Abdominal Imaging
ª Springer Science+Business Media New York (outside the USA) 2015
Abdom Imaging (2015) DOI: 10.1007/s00261-015-0471-3
Non-oncologic applications of diffusionweighted imaging (DWI) in the genitourinary system Dell P. Dunn,1 Nathan R. Kelsey,1 Karen S. Lee,2 Martin P. Smith,2 Koenraad J. Mortele2 1
Department of Radiology, David Grant Medical Center, 101 Bodin Cir, Travis AFB, CA 94535, USA Division of Body MRI, Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston MA 02215, USA 2
Abstract Diffusion-weighted imaging (DWI) has become an increasingly used tool in abdominal and pelvic magnetic resonance imaging (MRI), primarily in the oncologic setting. DWI sequences are being added to routine MRI protocols at many institutions, and as its use has spread, more non-oncologic applications have been explored. The purpose of this article is to provide a review of DWI applications in inflammatory, infectious, autoimmune-mediated, and ischemic processes affecting the genitourinary system. Key words: MRI—Diffusion-weighted imaging— DWI—Genitourinary—Pelvis—Restricted diffusion
Over the past decade, the use of diffusion-weighted imaging (DWI) has expanded far beyond its initial central nervous system applications [1] for detecting ischemia and characterizing ring-enhancing lesions. DWI is currently established as a useful tool in the detection and assessment of an array of neoplastic processes in the abdomen and pelvis. As more body MRI protocols include DWI sequences, additional applications in non-oncologic disorders have been described and investigated. Some of the potential benefits of using DWI in the abdomen and pelvis in a non-oncologic patient include the following: (1) increased conspicuity and therefore detection of inflammatory lesions; (2) physiologic information regarding cellular density, cytotoxic edema, and abscess formation; and (3) improved characterization of lesions when Gadoliniumbased contrast agents (GBCA) are contraindicated. However, familiarity with clinical situations where DWI
Correspondence to: Dell P. Dunn; email: [email protected]
may be helpful and pitfalls that may arise is essential in employing DWI as an effective imaging tool in the nononcologic patient.
Basic DWI physics DWI is a fluid-sensitive technique that allows distinction between freely moving hydrogen protons and those that are constrained. It has long been used in brain imaging, but over the last decade, advances such as parallel imaging, echo-planar sequences, phased array coils, and high-amplitude gradients have allowed for application in abdominal imaging. Diffusion can be restricted by cell and organelle membranes or by extracellular macromolecules [2] in pathologic processes such as cellular tumors, cytotoxic edema, abscess, and fibrosis. Most DWI sequences utilize a modified echo-planar imaging (EPI) sequence. Inversion recovery is used to attain homogenous fat saturation with either selective suppression of fat or a standard short tau inversion recovery (STIR). Diffusion weighting is achieved by applying symmetric dephasing and rephrasing gradients on either side of the 180° refocusing pulse. Immobile protons experience both the dephasing and rephasing gradients and remain in phase with one another with relatively preserved signal. A proton which diffuses to another location in the time between the dephasing and rephrasing gradients experiences asymmetric gradients. Consequently, mobile protons become out of phase with neighboring protons resulting in a loss of net signal intensity. The relative strength, duration, and time interval of the dephasing and rephrasing gradients is represented by the b value. Since the signal intensity on DWI of each voxel is affected by the density of excited protons, at least two different b values are necessary to control for underlying tissue proton density. Typical b values for abdominal imaging are b 0–50 and b 500–1000. Signal that is
D. P. Dunn et al.: Non-oncologic applications of DWI
relatively preserved on high b values compared to low b values indicates restricted diffusion. An apparent diffusion coefficient (ADC) map is a graphical representation of signal preservation between low and high b values. The ADC values are a logarithmic function of the absolute value of the slope of the line plotted from the signal obtained at different b values [3]. Areas of restricted diffusion have preserved signal with a shallow slope between low and high b values and thus low ADC values. Regions of freely mobile protons have signal loss between low and high b values resulting in a steeper line (more negative slope) and thus higher ADC values (Fig. 1C). Regions that are bright on both high b value images and ADC can
be attributable to an increased density of excited water protons, termed ‘‘T2 shine-through.’’
DWI techniques DWI sequences can be added to any MRI protocol. The scan time necessary is largely determined by whether breath-hold, free-breathing, respiratory-triggered, or navigator technique is used. DWI sequences with large b values are more sensitive to diffusion at the expense of the signal-to-noise ratio (SNR). This signal loss can be overcome with multiple signal averages and increased scan time. With a single-
B
A
D
Signal Intensity
C
b50
b650
Fig. 1. A Normal DWI in the abdomen. The contrast in the low b value DWI (b = 50 s/mm2) image resembles a fatsuppressed T2-WI. Note the black blood in the aorta. The high signal cerebrospinal fluid (CSF) is helpful to identify the low b value image. B Normal DWI in the abdomen. High b value DWI (b = 650 s/mm2) image shows an overall drop in signal due to the stronger gradients applied. Note the persistent high signal in the spleen which is typical for lymphatic tissue. The loss of signal in the CSF helps identify the high b value image. C Normal DWI in the abdomen. Simplified
graphical representation of the drop in SI between the low and high b value images for a voxel in the CSF (gray line) and spleen (black line) shown in A and B. D Normal DWI in the abdomen. The ADC map is calculated from the slope of the SI drop for each voxel between at least two b value images. The steeper slope of the CSF (gray line in C) voxel results in a higher ADC value and bright pixel on the ADC map. The flatter slope of the splenic voxel (black line in C) results in a lower ADC value and darker pixels on the ADC map.
D. P. Dunn et al.: Non-oncologic applications of DWI
Fig. 2. 44-year-old female with history of bladder cancer and neobladder presenting with right flank pain. A Post-contrast T1WI (left) shows subtle striated nephrogram (arrows). B High b value image (b600) shows wedge shaped areas of high signal
intensity nephrogram which correspond to the regions of reduced enhancement. C There is clear restriction of diffusion on ADC map in the areas of hypoenhancement and DWI signal shown on A and B, consistent with pyelonephritis.
breath-hold technique, b values are typically 20–50 and 500–600. Free-breathing technique can also be performed, but more signal averages are required due to ghosting from respiratory motion. Some quantitative techniques in oncologic imaging of the abdomen and pelvis require multiple b values. When more or higher b values are desired, respiratory triggering or navigator technique is generally employed. If more than two b values are desired in the abdomen and pelvis, it is recommended to have at least one value of 100 or greater and one value of 500 or greater for adequate ADC calculation [4]. At our institution we use 500 and 800. With low b values, perfusion (blood flow) can increase signal intensity as well as diffusion. If three or
more b values are utilized, the contributions of perfusion and diffusion can be separated according to the intravoxel incoherent motion model utilizing a bi-exponential decay function instead of the traditional mono-exponential function as described by Le Bihan et al. [5]. ADC values based solely on the diffusion component exhibit increased precision and accuracy [6]. These methods have been applied to assess hepatic fibrosis and renal transplant rejection [7, 8]. A variety of shortcomings limit the utility of DWI in the abdomen. As a gradient sequence, DWI is sensitive to susceptibility from metal or air (to include air in bowel). To limit susceptibility, TE must be kept as low as possible. Phase-encoding motion artifact (ghosting) is
D. P. Dunn et al.: Non-oncologic applications of DWI
produced by cardiac and aortic pulsation as well as bowel and diaphragm motion during DWI. Ghosting can be mitigated with single-breath-hold, breath-gating, or navigator techniques. Inhomogeneity in the phase gradients over large areas may result in distortion of the periphery. Parallel imaging is utilized to decrease the scan time and to reduce distortion. Additionally, lack of standardization in image acquisition techniques limits the utility of ADC values in clinical practice. There is wide variability in the specific b values employed at different institutions as well as the number of b value steps acquired which affects the calculated ADC. Scanner manufacturer and breath-hold techniques also can affect ADC further contributing to variability [9].
