Diffusion-Weighted MRI in Pediatric Inflammatory Bowel Disease

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1 Pediatric Imaging Review Morani et al. DWI in Pediatric ID Pediatric Imaging Review Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved jaykumar. Morani 1 Ethan. Smith 2 Dhakshina Ganeshan 1 Jonathan R. Dillman 2 Morani, Smith E, Ganeshan D, Dillman JR Keywords: diffusion-weighted imaging (DWI), MR enterography, pediatric inflammatory bowel disease (ID) DOI: /JR Received June 15, 2014; accepted after revision November 4, Department of Radiology, The University of Texas M. D. nderson ancer enter, 1400 Pressler St, Unit 1473, Houston, TX ddress correspondence to.. Morani (ajaycmorani@yahoo.com). 2 Section of Pediatric Radiology, Department of Radiology,. S. Mott hildren s Hospital, University of Michigan Health System, nn rbor, MI. This article is available for credit. JR 2015; 204: X/15/ merican Roentgen Ray Society Diffusion-Weighted MRI in Pediatric Inflammatory owel Disease OJETIVE. Pediatric patients with inflammatory bowel disease (ID) commonly need repetitive imaging to assess disease activity and complications. Recently, MR enterography has become a first-line radiologic study in children with ID because of improved image quality, excellent soft-tissue contrast resolution, and lack of ionizing radiation. The purpose of this article is to describe the use of diffusion-weighted imaging (DWI) in MR enterography and the evaluation of pediatric ID. ONLUSION. Several contemporary publications have shown that DWI can be useful for assessing both pediatric and adult patients with ID as an important adjunct pulse sequence. Specifically, DWI can be used to identify abnormal bowel segments, assess disease inflammatory activity, and detect and characterize a variety of extraintestinal ID-related manifestations and complications. rohn disease (D) and ulcerative colitis (U) are two forms of inflammatory bowel disease (ID), characterized by relapsing and remitting active and chronic inflammation of the intestine [1]. lthough disease evaluation relies in part on clinical assessment of the patient, laboratory evaluation, and endoscopy with superficial biopsy, imaging also plays a very important role [2 7]. ross-sectional enterography (both T and MR) provides for the first time in a single test comprehensive assessment of the bowel lumen, bowel wall (including characterization of disease activity), mesentery and periintestinal soft tissues, and distant abdominopelvic soft-tissue and osseous structures. These forms of imaging further allow detailed evaluation of the entire abdominopelvic gastrointestinal tract, from the stomach through the anus. MR enterography is fast becoming the radiologic study of choice to evaluate the bowel in children and young adult patients with ID because this technique can excellently depict both intestinal and extraintestinal disease-related manifestations and complications [2, 8 10]. ecause many patients with ID require repetitive imaging to assess disease activity and complications [11], MRI is an attractive imaging modality owing to its lack of ionizing radiation [12], inherent multiplanar capability, excellent soft-tissue contrast resolution, and cine-imaging capabilities [2 5, 12]. Recently, the use of diffusion-weighted imaging (DWI) has been described in both pediatric and adult MR enterography protocols as an adjunct pulse sequence for ID evaluation [13, 14]. On the basis of the literature and our clinical experience, DWI can be used to identify abnormal bowel segments, assess disease inflammatory activity, and detect a variety of extraintestinal disease-related manifestations and complications. DWI exploits differences in the motion of water molecules in tissues to produce image contrast and provides both qualitative and quantitative information at the microscopic (cellular and subcellular) level [15 17]. Diffusion of water is modified and limited by interactions with cell membranes and macromolecules. The role of DWI in abdominopelvic MRI has increased considerably over the past decade owing to the development of improved diffusion gradient coils and faster imaging techniques. This has been most notable in the realm of oncologic imaging [15 19]. The purpose of this article is to describe the various applications of DWI in pediatric MR enterography and the assessment of ID. Diffusion-Weighted Imaging Technique Whereas standard pediatric and adult MR enterography protocols generally consist of JR:204, June

