had a previous severe allergic reaction to iodinated contrast agents.59 The use of non-contrast-enhanced sequences to quantify tumour perfusion, such as arterial spin labelling (ASL), demonstrate promising preliminary results but require further validation on a larger scale.61,62 FS T1W GRE

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Figure 13 A 78-year-old woman with a large Fuhrman grade 3 cc-RCC in the left kidney (Fig 4). (a) Axial pre-contrast, (b) CM, (c) NG, and (d) 4min delayed contrast-enhanced FS T1W 3D GRE images demonstrate avid enhancement on the CM phase (greater than adjacent renal cortical parenchyma anteriorly) and washout kinetics on the NG and delayed-phase imaging. This enhancement pattern in combination with intracytoplasmic lipid (see Fig 4) and heterogeneously increased T2W SI (not shown) is characteristic of cc-RCC.

Figure 14 A 64-year-old man with p-RCC (Fig 2b). (a) Axial pre-contrast, (b) CM, (c) NG, and (d) 4-min delayed contrast-enhanced FS T1W 3D GRE images demonstrate minimal progressive enhancement over time which, in combination with low T2W SI (see Fig 2b), is characteristic of pRCC subtype.

sequences are typically performed using a 3D interpolated technique to enhance spatial resolution. 3D GRE sequences are prone to motion artefact, which is overcome by BH. BH is more consistent with end-expiratory (compared to endinspiratory) scanning, which improves subtraction imaging12; however, the duration of the BH (and therefore, anatomical coverage) is decreased. Typically, endexpiratory BH is sufficient for renal coverage and is suggested for renal mass imaging. 2D techniques, RT, or radial

acquisitions can reduce motion artefact with necessary comprises in resolution or acquisition time.63 To confirm subtle enhancement with MRI, subtraction imaging is generally performed; however, this technique is highly dependent on consistency of BH and does not work when data sets are not perfectly co-registered (Fig 12). Assessment of the degree of ghosting artefact around the renal contour and adjacent parenchyma has been suggested as a means to determine the degree of misregistration12;

Figure 15 A 54-year-old woman with haematuria and severe previous allergy to iodinated contrast medium, imaged with conventional extracellular gadolinium-enhanced MRU demonstrates poor-quality MRU due to insufficient gadolinium dilution. Full-strength gadolinium injection without dilution or diuretic administration results in markedly concentrated gadolinium in the collecting systems and strong T2* effects that overwhelm the T1 shortening properties of gadolinium. Axial T1W 2D GRE images obtained at the interpolar region of the kidneys (a) and mid-ureters (b) demonstrate blooming artefact in the bilateral renal pelves and bilateral ureters (white arrow and arrowheads). The left collecting system is also completely collapsed (arrowheads) due to the lack of appropriate pre-hydration and diuresis. Please cite this article in press as: Ramamurthy NK, et al., Multiparametric MRI of solid renal masses: pearls and pitfalls, Clinical Radiology (2014), http://dx.doi.org/10.1016/j.crad.2014.10.006

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however, in our experience cross-referencing the two images that are to be subtracted to a fixed reference (the spine) is a more reliable method to determine whether subtraction will be accurate (Fig 12). Quantitative assessment using SI ratios [SIR ¼ (SIpost  SIpre)/SIpre  100%; where post is the post-gadolinium enhanced image and pre is the pregadolinium image] can also be used to confirm enhancement in difficult cases. Using a threshold value of 15e20% (2e4 min post-contrast) to confirm enhancement provides excellent sensitivity and specificity for differentiating solid and cystic renal lesions64 (Fig 12). Previously, Hecht et al.65 demonstrated that qualitative assessment of subtracted images is superior to SIR to detect enhancement in renal masses65; however, SIR remain of value when subtraction images are not adequately co-registered. It should be noted that quantification of enhancement in renal masses is better suited to the density measurements obtained at CT rather than SI measurements obtained at MRI due to technical variability in SI measures at MRI and the more linear relationship between iodine concentration and radiodensity at CT. The acquisition of contrast-enhanced images in a dynamic fashion [corticomedullary (CM), nephrographic (NG) and excretory phases (EP)] yields important information for the characterization of renal masses. Studies evaluating quantitative assessment of DCE have consistently shown that cc-RCC enhance to a greater degree than the renal

Figure 16 A 61-year-old man with previous bladder cancer status post-total cysto-prostatectomy and neo-bladder formation and severe allergy to iodinated contrast medium imaged with conventional extracellular gadolinium-enhanced MRU demonstrates excellentquality MRU. Prior to the examination, the patient received 500 ml of normal saline intravenously and just prior to the injection of diluted (half-dose) gadolinium, furosemide was also administered intravenously. The hydration in combination with furosemide and dilute gadolinium results in lower concentrations of gadolinium in the collecting system and exploits the T1 shortening effects of gadolinium rather than the T2* effects, which occur when gadolinium is concentrated. Hydration and furosemide also serve to increase renal excretion and better distend the collecting systems. Coronal maximum intensity projection (MIP) images obtained from source 3D T1W FS GRE demonstrate high-quality MRU images of the bilateral collecting systems, including the ureters (arrowheads), renal pelvis, and calyceal system (arrow), in this patient with neo-bladder reconstruction.