Renal applications
Pyelonephritis can present as a focal, multifocal, or diffuse process, and DWI has been shown to be able to depict areas of parenchymal infection in the kidneys before abscess formation (Fig. 2) [10, 11]. Renal and perinephric abscesses can complicate pyelonephritis and have the same appearance as abscesses do elsewhere: fluid collections with increased SI on T2-weighted images and restricted diffusion centrally surrounded by a capsule of relatively low SI and restricted diffusion that enhances after GBCA administration (Fig. 3). The technique can also be used to differentiate pyonephrosis from hydronephrosis, with pyonephrotic renal collecting systems demonstrating significantly decreased ADC values compared to hydronephrotic renal collecting systems along with marked hyperintensity on DWI sequences. [12].
Pyelonephritis, pyonephrosis, and abscesses
Renal infarcts and papillary necrosis
In evaluating patients with severe renal failure, DWI can be a helpful alternative if GBCA are contraindicated.
The initial and most common application of DWI focused on the assessment of cerebral ischemia, but the
Fig. 3. 21-year-old male with paroxysmal nocturnal hemoglobinuria (PNH) and renal vein thrombus leading to severe papillary necrosis. A Contrast-enhanced fat-suppressed T1-WI shows no enhancement of the left renal medulla and decreased enhancement of the cortex compared to the contralateral kidney. B On DWI, the b800 image shows
higher SI in the renal medulla than in the contralateral kidney (arrow). Very low SI in bilateral cortices is due to iron deposition from PNH (compare to Fig. 1B) which is more pronounced on the DWI sequences than conventional sequences (A). C ADC map shows decreased values in the renal medulla on the left relative to the right.
D. P. Dunn et al.: Non-oncologic applications of DWI
same concepts apply to ischemia in other organs including the kidneys. Case reports describe restricted diffusion of the kidney associated with renal artery dissection, and in a dog study, DWI showed both acute and chronic effects of ischemia [13, 14]. In this study, after temporary ligation of a single renal artery in dogs, Liu et al. found lower ADC values persisting in the medulla, while ADC values in the cortex returned to normal reflecting the sensitivity of the renal medulla to ischemia (Fig. 3).
ments in transplanted kidneys. Additional studies utilizing diffusion tensor imaging (DTI) in addition to DWI were able to show correlation between transplant renal function and DTI fractional anisotropy in the renal cortex and medulla [15]. However, at this point DWI has not been able predict acute rejection [8]. DWI can be helpful in depicting common transplant complications such as focal pyelonephritis in the setting of reflux nephropathy or characterizing the nature of post-transplant perinephric fluid collections (Fig. 4).
Renal transplant
Chronic kidney disease (CKD)
Limited studies evaluating DWI as a non-invasive tool to monitor transplant dysfunction are promising, especially since transplant patients with acute or severe renal failure are at risk for nephrogenic systemic fibrosis with gadolinium-based contrast administration. Thoeny et al. demonstrated high reproducibility of ADC measure-
Chronic kidney disease has been shown to affect diffusion in the kidneys with reduction in ADC (increased restriction of diffusion) as the glomerular filtration rate drops [16]. Comparison of ADC values with degree of CKD on biopsy specimens also showed a clear correlation with increased degree of pathology associated with
Fig. 4. 38-year-old woman presenting with fever and pelvic pain. A T2-WI shows a left adnexal cystic lesion (asterisk) and a dilated fluid-filled right fallopian tube (arrow). B DWI (b = 800 s/mm2) image shows high SI in both adnexal
lesions. C ADC map shows low values in the dilated fallopian tube (arrow), consistent with pyosalpinx, and high values in the left adnexal simple cyst (asterisk) from T2 shine-through.
D. P. Dunn et al.: Non-oncologic applications of DWI
decreased ADC values. However, no correlation was seen between specific types of medical renal disease and ADC values [17].
IgG4-KD and found DWI to be 100% sensitive in detecting IgG4 deposits in the kidneys with more lesions detected on DWI than conventional T2-WI and contrastenhanced sequences [19].
Acute ureteral obstruction
Pelvic applications
Pregnant patients and renal transplant recipients frequently present with dilated collecting systems on imaging, but often without identifiable cause of obstruction. Conversely, early acute obstruction may present without collection system dilation. DWI may prove useful as a problem-solving tool particularly when contrast is contraindicated, as frequently it is in these situations. Using DWI, a slight but statistically significant difference in diffusion and perfusion values was demonstrated between the acutely obstructed and contralateral, unaffected kidney [18].
Hydrosalpinx and tubo-ovarian abscess
IgG4 disease is an autoimmune-mediated process for which the most common presentation is autoimmune pancreatitis. Other manifestations include retroperitoneal fibrosis, biliary disease, and renal deposits. These renal deposits can simulate tumors or lymphoma. Kim et al. reviewed the MRI appearance of 31 patients with
Fluid-filled cystic and tubular structures are frequently encountered in the pelvis and DWI has value in their characterization, both to substitute for or supplement GBCA. A fluid-filled structure anywhere in the body with homogenous restriction of diffusion is concerning for an abscess (Fig. 5). However, an uninfected hematoma, hematosalpinx, endometrioma, dermoid, or hemorrhagic cyst can also have restricted diffusion and confound the diagnosis. With the use of other sequences, including non-contrast-enhanced T1-weighted and T2weighted images, many of these can be differentiated. Li et al. showed that the addition of DWI sequences to conventional pelvic MRI improved accuracy in diagnosis pelvic inflammatory disease from 91.2% to 97.5%. In their study, the addition of DWI demonstrated restricted diffusion in several pseudo-solid abscess cavities that were thought to be solid ovarian or fallopian stroma on conventional sequences. [20] Cystic or necrotic neo-
Fig. 5. 29-year-old pregnant woman at 22-week gestation with RLQ pain but negative ultrasound and equivocal clinical exam. A T2-WI shows a gravid uterus and mildly enlarged and edematous right ovary with stromal hypertrophy centrally and peripheralization of follicles which raises
concern for torsion. B DWI image (b = 600 s/mm2) shows restricted diffusion in the right ovary. C ADC map shows low values in areas corresponding to high SI on DWI confirming restricted diffusion in the ovary. Ovarian torsion was proven at surgery.