2 Morani et al. Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved multiple rapidly acquired axial and coronal pulse sequences with and without fat saturation (e.g., single-shot fast spin-echo and 2D balanced steady-state free precession) followed by contrast-enhanced imaging in the axial and coronal planes, several groups have recently described the addition of DWI to their routine MR enterography protocols [13, 20 22]. It is well accepted when performing DWI that higher b values are more sensitive to diffusion effects and provide greater suppression of background signal. Tissues and lesions with restricted (or impeded) diffusion of water (motion of water molecules is normally random or brownian) appear hyperintense on high-b-value DW images because they show less signal intensity loss than tissues with unrestricted (free) water diffusivity (Fig. 1). ecause tissues and lesions can also appear hyperintense on DWI owing to very long T2 relaxation times, apparent diffusion coefficient (D) maps can be used in conjunction with DWI to identify T2 shine-through artifact (i.e., high signal intensity on DWI that is not due to restricted diffusion) (Fig. 1). D calculation allows quantitative assessment of water diffusivity and requires that DWI be performed using a minimum of two b values (e.g., b = 0 and b = mm 2 /s). The term b value refers to the strength of the diffusion-sensitizing gradient and relates to both gradient amplitude and duration, and increasing the number of values comes at the cost of signal-to-noise ratio (SNR) and scanning time. D values are inversely proportional to water diffusivity; that is, high D values express free unrestricted diffusion of water molecules, typical for healthy biologic tissues or benign pathologic processes, whereas low D values indicate restricted diffusion of water, which can be seen in certain normal hypercellular tissues (e.g., lymph nodes and spleen) as well as malignancies, inflammation, abscesses, and fibrosis [15 19, 23, 24]. s described by Freiman et al. [25], DWI signal decay can be separated into a slow diffusivity component, which is more from extravascular water molecules, and a fast diffusivity component, which is more from intravascular water molecules by modeling intravoxel incoherent motion. Whereas overall D value and DWI signal decay reflect both the slow and fast diffusivity components together, the intravoxel incoherent motion model allows the individual contributions of slow and fast diffusion to be distinguished. Freiman et al. showed that the reduced D observed in D is primarily related to changes in the fast diffusion rather than to changes in the slow diffusion. With regard to technique, DWI of the abdomen and pelvis, including the bowel, can be performed either with the patient doing free breathing or using breath-hold or respiratory-gated techniques. Typically, a single-shot echo-planar based pulse sequence is used. The use of multiple signal averages (e.g., up to 6 8) improves DW image quality when images are acquired with the patient doing free breathing by increasing the SNR and decreasing the conspicuity of motion artifact due to respiration [20, 22]. reath-hold and respiratory-gated (using either a respiratory sensor [e.g., respiratory bellows] on the abdomen or navigator triggering based on the location of the right hemidiaphragm) techniques generally require fewer signal averages (e.g., 3 4) to obtain high-quality DW images. Frequency selective or inversion recovery based complete fat suppression with volume shimming is used to eliminate the chemical shift and ringing artifacts at fat-water interfaces. Fat suppression also increases the conspicuity of lesions with restricted diffusion, which appear bright in the background of dark signal intensity from fat suppression. Parallel imaging techniques using multichannel surface coils can be used to minimize imaging time as well as decrease susceptibility, chemical shift, and motion artifacts. Specifically, parallel imaging shortens the echo-planar imaging train, thereby decreasing the filling time of k-space [15, 19, 26]. pplications of Diffusion-Weighted Imaging in Pediatric Inflammatory owel Disease ffected owel Segment Localization and ssessment of Disease ctivity lassic MR enterography findings suggestive of active ID include bowel wall thickening, mural edema on T2-weighted images, and hyperenhancement on contrastenhanced images [20, 27]. Recent studies have shown that bowel segments affected by both D and U also show restricted diffusion of water on DWI [5, 18, 20, 22, 25, 28 30]. This finding can be used to identify segments of bowel affected by both D and U (Figs. 2 and 3) and can increase radiologists confidence