cortex during the corticomedullary phase of enhancement and washout during the nephrographic phase (Fig 13), whereas p-RCC enhance less than the renal cortex on both phases of enhancement and demonstrate gradual progressive enhancement (Fig 14).7 DCE shows promise for differentiation of AML without visible fat from p-RCC, which are otherwise difficult to differentiate due to similar low SI on T2WI. Although SI drop at CS-MRI in combination with low T2W SI is suggestive of minimal fat AML, a proportion of these AML will not demonstrate SI drop due to a paucity of microscopic fat.66 p-RCCs enhance more slowly than AMLs using a wash-in arterial index13; therefore, the combination of homogeneous low T2W SI and rapid arterial enhancement is suggestive of minimal-fat AML rather than pRCC.7,66 A single study demonstrated that oncocytoma could be differentiated from chromophobe and cc-RCCs based on delayed enhancement with high specificity13 and the imaging finding of segmental enhancement inversion has been described as a specific imaging finding of oncocytoma67; however, other studies have been unable to

Figure 17 A 34-year-old woman with suspected liver lesion on ultrasound and history of haematuria investigated with gadoxetateenhanced abdominal MRI to evaluate the liver and collecting systems, illustrates the use of gadoxetic acid for MRU. Gadoxetic acid is administered at a lower concentration than other gadolinium agents due to stronger T1 shortening effects and combined with 50% biliary and 50% renal excretion, this leads to physiological dilution of the gadolinium agent in the collecting systems and minimal T2* effects. Coronal MIP image obtained from 3D T1W FS GRE demonstrates excellent opacification of the bilateral collecting systems (arrowheads). Also note excretion in the biliary tree (white arrow).

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Classic (triphasic AML) and some minimal-fat AML Classic and minimal-fat AML Minimal-fat AML

Haemorrhagic cyst

Cyst

Abscess

Rarely in clear cell and papillary RCCb

Papillary RCC Clear cell RCC

T2W, T2-weighted; SI, signal intensity; RCC, renal cell carcinoma; AML, angiomyolipoma. a All subtypes of RCC demonstrate restricted diffusion, although apparent diffusion coefficient (ADC) values have been reported to be consistently lowest in papillary RCC and lower in higher Fuhrman grade tumours.53 b Very rarely, bulk fat has been reported in clear cell and papillary RCC.32 c Other renal cortical tumours, including papillary RCC, chromophobe RCC, and oncocytoma, have been reported to demonstrate SI drop on chemical-shift MRI from clear cell heterogeneity and foamy histiocytes,26 although SI drop is mild and usually <25% using chemical-shift SI index.

Some minimal-fat AML

Clear cell RCC RCC (all subtypes)a

Classic and minimal-fat AML (microscopic fat) Clear cell RCC (intracellular lipid) Other renal cortical tumoursc Classic (triphasic) AML

Abscess and pyelonephritis Some haemorrhagic cysts

Papillary RCC

Hyper-enhancement with washout kinetics Restricted diffusion SI drop on chemical-shift MRI Macroscopic (bulk) fat content Reduced T2W SI Increased T2W signal intensity (SI)

Table 2 Key imaging findings at multiparametric renal MRI and the renal lesions which may demonstrate these imaging findings.

Hypo-enhancement with progressive enhancement pattern

N.K. Ramamurthy et al. / Clinical Radiology xxx (2014) e1ee13

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reliably differentiate oncocytoma from RCC at MRI.68e70 DCE has also been shown to be useful for distinguishing tumour grade; a small series identified increased perfusion values in higher-grade tumours.71 Studies evaluating pharmacokinetic modelling using high-temporal resolution DCE in renal masses are emerging7 and are likely to become integrated into renal mass imaging protocols in the near future with further validation and as preliminary pulse sequence designs become more commercially available.

MRU When imaging of the urothelium is desired, MRU can be performed in conjunction with MP-MRI. Dilution of gadolinium is a critical component of MRU because at high concentrations the T2* effects of gadolinium overwhelm T1 shortening effects rendering the examination non-diagnostic72 (Fig 15). A saline bolus, administration of a diuretic, and a reduced dose of contrast medium can be used to dilute gadolinium concentration in the collecting systems and improve image quality (Fig 16).72 The use of a hepatobiliary contrast agent (gadoxetic acid, Bayer Pharmaceuticals) may also be considered for MRU73 because it is only 50% excreted by the kidneys, generally resulting in adequate image quality (Fig 17); however, differences in cost should be considered when compared to conventional extracellular gadolinium agents.

Conclusion In conclusion, combining function sequences with conventional renal MRI protocols constitutes a state-of-the-art MP-MRI protocol; which is becoming the reference standard for renal mass imaging in clinical practice. Slight modifications in the MRI protocol can make MP-MRI a timeefficient proposition. Critical information is provided through MP-MRI (Table 2); however, the technique is fraught with technical and interpretive pitfalls that can be only be avoided with a thorough understanding of principles of MP-MRI and an understanding of the basis for important imaging findings.

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