IgG4 kidney disease (IgG4-KD)
D. P. Dunn et al.: Non-oncologic applications of DWI
plasms typically only demonstrate restricted diffusion at the periphery where there is high cellular density, whereas abscesses demonstrate more restricted diffusion centrally than peripherally. Depending on the viscosity of the pus, abscess contents may show heterogeneous restriction of diffusion with more restriction dependently or in loculations [21].
yield has been demonstrated in diagnosing ovarian torsion by the addition of DWI sequences, but DWI has been shown to be beneficial in identifying hemorrhagic infarction in torsed ovaries where lower ADC values are seen than in ovaries without hemorrhagic infarction [23].
Ovarian torsion
While deep infiltrating endometriosis has been shown to have low ADC values [24], the utility of DWI in characterizing endometriosis is limited by overlapping ADC ranges with other benign and malignant adnexal processes. The appearance of blood products on low b value images is similar to that seen on T2-weighted images, such as T2 shading [25]. Low b value images provide contrast similar to a T2-weighted fat-suppressed sequence, which can highlight the ectopic endometrial glands sometimes seen in larger endometrial implants (Fig. 6). Small endometrial implants are often not conspicuous on DWI and may be more difficult to identify on DWI due to the reduced resolution and SNR compared to conventional MR images. In the study by Busard et al. referenced above, they were only able to obtain accurate ADC measurements in 60 of 110 infiltrating lesions due to the small size of the implants.
Sonography remains the standard first-line imaging tool in cases of suspected torsion; however, MRI is occasionally used in equivocal or difficult cases. T2-weighted sequences, including b0 low b value images, can show enlargement, mass lesions, stromal hypertrophy, and peripheralization of follicles which suggest torsion. Asymmetric restricted diffusion in the ovarian stroma can reflect ischemia (Fig. 6) and can be seen sometimes in follicles and cysts that have undergone ischemia. DWI can also increase the conspicuity of a twisted fallopian tube [22]. To our knowledge, no additional diagnostic
Endometriosis
Ectopic pregnancy Ectopic pregnancy is typically diagnosed by trans-vaginal ultrasound (TVUS); however, there are cases where the site of ectopic implantation is not identified [26]. In a study of 24 patients with clinically suspected ectopic pregnancy, but inconclusive TVUS, the ectopic gestational sac was identified with MRI in 22/24 patients. While other imaging features such as T2 characteristics, T2*, and dynamic contrast enhancement were the primary tools for detection and characterization, Takehashi et al. reported that 91% of implantations demonstrated a ring-like or stippled pattern of restricted diffusion [27].
Placental abnormalities
Fig. 6. 47-year-old female with a submucosal nodule in the upper rectum. A MRI of the pelvis demonstrated hematosalpinx (not shown) as well as several deposits of deep infiltrating endometriosis. Contrast-enhanced T1-WI shows an enhancing deposit (arrow) on the serosa of the rectum (asterisk). B DWI (b = 800 s/mm2) shows mild restriction of diffusion.
MRI has become an important second-line tool in the evaluation of placental abnormalities including placental invasion, abruption, and insufficiency [28]. As GBCA remain relatively contraindicated in pregnancy [29], several investigators have evaluated DWI for characterization of these pathologies. In a feasibility study examining DWI in placental invasion, Morita et al. described improved tissue contrast between the placenta and myometrium with DWI over conventional pulse sequences and clear depiction of a case of placenta increta, though placenta accreta was not well depicted [30]. Masselli et al., reporting on a series of 19 cases of placental abruption, found 53% sensitivity with US, 95% sensitivity with T1-WI, and 100% sensitivity with DWI in
D. P. Dunn et al.: Non-oncologic applications of DWI
Fig. 7. 28-year-old female with a history for uterine fibroids and acute peri-umbilical pain. A Sag T2-WI shows several large predominantly sub-serosal uterine fibroids with a large exophytic fibroid at the fundus (star). B Axial DWI (b = 800/
mm2) shows high signal in the fundal fibroid suggesting restricted diffusion (star). C Low ADC values confirm restriction of diffusion in the fibroid (star) indicating ischemia secondary to early acute degeneration.
making the diagnosis of abruption. There were no false positives with either MR sequence [31]. Finally, Bonel et al. found that MRI with DWI increased accuracy in diagnosing placental insufficiency from 91% to 99% as compared to ultrasound alone [32]. Despite being in the early stages of research, due to the advantageous tissue contrast of DWI and the ability to provide physiologic placental data without GBCA, DWI will likely have a role in placental imaging going forward.
which can be confirmed with DWI (Fig. 7) [33]. Reduction in ADC values following uterine artery embolization has also been shown to correlate with subsequent volume reduction of fibroids [34].
Uterine fibroids Degenerating fibroids can also be a source of pelvic pain in pregnancy as fibroids may hypertrophy to the point of outstripping their blood supply. Conventional MR sequences can depict cystic or hemorrhagic (red) degeneration, but early acute degeneration with ischemic fibroids
Prostatitis DWI has become a part of most prostate MRI protocols focused on detection, localization, and staging of prostate cancer in the setting of a positive prostate biopsy or elevated PSA. Prostatitis is the second most common cause of falsely elevated PSA, and while prostatitis has slightly higher SI on DWI sequences compared to normal peripheral zone, Nagel et al. showed a significant difference between prostate cancer and prostatitis with prostate cancer restricting diffusion to a greater degree; however, there was some overlap in ADC values between
D. P. Dunn et al.: Non-oncologic applications of DWI
the two. They did not report a significant difference in ADC values between normal prostate tissue and prostatitis [35]. Characterization of a (peri-) prostatic abscess as a complication of prostatitis can also be aided by DWI [36].
Scrotum and testes Preliminary studies have evaluated the benefit of DWI in testicular torsion, varicocele, and hydrocele. In the case of torsion, the presence of the unaffected contralateral testicle provides an ideal control to assess whether restricted diffusion is present on the affected side. Maki et al. found significantly lower ADC values in torsed testicles compared to the normal testes, though there was an overlap in the ranges [37]. Karakas et al. reported reduced ADC values in both testes in patients with a varicocele, regardless of side, compared to healthy controls. They also found lower ADC values to be inversely correlated to varix size suggesting that larger varicoceles resulted in increasing testicular fibrosis [38]. Finally, Gulum et al. demonstrated that unilateral hydroceles correlated with reduced ADC values in the testis on the affected side and that the size of the hydrocele also inversely correlated with ADC suggesting a negative effect on fertility from larger hydroceles [39].