in the setting of equivocal wall thickening or equivocal hyperenhancement on contrast-enhanced images. Studies by Oto et al. [20] and Kiryu et al. [22] have shown that bowel segments affected by D have significantly lower D values than normal bowel segments. For example, Oto et al. [20] showed that, in adult patients, the mean D value of bowel (terminal ileum and colon) affected by D was 1.59 ± mm 2 /s, compared with 2.74 ± mm 2 /s in normal bowel segments (p < ). In clinical practice, DWI may be more sensitive for detecting U compared with D because the continuous inflammation of U can appear more conspicuous than bowel segments affected by D (which may be short and have skip segments of normal intervening bowel) [18, 29]. Recent studies also suggest that restricted diffusion within the bowel wall is indicative of active inflammation [13, 29]. Oto et al. [29] found that DWI is more sensitive than dynamic contrast-enhanced and perfusion MRI for detecting active bowel wall inflammation. study by Ream et al. [13] showed that increasing bowel wall restricted diffusion in the setting of pediatric smallbowel D was associated with increasing bowel wall thickening, greater mesenteric inflammatory changes, striated pattern of arterial phase hyperenhancement on contrastenhanced images, and greater bowel wall relative contrast-enhanced hyperenhancement all findings suggestive of active bowel inflammation. lthough inflamed bowel segments show restricted diffusion, the exact mechanism remains unclear. Oto et al. [20, 29] proposed that narrowing of the extracellular space due to increased cell density from inflammatory cells and lymphoid aggregates, dilated lymphatic vessels, and granulomas in the bowel wall contributes to restricted diffusion in active D. recent study by Freiman et al. [25] showed that lower D values are observed in inflamed bowel segments primarily because of the fast diffusion component on the basis of the intravoxel incoherent motion model and that restricted diffusion is at least in part due to increased perfusion. ccording to Maccioni et al. [18], bowel wall restricted diffusion also can be seen in association with mural fibrosis. s dler et al. [31] and Zappa et al. [32] have shown, many bowel segments affected by D commonly contain both active inflammation and fibrosis by histopathology; consequently, it is difficult to determine in this setting whether restricted diffusion is due to inflammation or fibrosis. Whatever the reason for restricted diffusion, it is conceivable that DWI could someday replace contrast-enhanced imag JR:204, June 2015

3 DWI in Pediatric ID Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved ing for the quantification of disease activity and determination of response to therapy on the basis of changes in visual signal intensity and quantitative D analysis [21]. This may be particularly important in patients who cannot receive IV gadolinium-based contrast materials because of severe chronic kidney disease (and associated nephrogenic systemic fibrosis risk) or a history of prior allergiclike reaction to gadolinium chelates. Detection of Penetrating omplications Sinus tracts and fistulas In D, transmural active inflammation, including penetrating deep ulcerations, can lead to the formation of sinus tracts or fistulas. Such penetrating complications are common in pediatric and adult D and only very rarely occur in U. Sinus tracts are blind-ended extensions of penetrating inflammation beyond the bowel wall, whereas fistulas communicate with a second epithelialized surface. Fistulas can involve numerous epithelialized structures, such as adjacent bowel, stomach, genitourinary structures (e.g., urinary bladder or ureter), and skin [3, 4, 8]. Penetrating complications also commonly affect the perianal region in D. These tracts may also be blind ended or communicate with the skin. Highresolution, small-fov MRI has been shown to excellently detect perianal abnormalities in D, including fistulas and abscesses, as well as to assess fistula activity [4, 33]. Intraabdominal and perianal sinus tracts and fistulas can be hypointense or hyperintense on T2-weighted images and generally show hyperenhancement on contrast-enhanced images. omplex intraabdominal fistulous disease may sometimes have a stellate appearance (i.e., star sign ) because of multiple converging tethered loops of inflamed bowel [3, 4, 34]. DWI can serve as a useful adjunct pulse sequence when assessing possible intraabdominal and perianal penetrating complications (Figs. 4 and 5). Schmid-Tannwald et al. [35] have shown that the addition of DWI increases the detection rate of intraabdominal penetrating complications as well as improves reader confidence. The combination of DWI and T2-weighted imaging was found to be superior for the detection of perianal fistulas compared with T2-weighted imaging alone, and combined DWI and T2-weighted imaging was found to be similar to combined T2-weighted and contrast-enhanced imaging [36]. Thus, as mentioned previously, DWI may prove particularly useful for MR enterography examinations in patients who have contraindications to IV administration of gadolinium chelates [35, 37]. nother recent study in adult patients showed that DWI can be used to establish and follow perianal fistula inflammatory activity [36, 38]. bscesses Localized bowel wall perforation due to penetrating disease in the setting of active ID can lead to infected focal fluid collections. Such fluid collections typically arise from a sinus tract or fistula that may or may not be discernable. D-related abdominopelvic phlegmons, or unorganized inflammatory or infectious inflammatory lesions, are most often located adjacent to the terminal ileum. bscesses are organized walled-off inflammatory or infectious focal fluid collections that also most often occur adjacent to the terminal ileum, although on occasion they can involve the retroperitoneum and abdominal wall. bscesses in the perirectal and perianal regions are also common in D. bscesses, unlike areas of phlegmon, are well circumscribed on MR enterography, with a discrete peripherally enhancing wall, and they markedly restrict diffusion, appearing lightbulb bright (Figs. 6 and 7). bscesses also appear very dark on D images, suggesting that the DWI signal hyperintensity is not due to T2 shine-through. DWI can be used to confirm that a focal fluid collection is an abscess when IV gadolinium-based contrast material is contraindicated [39, 40]. Identifying these intraabdominal and perianal focal infected fluid collections is imperative because they require antibiotic therapy and sometimes percutaneous aspiration or drainage catheter placement, depending on size and location [3, 4]. It is also important to identify abscesses before initiation of medical therapy for D because certain immunosuppressive medications can cause worsening of existing infectious processes and deterioration in clinical condition [4]. Detection of Lymph Nodes Prominent and enlarged perienteric (within small-bowel mesentery), pericolic (including within the mesocolon), and perirectal lymph nodes are commonplace in active ID (both D and U) and are usually considered to be reactive in nature. However, on rare occasion, lymphadenopathy in patients with ID who have experienced chronic immune system suppression may be due to lymphoma [3]. lthough intraabdominal lymph nodes can be identified on most pulse sequences, they are often well appreciated on fat-saturated T2-weighted and contrast-enhanced pulse sequences. Intraabdominal lymph nodes generally are more difficult to visualize on nonfat-saturated pulse sequences, including single-shot fast spin-echo imaging without fat saturation. High-b-value DW images (b = s/mm 2 ) can be very helpful for detecting intraabdominal lymph nodes, because hypercellular structures (including normal lymph nodes) markedly restrict diffusion and appear strikingly hyperintense (Figs. 1, 8, and 9). lthough DWI increases the conspicuity and detectability of intraabdominal lymph nodes, it cannot reliably differentiate reactive lymphadenopathy from lymphomatous or metastatic lymphadenopathy, which may also show restricted diffusion owing to hypercellularity [15, 24, 41] (Fig. 8). The presence of an increased number of lymph nodes (either nonenlarged or enlarged) adjacent to a portion of the small bowel, colon, or rectum on DWI may be indicative of local bowel wall inflammation and should prompt close evaluation for additional findings suggestive of ID, including bowel wall restricted diffusion (Figs. 1 and 9). Detection of Inflammatory owel Disease ssociated rthritis (Sacroiliitis) Sacroiliitis is a relatively common extraintestinal manifestation of U and D that is more commonly recognized in adults. DWI has been shown to be a sensitive and costeffective technique in the detection of early sacroiliitis [42] (Fig. 10). This technique also can differentiate between normal and abnormal subchondral bone [42]. Furthermore, DWI may be a useful tool for following sacroiliac joint inflammatory activity over time in patients with ID when quantified as an D value [42, 43]. Pitfalls of Diffusion-Weighted Imaging Placing ROIs on D maps for quantitative assessment of restricted diffusion can be challenging when the bowel wall is of normal thickness (< 3 mm) or only mildly thickened. Hence, D values of normal bowel wall may be inaccurate, because ROIs can include intraluminal contents and adjacent mesentery (or other soft tissues) in addition to the bowel wall. nother limitation when using DWI to establish whether there is bowel wall inflammatory activity is that there can be significant variation in D values along the course of an abnormal bowel loop [18]. This is because JR:204, June