Conclusion Although the primary application of DWI in MRI of the abdomen and pelvis is, and will likely continue to be, focused on oncologic imaging, there are many non-oncologic applications where the technique can be very helpful in detection, characterization, and problem solving in a variety of organ systems and processes in the abdomen and pelvis. References 1. Le Bihan D, Breton E, Lallemand D, et al. (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401–407 2. Taouli B, Koh DM (2010) Diffusion-weighted MR imaging of the liver. Radiology 251:47–66 3. Qayyum A (2009) Diffusion-weighted imaging in the abdomen and pelvis: concepts and applications. Radiographics 29:1797–1810 4. Padhani AR, Liu G, Koh DM, et al. (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125 5. Le Bihan D, Breton E, Lallemand D, et al. (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505 6. Zhang JL, Sigmund EE, Chandarana H, et al. (2010) Variability of renal apparent diffusion coefficients: limitations of the monoexponential model for diffusion quantification. Radiology 254:783– 792 7. Luciani A, Vignaud A, Cavet M, et al. (2008) Liver cirrhosis: intravoxel incoherent motion MR imaging—Pilot Study. Radiology 249:891–899 8. Thoeny HC, De Keyzer F (2011) Diffusion-weighted MR imaging of native and transplanted kidneys. Radiology 259:25–38 9. Guiu B, Cercuell JP (2011) Liver diffusion-weighted MR imaging: the tower of Babel? Eur Radiol 21:463–467
10. Thoeny HC, De Keyzer F, Oyen RH, Peeters RR (2005) Diffusionweighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience 1. Radiology 235:911– 917 11. Verswijvel G, Vandecaveye V, Gelin G, et al. (2002) Diffusionweighted MR imaging in the evaluation of renal infection: preliminary results. JBR-BTR 85:100–103 12. Chan JH, Tsui EY, Luk S, et al. (2001) MR diffusion-weighted imaging of kidney: differentiation between hydronephrosis and pyonephrosis. Clin Imaging 25:110–113 13. Yamanouchi Y, Yamamoto K, Noda K, Tomori K, Kinoshita T (2008) Renal infarction in a patient with spontaneous dissection of segmental arteries: diffusion-weighted magnetic resonance imaging. Am J Kidney Dis 52:788–791 14. Liu AS, Xie JX (2003) Functional evaluation of normothermic ischemia and reperfusion injury in dog kidney by combining MR diffusion-weighted imaging and Gd-DTPA enhanced first-pass perfusion. J Magn Reson Imaging 17:683–693 15. Lanzman RS, Ljimani A, Pentang G, et al. (2013) Kidney transplant: functional assessment with diffusion-tensor MR imaging at 3T. Radiology 266:218–225 16. Macarini L, Stoppino LP, Milillo P, et al. (2010) Diffusionweighted MRI with parallel imaging technique: apparent diffusion coefficient determination in normal kidneys and in nonmalignant renal diseases. Clin Imaging 34:432–440 17. Li Q, Li J, Zhang L, et al. (2014) Diffusion-weighted imaging in assessing renal pathology of chronic kidney disease: a preliminary clinical study. Eur J Radiology 83:756–762 18. Thoeny HC, Binser T, Roth B, Kessler TM, Vermathen P (2009) Noninvasive assessment of acute ureteral obstruction with diffusion-weighted MR imaging: a prospective study. Radiology 252:721–728 19. Kim B, Kim JH, Byun JH, et al. (2014) IgG4-related kidney disease: MRI findings with emphasis on the usefulness of diffusionweighted imaging. Eur J Radiol 83:1057–1062 20. Li WH, Zhang YZ, Cui YF, Zhang P, Wu XR (2013) Pelvic inflammatory disease: evaluation of diagnostic accuracy with conventional MR with added diffusion-weighted imaging. Abdom Imaging 38:193–200 21. Unal O, Koparan HI, Avcu S, Kalender AM, Kisli E (2011) The diagnostic value of diffusion-weighted magnetic resonance imaging in soft tissue abscesses. Eur J Radiol 77:490–494 22. Fujii S, Kaneda S, Kakite S, et al. (2011) Diffusion-weighted imaging findings of adnexal torsion: initial results. Eur J Radiol 77:330–334 23. Kato H, Kanematsu M, Uchiyama M, et al. (2014) Diffusionweighted imaging of ovarian torsion: usefulness of apparent diffusion coefficient (ADC) values for the detection of hemorrhagic infarction. Magn Reson Med Sci 13:39–44 24. Busard MPH, Mijatovic V, van Kuijk C, et al. (2010) Erratum: magnetic resonance imaging in the evaluation of (deep infiltrating) endometriosis: the value of diffusion-weighted imaging. J Magn Reson Imaging 32:1003–1009 25. Siegelman ES, Oliver ER (2012) MR imaging of endometriosis: ten imaging pearls. Radiographics 32:1675–1691 26. Tamai K, Koyama T, Togashi K (2007) MR features of ectopic pregnancy. Eur Radiol 17:3236–3246 27. Takahashi A, Takahama J, Marugami N, et al. (2013) Ectopic pregnancy: MRI findings and clinical utility. Abdom Imaging 38:844–850 28. Masselli G, Gualdi G (2013) MR imaging of the placenta: what a radiologist should know. Abdom Imaging 38:573–587 29. Expert Panel on MR Safety, Kanal E, Barkovich AJ, Bell C, et al. (2013) ACR guidance document on MR safe practices: 2013. J Magn Reson Imaging 37:501–530 30. Morita S, Ueno E, Fujimura M, et al. (2009) Feasibility of diffusion-weighted MRI for defining placental invasion. J Magn Reson Imaging 30:666–671 31. Masselli G, Brunelli R, Di Tola M, Anceschi M, Gualdi G (2011) MR imaging in the evaluation of placental abruption: correlation with sonographic findings. Radiology 259:222–230 32. Bonel HM, Stolz B, Diedrichsen L, et al. (2010) Diffusion-weighted MR imaging of the placenta in fetuses with placental insufficiency. Radiology 257:810–819
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33. Bailey AA, Pedrosa I, Twickler DM, Rofsky NM (2012) MRI of abdominal and pelvic pain in pregnancy. Appl Radiol 42: 15–24 34. Ananthakrishnan G, Macnaught G, Hinksman L, et al. (2012) Diffusion-weighted imaging in uterine artery embolisation: do findings correlate with contrast enhancement and volume reduction? Br J Radiol 85:e1046–e1050 35. Nagel KNA, Schouten MG, Hambrock T, et al. (2013) Differentiation of prostatitis and prostate cancer by using diffusionweighted MR imaging and MR-guided biopsy at 3T. Radiology 267:164–172
36. Lal A, Yadav M, Khandelwal N, Singh P, Singh S (2011) Case series: diffusion weighted MRI appearance in prostatic abscess. Indian J Radiol Imaging 21:46–48 37. Maki D, Watanabe Y, Nagayama M, et al. (2011) Diffusionweighted magnetic resonance imaging in the detection of testicular torsion: feasibility study. J Magn Reson Imaging 34:1137–1142 38. Karakas E, Karakas O, Cullu N, et al. (2014) Diffusion-weighted MRI of the testes in patients with varicocele: a preliminary study. AJR 202:324–328 39. Gulum M, Cece H, Yeni E, et al. (2012) Diffusion-weighted MRI of the testis in hydrocele: a pilot study. Urol Int 89:191–195
ª Springer Science+Business Media New York (outside the USA) 2015
Abdom Imaging (2015) DOI: 10.1007/s00261-015-0471-3
Non-oncologic applications of diffusionweighted imaging (DWI) in the genitourinary system Dell P. Dunn,1 Nathan R. Kelsey,1 Karen S. Lee,2 Martin P. Smith,2 Koenraad J. Mortele2 1
Department of Radiology, David Grant Medical Center, 101 Bodin Cir, Travis AFB, CA 94535, USA Division of Body MRI, Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston MA 02215, USA 2
Abstract Diffusion-weighted imaging (DWI) has become an increasingly used tool in abdominal and pelvic magnetic resonance imaging (MRI), primarily in the oncologic setting. DWI sequences are being added to routine MRI protocols at many institutions, and as its use has spread, more non-oncologic applications have been explored. The purpose of this article is to provide a review of DWI applications in inflammatory, infectious, autoimmune-mediated, and ischemic processes affecting the genitourinary system. Key words: MRI—Diffusion-weighted imaging— DWI—Genitourinary—Pelvis—Restricted diffusion
Over the past decade, the use of diffusion-weighted imaging (DWI) has expanded far beyond its initial central nervous system applications [1] for detecting ischemia and characterizing ring-enhancing lesions. DWI is currently established as a useful tool in the detection and assessment of an array of neoplastic processes in the abdomen and pelvis. As more body MRI protocols include DWI sequences, additional applications in non-oncologic disorders have been described and investigated. Some of the potential benefits of using DWI in the abdomen and pelvis in a non-oncologic patient include the following: (1) increased conspicuity and therefore detection of inflammatory lesions; (2) physiologic information regarding cellular density, cytotoxic edema, and abscess formation; and (3) improved characterization of lesions when Gadoliniumbased contrast agents (GBCA) are contraindicated. However, familiarity with clinical situations where DWI
Correspondence to: Dell P. Dunn; email: [email protected]
may be helpful and pitfalls that may arise is essential in employing DWI as an effective imaging tool in the nononcologic patient.
Basic DWI physics DWI is a fluid-sensitive technique that allows distinction between freely moving hydrogen protons and those that are constrained. It has long been used in brain imaging, but over the last decade, advances such as parallel imaging, echo-planar sequences, phased array coils, and high-amplitude gradients have allowed for application in abdominal imaging. Diffusion can be restricted by cell and organelle membranes or by extracellular macromolecules [2] in pathologic processes such as cellular tumors, cytotoxic edema, abscess, and fibrosis. Most DWI sequences utilize a modified echo-planar imaging (EPI) sequence. Inversion recovery is used to attain homogenous fat saturation with either selective suppression of fat or a standard short tau inversion recovery (STIR). Diffusion weighting is achieved by applying symmetric dephasing and rephrasing gradients on either side of the 180° refocusing pulse. Immobile protons experience both the dephasing and rephasing gradients and remain in phase with one another with relatively preserved signal. A proton which diffuses to another location in the time between the dephasing and rephrasing gradients experiences asymmetric gradients. Consequently, mobile protons become out of phase with neighboring protons resulting in a loss of net signal intensity. The relative strength, duration, and time interval of the dephasing and rephrasing gradients is represented by the b value. Since the signal intensity on DWI of each voxel is affected by the density of excited protons, at least two different b values are necessary to control for underlying tissue proton density. Typical b values for abdominal imaging are b 0–50 and b 500–1000. Signal that is
D. P. Dunn et al.: Non-oncologic applications of DWI
relatively preserved on high b values compared to low b values indicates restricted diffusion. An apparent diffusion coefficient (ADC) map is a graphical representation of signal preservation between low and high b values. The ADC values are a logarithmic function of the absolute value of the slope of the line plotted from the signal obtained at different b values [3]. Areas of restricted diffusion have preserved signal with a shallow slope between low and high b values and thus low ADC values. Regions of freely mobile protons have signal loss between low and high b values resulting in a steeper line (more negative slope) and thus higher ADC values (Fig. 1C). Regions that are bright on both high b value images and ADC can
be attributable to an increased density of excited water protons, termed ‘‘T2 shine-through.’’
DWI techniques DWI sequences can be added to any MRI protocol. The scan time necessary is largely determined by whether breath-hold, free-breathing, respiratory-triggered, or navigator technique is used. DWI sequences with large b values are more sensitive to diffusion at the expense of the signal-to-noise ratio (SNR). This signal loss can be overcome with multiple signal averages and increased scan time. With a single-
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Signal Intensity
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b50
b650
Fig. 1. A Normal DWI in the abdomen. The contrast in the low b value DWI (b = 50 s/mm2) image resembles a fatsuppressed T2-WI. Note the black blood in the aorta. The high signal cerebrospinal fluid (CSF) is helpful to identify the low b value image. B Normal DWI in the abdomen. High b value DWI (b = 650 s/mm2) image shows an overall drop in signal due to the stronger gradients applied. Note the persistent high signal in the spleen which is typical for lymphatic tissue. The loss of signal in the CSF helps identify the high b value image. C Normal DWI in the abdomen. Simplified
graphical representation of the drop in SI between the low and high b value images for a voxel in the CSF (gray line) and spleen (black line) shown in A and B. D Normal DWI in the abdomen. The ADC map is calculated from the slope of the SI drop for each voxel between at least two b value images. The steeper slope of the CSF (gray line in C) voxel results in a higher ADC value and bright pixel on the ADC map. The flatter slope of the splenic voxel (black line in C) results in a lower ADC value and darker pixels on the ADC map.
D. P. Dunn et al.: Non-oncologic applications of DWI
Fig. 2. 44-year-old female with history of bladder cancer and neobladder presenting with right flank pain. A Post-contrast T1WI (left) shows subtle striated nephrogram (arrows). B High b value image (b600) shows wedge shaped areas of high signal
intensity nephrogram which correspond to the regions of reduced enhancement. C There is clear restriction of diffusion on ADC map in the areas of hypoenhancement and DWI signal shown on A and B, consistent with pyelonephritis.
breath-hold technique, b values are typically 20–50 and 500–600. Free-breathing technique can also be performed, but more signal averages are required due to ghosting from respiratory motion. Some quantitative techniques in oncologic imaging of the abdomen and pelvis require multiple b values. When more or higher b values are desired, respiratory triggering or navigator technique is generally employed. If more than two b values are desired in the abdomen and pelvis, it is recommended to have at least one value of 100 or greater and one value of 500 or greater for adequate ADC calculation [4]. At our institution we use 500 and 800. With low b values, perfusion (blood flow) can increase signal intensity as well as diffusion. If three or
more b values are utilized, the contributions of perfusion and diffusion can be separated according to the intravoxel incoherent motion model utilizing a bi-exponential decay function instead of the traditional mono-exponential function as described by Le Bihan et al. [5]. ADC values based solely on the diffusion component exhibit increased precision and accuracy [6]. These methods have been applied to assess hepatic fibrosis and renal transplant rejection [7, 8]. A variety of shortcomings limit the utility of DWI in the abdomen. As a gradient sequence, DWI is sensitive to susceptibility from metal or air (to include air in bowel). To limit susceptibility, TE must be kept as low as possible. Phase-encoding motion artifact (ghosting) is
D. P. Dunn et al.: Non-oncologic applications of DWI
produced by cardiac and aortic pulsation as well as bowel and diaphragm motion during DWI. Ghosting can be mitigated with single-breath-hold, breath-gating, or navigator techniques. Inhomogeneity in the phase gradients over large areas may result in distortion of the periphery. Parallel imaging is utilized to decrease the scan time and to reduce distortion. Additionally, lack of standardization in image acquisition techniques limits the utility of ADC values in clinical practice. There is wide variability in the specific b values employed at different institutions as well as the number of b value steps acquired which affects the calculated ADC. Scanner manufacturer and breath-hold techniques also can affect ADC further contributing to variability [9].