4 Morani et al. Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved bowel wall inflammation can be quite variable along the length and circumference of an abnormal bowel segment. Finally, calculated D values can vary on the basis of the exact b values chosen, number of b values selected, differences in gradient coils, and magnetic field inhomogeneities. onclusion DWI can be a very useful adjunct pulse sequence for MR enterography in both children and adults with ID. In addition to helping identify segments of bowel affected by both D and U and assessing disease activity, DWI can be used to identify and characterize abscesses, penetrating tracts, lymph nodes, and inflammation of the sacroiliac joints. Further research is needed to establish whether bowel wall restricted diffusion, when quantified as an D value, can be used to precisely quantify bowel wall inflammatory activity, thus potentially eliminating the need for IV contrast material in some patients. References 1. Diefenbach K, reuer K. Pediatric inflammatory bowel disease. World J Gastroenterol 2006; 12: l-hawary M, Zimmermann EM. new look at rohn s disease: novel imaging techniques. urr Opin Gastroenterol 2012; 28: Griffin N, Grant L, nderson S, Irving P, Sanderson J. Small bowel MR enterography: problem solving in rohn s disease. Insights Imaging 2012; 3: Mazziotti S, scenti G, Scribano E, et al. Guide to magnetic resonance in rohn s disease: from common findings to the more rare complicances. Inflamm owel Dis 2011; 17: Sinha R. Recent advances in intestinal imaging. Indian J Radiol Imaging 2011; 21: Dillman JR, dler J, Zimmermann EM, Strouse PJ. T enterography of pediatric rohn disease. 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5 DWI in Pediatric ID Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved activity: feasibility study. Eur J Radiol 2012; 81: oudghène F, boun H, Grange JD, Wallays, odin F, igot JM. Magnetic resonance imaging in the exploration of abdominal and anoperineal fistulas in rohn s disease [in French]. Gastroenterol lin iol 1993; 17: Hori M, Oto, Orrin S, Suzuki K, aron RL. Diffusion-weighted MRI: a new tool for the diagnosis of fistula in ano. J Magn Reson Imaging 2009; 30: Oto, Schmid-Tannwald, grawal G, et al. Diffusion-weighted MR imaging of abdominopelvic abscesses. Emerg Radiol 2011; 18: Neubauer H, Platzer I, Mueller VR, et al. Diffusion-weighted MRI of abscess formations in children and young adults. World J Pediatr 2012; 8: Punwani S, Taylor S, Saad ZZ, et al. Diffusionweighted MRI of lymphoma: prognostic utility and implications for PET/MRI? Eur J Nucl Med Mol Imaging 2013; 40: ozgeyik Z, Ozgocmen S, Kocakoc E. Role of diffusion-weighted MRI in the detection of early active sacroiliitis. JR 2008; 191: Gaspersic N, Sersa I, Jevtic V, Tomsic M, Praprotnik S. Monitoring ankylosing spondylitis therapy by dynamic contrast-enhanced and diffusion-weighted magnetic resonance imaging. Skeletal Radiol 2008; 37: Fig year-old boy with rohn disease., Hyperintense signal is evident in ileocecal region (arrows) and in adjacent reactive mesenteric lymph nodes (arrowhead) on b = 0 diffusion-weighted image., Hyperintense signal in ileocecal region (arrows) and in adjacent reactive mesenteric lymph nodes (arrowhead) is more conspicuous owing to restricted diffusion on b = 500 diffusion-weighted image, which otherwise shows decreased signal intensity in other normal bowel loops compared b = 0 diffusion-weighted image., Hypointense signal in ileocecal region (circle) and in adjacent reactive mesenteric lymph nodes (arrowhead) on apparent diffusion coefficient map corresponds to hyperintense signal on b = 500 diffusion-weighted images, consistent with restricted diffusion (arrows) due to active rohn disease. JR:204, June