Renal applications
Pyelonephritis can present as a focal, multifocal, or diffuse process, and DWI has been shown to be able to depict areas of parenchymal infection in the kidneys before abscess formation (Fig. 2) [10, 11]. Renal and perinephric abscesses can complicate pyelonephritis and have the same appearance as abscesses do elsewhere: fluid collections with increased SI on T2-weighted images and restricted diffusion centrally surrounded by a capsule of relatively low SI and restricted diffusion that enhances after GBCA administration (Fig. 3). The technique can also be used to differentiate pyonephrosis from hydronephrosis, with pyonephrotic renal collecting systems demonstrating significantly decreased ADC values compared to hydronephrotic renal collecting systems along with marked hyperintensity on DWI sequences. [12].
Pyelonephritis, pyonephrosis, and abscesses
Renal infarcts and papillary necrosis
In evaluating patients with severe renal failure, DWI can be a helpful alternative if GBCA are contraindicated.
The initial and most common application of DWI focused on the assessment of cerebral ischemia, but the
Fig. 3. 21-year-old male with paroxysmal nocturnal hemoglobinuria (PNH) and renal vein thrombus leading to severe papillary necrosis. A Contrast-enhanced fat-suppressed T1-WI shows no enhancement of the left renal medulla and decreased enhancement of the cortex compared to the contralateral kidney. B On DWI, the b800 image shows
higher SI in the renal medulla than in the contralateral kidney (arrow). Very low SI in bilateral cortices is due to iron deposition from PNH (compare to Fig. 1B) which is more pronounced on the DWI sequences than conventional sequences (A). C ADC map shows decreased values in the renal medulla on the left relative to the right.
D. P. Dunn et al.: Non-oncologic applications of DWI
same concepts apply to ischemia in other organs including the kidneys. Case reports describe restricted diffusion of the kidney associated with renal artery dissection, and in a dog study, DWI showed both acute and chronic effects of ischemia [13, 14]. In this study, after temporary ligation of a single renal artery in dogs, Liu et al. found lower ADC values persisting in the medulla, while ADC values in the cortex returned to normal reflecting the sensitivity of the renal medulla to ischemia (Fig. 3).
ments in transplanted kidneys. Additional studies utilizing diffusion tensor imaging (DTI) in addition to DWI were able to show correlation between transplant renal function and DTI fractional anisotropy in the renal cortex and medulla [15]. However, at this point DWI has not been able predict acute rejection [8]. DWI can be helpful in depicting common transplant complications such as focal pyelonephritis in the setting of reflux nephropathy or characterizing the nature of post-transplant perinephric fluid collections (Fig. 4).
Renal transplant
Chronic kidney disease (CKD)
Limited studies evaluating DWI as a non-invasive tool to monitor transplant dysfunction are promising, especially since transplant patients with acute or severe renal failure are at risk for nephrogenic systemic fibrosis with gadolinium-based contrast administration. Thoeny et al. demonstrated high reproducibility of ADC measure-
Chronic kidney disease has been shown to affect diffusion in the kidneys with reduction in ADC (increased restriction of diffusion) as the glomerular filtration rate drops [16]. Comparison of ADC values with degree of CKD on biopsy specimens also showed a clear correlation with increased degree of pathology associated with
Fig. 4. 38-year-old woman presenting with fever and pelvic pain. A T2-WI shows a left adnexal cystic lesion (asterisk) and a dilated fluid-filled right fallopian tube (arrow). B DWI (b = 800 s/mm2) image shows high SI in both adnexal
lesions. C ADC map shows low values in the dilated fallopian tube (arrow), consistent with pyosalpinx, and high values in the left adnexal simple cyst (asterisk) from T2 shine-through.
D. P. Dunn et al.: Non-oncologic applications of DWI
decreased ADC values. However, no correlation was seen between specific types of medical renal disease and ADC values [17].
IgG4-KD and found DWI to be 100% sensitive in detecting IgG4 deposits in the kidneys with more lesions detected on DWI than conventional T2-WI and contrastenhanced sequences [19].
Acute ureteral obstruction
Pelvic applications
Pregnant patients and renal transplant recipients frequently present with dilated collecting systems on imaging, but often without identifiable cause of obstruction. Conversely, early acute obstruction may present without collection system dilation. DWI may prove useful as a problem-solving tool particularly when contrast is contraindicated, as frequently it is in these situations. Using DWI, a slight but statistically significant difference in diffusion and perfusion values was demonstrated between the acutely obstructed and contralateral, unaffected kidney [18].
Hydrosalpinx and tubo-ovarian abscess
IgG4 disease is an autoimmune-mediated process for which the most common presentation is autoimmune pancreatitis. Other manifestations include retroperitoneal fibrosis, biliary disease, and renal deposits. These renal deposits can simulate tumors or lymphoma. Kim et al. reviewed the MRI appearance of 31 patients with
Fluid-filled cystic and tubular structures are frequently encountered in the pelvis and DWI has value in their characterization, both to substitute for or supplement GBCA. A fluid-filled structure anywhere in the body with homogenous restriction of diffusion is concerning for an abscess (Fig. 5). However, an uninfected hematoma, hematosalpinx, endometrioma, dermoid, or hemorrhagic cyst can also have restricted diffusion and confound the diagnosis. With the use of other sequences, including non-contrast-enhanced T1-weighted and T2weighted images, many of these can be differentiated. Li et al. showed that the addition of DWI sequences to conventional pelvic MRI improved accuracy in diagnosis pelvic inflammatory disease from 91.2% to 97.5%. In their study, the addition of DWI demonstrated restricted diffusion in several pseudo-solid abscess cavities that were thought to be solid ovarian or fallopian stroma on conventional sequences. [20] Cystic or necrotic neo-
Fig. 5. 29-year-old pregnant woman at 22-week gestation with RLQ pain but negative ultrasound and equivocal clinical exam. A T2-WI shows a gravid uterus and mildly enlarged and edematous right ovary with stromal hypertrophy centrally and peripheralization of follicles which raises
concern for torsion. B DWI image (b = 600 s/mm2) shows restricted diffusion in the right ovary. C ADC map shows low values in areas corresponding to high SI on DWI confirming restricted diffusion in the ovary. Ovarian torsion was proven at surgery.
IgG4 kidney disease (IgG4-KD)
D. P. Dunn et al.: Non-oncologic applications of DWI
plasms typically only demonstrate restricted diffusion at the periphery where there is high cellular density, whereas abscesses demonstrate more restricted diffusion centrally than peripherally. Depending on the viscosity of the pus, abscess contents may show heterogeneous restriction of diffusion with more restriction dependently or in loculations [21].
yield has been demonstrated in diagnosing ovarian torsion by the addition of DWI sequences, but DWI has been shown to be beneficial in identifying hemorrhagic infarction in torsed ovaries where lower ADC values are seen than in ovaries without hemorrhagic infarction [23].
Ovarian torsion
While deep infiltrating endometriosis has been shown to have low ADC values [24], the utility of DWI in characterizing endometriosis is limited by overlapping ADC ranges with other benign and malignant adnexal processes. The appearance of blood products on low b value images is similar to that seen on T2-weighted images, such as T2 shading [25]. Low b value images provide contrast similar to a T2-weighted fat-suppressed sequence, which can highlight the ectopic endometrial glands sometimes seen in larger endometrial implants (Fig. 6). Small endometrial implants are often not conspicuous on DWI and may be more difficult to identify on DWI due to the reduced resolution and SNR compared to conventional MR images. In the study by Busard et al. referenced above, they were only able to obtain accurate ADC measurements in 60 of 110 infiltrating lesions due to the small size of the implants.
Sonography remains the standard first-line imaging tool in cases of suspected torsion; however, MRI is occasionally used in equivocal or difficult cases. T2-weighted sequences, including b0 low b value images, can show enlargement, mass lesions, stromal hypertrophy, and peripheralization of follicles which suggest torsion. Asymmetric restricted diffusion in the ovarian stroma can reflect ischemia (Fig. 6) and can be seen sometimes in follicles and cysts that have undergone ischemia. DWI can also increase the conspicuity of a twisted fallopian tube [22]. To our knowledge, no additional diagnostic
Endometriosis
Ectopic pregnancy Ectopic pregnancy is typically diagnosed by trans-vaginal ultrasound (TVUS); however, there are cases where the site of ectopic implantation is not identified [26]. In a study of 24 patients with clinically suspected ectopic pregnancy, but inconclusive TVUS, the ectopic gestational sac was identified with MRI in 22/24 patients. While other imaging features such as T2 characteristics, T2*, and dynamic contrast enhancement were the primary tools for detection and characterization, Takehashi et al. reported that 91% of implantations demonstrated a ring-like or stippled pattern of restricted diffusion [27].
Placental abnormalities
Fig. 6. 47-year-old female with a submucosal nodule in the upper rectum. A MRI of the pelvis demonstrated hematosalpinx (not shown) as well as several deposits of deep infiltrating endometriosis. Contrast-enhanced T1-WI shows an enhancing deposit (arrow) on the serosa of the rectum (asterisk). B DWI (b = 800 s/mm2) shows mild restriction of diffusion.
MRI has become an important second-line tool in the evaluation of placental abnormalities including placental invasion, abruption, and insufficiency [28]. As GBCA remain relatively contraindicated in pregnancy [29], several investigators have evaluated DWI for characterization of these pathologies. In a feasibility study examining DWI in placental invasion, Morita et al. described improved tissue contrast between the placenta and myometrium with DWI over conventional pulse sequences and clear depiction of a case of placenta increta, though placenta accreta was not well depicted [30]. Masselli et al., reporting on a series of 19 cases of placental abruption, found 53% sensitivity with US, 95% sensitivity with T1-WI, and 100% sensitivity with DWI in
D. P. Dunn et al.: Non-oncologic applications of DWI
Fig. 7. 28-year-old female with a history for uterine fibroids and acute peri-umbilical pain. A Sag T2-WI shows several large predominantly sub-serosal uterine fibroids with a large exophytic fibroid at the fundus (star). B Axial DWI (b = 800/
mm2) shows high signal in the fundal fibroid suggesting restricted diffusion (star). C Low ADC values confirm restriction of diffusion in the fibroid (star) indicating ischemia secondary to early acute degeneration.
making the diagnosis of abruption. There were no false positives with either MR sequence [31]. Finally, Bonel et al. found that MRI with DWI increased accuracy in diagnosing placental insufficiency from 91% to 99% as compared to ultrasound alone [32]. Despite being in the early stages of research, due to the advantageous tissue contrast of DWI and the ability to provide physiologic placental data without GBCA, DWI will likely have a role in placental imaging going forward.
which can be confirmed with DWI (Fig. 7) [33]. Reduction in ADC values following uterine artery embolization has also been shown to correlate with subsequent volume reduction of fibroids [34].
Uterine fibroids Degenerating fibroids can also be a source of pelvic pain in pregnancy as fibroids may hypertrophy to the point of outstripping their blood supply. Conventional MR sequences can depict cystic or hemorrhagic (red) degeneration, but early acute degeneration with ischemic fibroids
Prostatitis DWI has become a part of most prostate MRI protocols focused on detection, localization, and staging of prostate cancer in the setting of a positive prostate biopsy or elevated PSA. Prostatitis is the second most common cause of falsely elevated PSA, and while prostatitis has slightly higher SI on DWI sequences compared to normal peripheral zone, Nagel et al. showed a significant difference between prostate cancer and prostatitis with prostate cancer restricting diffusion to a greater degree; however, there was some overlap in ADC values between
D. P. Dunn et al.: Non-oncologic applications of DWI
the two. They did not report a significant difference in ADC values between normal prostate tissue and prostatitis [35]. Characterization of a (peri-) prostatic abscess as a complication of prostatitis can also be aided by DWI [36].
Scrotum and testes Preliminary studies have evaluated the benefit of DWI in testicular torsion, varicocele, and hydrocele. In the case of torsion, the presence of the unaffected contralateral testicle provides an ideal control to assess whether restricted diffusion is present on the affected side. Maki et al. found significantly lower ADC values in torsed testicles compared to the normal testes, though there was an overlap in the ranges [37]. Karakas et al. reported reduced ADC values in both testes in patients with a varicocele, regardless of side, compared to healthy controls. They also found lower ADC values to be inversely correlated to varix size suggesting that larger varicoceles resulted in increasing testicular fibrosis [38]. Finally, Gulum et al. demonstrated that unilateral hydroceles correlated with reduced ADC values in the testis on the affected side and that the size of the hydrocele also inversely correlated with ADC suggesting a negative effect on fertility from larger hydroceles [39].