6 Morani et al. Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved Fig. 2 Two patients with active inflammatory bowel disease. and, 15-year-old girl with newly diagnosed rohn disease. xial single-shot fast spin-echo image shows thickening of distal ileum (arrows, ) and sigmoid colon (arrowhead, ), and axial diffusion-weighted image shows that distal ileum (arrows, ) and sigmoid colon (arrowhead, ) are hyperintense, consistent with restricted diffusion., 10-year-old boy with ulcerative colitis. xial diffusion-weighted image shows restricted diffusion in descending colon (arrow). Fig. 3 Two patients with active rohn disease. and, 17-year-old boy with rohn disease involving appendix. xial diffusion-weighted image shows curvilinear area of restricted diffusion (arrow, ) in right lower quadrant of abdomen corresponding to appendix, and axial contrast-enhanced T1-weighted fat-saturated image reveals that focus of restricted diffusion corresponds to thick-walled, hyperenhancing appendix (arrow, ), consistent with active inflammation. (Fig. 3 continues on next page) 1274 JR:204, June 2015

7 DWI in Pediatric ID Fig. 3 (continued) Two patients with active rohn disease., 16-year-old boy with gastroduodenal rohn disease. xial diffusion-weighted image shows restricted diffusion in wall of duodenum (arrows). Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old girl with rohn disease., xial contrast-enhanced T1-weighted fat-saturated image shows hyperenhancement of active fistulous tract (arrow) between inflamed terminal ileum and ascending colon., xial diffusion-weighted image shows hyperintense active fistulous tract (arrow) between inflamed terminal ileum and ascending colon, corresponding to restricted diffusion. Fig year-old boy with perianal rohn disease. xial diffusion-weighted image shows perianal fistulous tract (arrow) that restricts diffusion. Fig. 6 Two patients with active rohn disease. and, 14-year-old girl with newly diagnosed rohn disease. xial diffusion-weighted image shows conspicuous hyperintensity of large pelvic fluid collection (arrow, ) corresponding to restricted diffusion, consistent with abscess. xial contrast-enhanced T1-weighted fat-saturated image shows large peripherally enhancing fluid collection (arrow, ) corresponding to restricted diffusion, consistent with abscess; tiny nondependent signal void (arrowhead, ) is due to gas. (Fig. 6 continues on next page) JR:204, June

8 Morani et al. Fig. 6 (continued) Two patients with active rohn disease., 11-year-old girl with labial rohn disease. xial diffusion-weighted image through perineum shows small focal fluid collection (arrow) in left labia majora that restricts diffusion, consistent with abscess. Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved Fig. 7 Two patients with active rohn disease., 15-year-old boy with newly diagnosed rohn disease and rectal pain. xial diffusion-weighted image shows large, horseshoe-shaped perirectal fluid collection (arrows) located in intersphincteric space with restricted diffusion, consistent with abscess. and, 11-year-old boy with untreated rohn disease. xial T2-weighted fat-saturated image shows small hyperintense lesion (arrow, ) in left hepatic lobe. xial diffusion-weighted image shows that hepatic lesion restricts diffusion (arrow, ); this proved to represent abscess. Fig year-old girl with rohn disease. Shortly after this examination, patient was diagnosed with diffuse large -cell lymphoma., oronal contrastenhanced T1-weighted fat-saturated image shows multiple enlarged lymph nodes (arrows) in root of small-bowel mesentery., xial diffusionweighted image shows that mesenteric lymph nodes (arrows) are hyperintense owing to restricted diffusion JR:204, June 2015

9 DWI in Pediatric ID Downloaded from by on 04/25/18 from IP address opyright RRS. For personal use only; all rights reserved Fig year-old boy with rectal rohn disease., xial T2-weighted fat-saturated image through pelvis shows multiple round intermediately hyperintense foci (arrows) adjacent to rectum, representing enlarged reactive perirectal lymph nodes., xial diffusion-weighted image through pelvis shows multiple round hyperintense foci (arrows) owing to restricted diffusion adjacent to rectum, representing enlarged reactive perirectal lymph nodes. FOR YOUR INFORMTION Fig year-old boy with rohn disease suspected to have early sacroiliitis based on imaging findings., oronal contrastenhanced T1-weighted fat-saturated image through sacroiliac joints shows sacral enhancement adjacent to both sacroiliac joints (arrows)., xial diffusionweighted image through sacroiliac joints shows mild restricted diffusion involving sacrum (arrows). This article is available for ME and Self-ssessment (S-ME) credit that satisfies Part II requirements for maintenance of certification (MO). To access the examination for this article, follow the prompts associated with the online version of the article. JR:204, June