Conclusion Although the primary application of DWI in MRI of the abdomen and pelvis is, and will likely continue to be, focused on oncologic imaging, there are many non-oncologic applications where the technique can be very helpful in detection, characterization, and problem solving in a variety of organ systems and processes in the abdomen and pelvis. References 1. Le Bihan D, Breton E, Lallemand D, et al. (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401–407 2. Taouli B, Koh DM (2010) Diffusion-weighted MR imaging of the liver. Radiology 251:47–66 3. Qayyum A (2009) Diffusion-weighted imaging in the abdomen and pelvis: concepts and applications. Radiographics 29:1797–1810 4. Padhani AR, Liu G, Koh DM, et al. (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125 5. Le Bihan D, Breton E, Lallemand D, et al. (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505 6. Zhang JL, Sigmund EE, Chandarana H, et al. (2010) Variability of renal apparent diffusion coefficients: limitations of the monoexponential model for diffusion quantification. Radiology 254:783– 792 7. Luciani A, Vignaud A, Cavet M, et al. (2008) Liver cirrhosis: intravoxel incoherent motion MR imaging—Pilot Study. Radiology 249:891–899 8. Thoeny HC, De Keyzer F (2011) Diffusion-weighted MR imaging of native and transplanted kidneys. Radiology 259:25–38 9. Guiu B, Cercuell JP (2011) Liver diffusion-weighted MR imaging: the tower of Babel? Eur Radiol 21:463–467
10. Thoeny HC, De Keyzer F, Oyen RH, Peeters RR (2005) Diffusionweighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience 1. Radiology 235:911– 917 11. Verswijvel G, Vandecaveye V, Gelin G, et al. (2002) Diffusionweighted MR imaging in the evaluation of renal infection: preliminary results. JBR-BTR 85:100–103 12. Chan JH, Tsui EY, Luk S, et al. (2001) MR diffusion-weighted imaging of kidney: differentiation between hydronephrosis and pyonephrosis. Clin Imaging 25:110–113 13. Yamanouchi Y, Yamamoto K, Noda K, Tomori K, Kinoshita T (2008) Renal infarction in a patient with spontaneous dissection of segmental arteries: diffusion-weighted magnetic resonance imaging. Am J Kidney Dis 52:788–791 14. Liu AS, Xie JX (2003) Functional evaluation of normothermic ischemia and reperfusion injury in dog kidney by combining MR diffusion-weighted imaging and Gd-DTPA enhanced first-pass perfusion. J Magn Reson Imaging 17:683–693 15. Lanzman RS, Ljimani A, Pentang G, et al. (2013) Kidney transplant: functional assessment with diffusion-tensor MR imaging at 3T. Radiology 266:218–225 16. Macarini L, Stoppino LP, Milillo P, et al. (2010) Diffusionweighted MRI with parallel imaging technique: apparent diffusion coefficient determination in normal kidneys and in nonmalignant renal diseases. Clin Imaging 34:432–440 17. Li Q, Li J, Zhang L, et al. (2014) Diffusion-weighted imaging in assessing renal pathology of chronic kidney disease: a preliminary clinical study. Eur J Radiology 83:756–762 18. Thoeny HC, Binser T, Roth B, Kessler TM, Vermathen P (2009) Noninvasive assessment of acute ureteral obstruction with diffusion-weighted MR imaging: a prospective study. Radiology 252:721–728 19. Kim B, Kim JH, Byun JH, et al. (2014) IgG4-related kidney disease: MRI findings with emphasis on the usefulness of diffusionweighted imaging. Eur J Radiol 83:1057–1062 20. Li WH, Zhang YZ, Cui YF, Zhang P, Wu XR (2013) Pelvic inflammatory disease: evaluation of diagnostic accuracy with conventional MR with added diffusion-weighted imaging. Abdom Imaging 38:193–200 21. Unal O, Koparan HI, Avcu S, Kalender AM, Kisli E (2011) The diagnostic value of diffusion-weighted magnetic resonance imaging in soft tissue abscesses. Eur J Radiol 77:490–494 22. Fujii S, Kaneda S, Kakite S, et al. (2011) Diffusion-weighted imaging findings of adnexal torsion: initial results. Eur J Radiol 77:330–334 23. Kato H, Kanematsu M, Uchiyama M, et al. (2014) Diffusionweighted imaging of ovarian torsion: usefulness of apparent diffusion coefficient (ADC) values for the detection of hemorrhagic infarction. Magn Reson Med Sci 13:39–44 24. Busard MPH, Mijatovic V, van Kuijk C, et al. (2010) Erratum: magnetic resonance imaging in the evaluation of (deep infiltrating) endometriosis: the value of diffusion-weighted imaging. J Magn Reson Imaging 32:1003–1009 25. Siegelman ES, Oliver ER (2012) MR imaging of endometriosis: ten imaging pearls. Radiographics 32:1675–1691 26. Tamai K, Koyama T, Togashi K (2007) MR features of ectopic pregnancy. Eur Radiol 17:3236–3246 27. Takahashi A, Takahama J, Marugami N, et al. (2013) Ectopic pregnancy: MRI findings and clinical utility. Abdom Imaging 38:844–850 28. Masselli G, Gualdi G (2013) MR imaging of the placenta: what a radiologist should know. Abdom Imaging 38:573–587 29. Expert Panel on MR Safety, Kanal E, Barkovich AJ, Bell C, et al. (2013) ACR guidance document on MR safe practices: 2013. J Magn Reson Imaging 37:501–530 30. Morita S, Ueno E, Fujimura M, et al. (2009) Feasibility of diffusion-weighted MRI for defining placental invasion. J Magn Reson Imaging 30:666–671 31. Masselli G, Brunelli R, Di Tola M, Anceschi M, Gualdi G (2011) MR imaging in the evaluation of placental abruption: correlation with sonographic findings. Radiology 259:222–230 32. Bonel HM, Stolz B, Diedrichsen L, et al. (2010) Diffusion-weighted MR imaging of the placenta in fetuses with placental insufficiency. Radiology 257:810–819
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33. Bailey AA, Pedrosa I, Twickler DM, Rofsky NM (2012) MRI of abdominal and pelvic pain in pregnancy. Appl Radiol 42: 15–24 34. Ananthakrishnan G, Macnaught G, Hinksman L, et al. (2012) Diffusion-weighted imaging in uterine artery embolisation: do findings correlate with contrast enhancement and volume reduction? Br J Radiol 85:e1046–e1050 35. Nagel KNA, Schouten MG, Hambrock T, et al. (2013) Differentiation of prostatitis and prostate cancer by using diffusionweighted MR imaging and MR-guided biopsy at 3T. Radiology 267:164–172
36. Lal A, Yadav M, Khandelwal N, Singh P, Singh S (2011) Case series: diffusion weighted MRI appearance in prostatic abscess. Indian J Radiol Imaging 21:46–48 37. Maki D, Watanabe Y, Nagayama M, et al. (2011) Diffusionweighted magnetic resonance imaging in the detection of testicular torsion: feasibility study. J Magn Reson Imaging 34:1137–1142 38. Karakas E, Karakas O, Cullu N, et al. (2014) Diffusion-weighted MRI of the testes in patients with varicocele: a preliminary study. AJR 202:324–328 39. Gulum M, Cece H, Yeni E, et al. (2012) Diffusion-weighted MRI of the testis in hydrocele: a pilot study. Urol Int 89:191–195
