MRI of Fetal and Maternal Diseases in Pregnancy 1st ed.

23. MRI of Appendicitis and Bowel Diseases in Pregnancy

Elena Resnick1 and Karen Lee 

(1)

Department of Radiology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA

Karen Lee

Email: kslee@bidmc.harvard.edu

Keywords

AppendicitisMRIPregnancyBowel

23.1 Introduction

Previously, the utilization of MRI in the pregnant population to diagnose maternal bowel conditions has been somewhat limited due to motion artifact from maternal bowel peristalsis and the fetus and from the inability to safely administer intravenous gadolinium-based contrast agents. Continuing technical advances in MRI with the development of ultrafast imaging techniques, as well as the excellent soft tissue contrast and multiplanar capabilities of MRI, however, have allowed MRI to emerge as a primary imaging modality with significant contribution to the workup of a pregnant patient with suspected bowel pathology.

23.2 MRI Protocol

In the use of MRI for bowel evaluation, the clinical indication may be quite broad, such as generalized abdominal pain, or relatively specific, as in the case of characterization of known bowel pathology. A general protocol for maternal abdominal imaging in pregnancy optimized for speed, feasibility, and safety is typically utilized in our institution, with adjustments and additions made for specific clinical situations.

One such recommended protocol is detailed below (Table 23.1), with numerous variations published [16]. This set of sequences is optimized for the evaluation of suspected appendicitis in pregnancy, one of the most common indications for MRI in this patient population.

Table 23.1

MRI protocol for suspected appendicitis in pregnancy

 

T2-weighted imaging

T1-weighted imaging

Parameter

Half-Fourier single-shot FSE

Half-Fourier single-shot FSE with fat suppression

Diffusion-weighted imaging

b800

2D dual-echo GRE

2D time of flight

Planes

Axial, coronal, sagittal

Axial

Axial

Axial

Axial

Coverage

Above gallbladder thru pelvis

Above gallbladder thru pelvis

Above gallbladder thru pelvis

Above gallbladder thru pelvis

Renal veins to pubic symphysis

FOV (mm)

360–440

300–360

360

300–360

300–360

TR (ms)

800–1100

800–1100

10,000

180–210

30

TE (ms)

60–80

50–70

55–80

2.2, 4.4

4.5–10

Slice thickness/intersection gap (mm)

4/1

4/1

5/0

5/1

3/1

NEX

1

1

1

1

1

Matrix

256 × 192

256 × 192

64 × 64

256 × 160

256 × 128

Breathing

Held

Held

Held

Held

Free

FSE fast spin echo, GRE gradient echo, FOV field of view

This protocol is both minimalist and thorough with each sequence serving a particular purpose. Multiplanar T2-weighted imaging (T2WI) with single-shot techniques is relatively motion insensitive and serves to best localize anatomic structures. Particularly in the pregnant population, these sequences are invaluable given fetal motion and potential limited breath-holding ability of the mother which can contribute to motion degradation of the study. T2WI with fat suppression and diffusion-weighted imaging (DWI) highlight bowel pathology with inflammation, edema, fluid, and focal lesions often appearing bright on these sequences. 2D dual-echo gradient echo T1-weighted imaging (T1WI) is used to characterize soft tissue lesions by assessing for the presence of hemorrhage, fat, and proteinaceous content which typically appears as hyperintense on this sequence, as well as for the presence of magnetic susceptibility from air, calcification, or hemosiderin depicted as blooming on the longer echo time sequence (in-phase sequence on 1.5 T magnet). Finally, 2D time of flight (TOF) is helpful in differentiating between the bowel and in particular the appendix from other vascular mimickers such as pelvic varices.

In optimal circumstances, image acquisition can be completed in approximately 15 min. Longer exam time may result with the use of respiratory-triggering or navigator techniques when the patient is unable to adequately hold their breath. Respiratory-triggered single-shot sequences have the added benefit of enabling sequential imaging of the bowel. Additional enterographic sequences can be considered when dynamic bowel evaluation is thought to be of benefit, as for a patient with known inflammatory bowel disease. These sequences include multiphase, multislice, cine imaging, acquired as heavily T2-weighted thick slabs, as well as coronal steady-state free precession (SSFP). The former allows for dynamic assessment of bowel peristalsis and distensibility, while the latter provides excellent anatomic detail due to motion insensitivity.

In order to expedite the imaging acquisition process, MRI obtained in pregnant patients with suspected appendicitis should be acquired without the use of oral contrast. Despite the controversial benefits of oral contrast agents, particularly an iron-containing negative contrast agent such as historically available ferumoxsil, recent literature has confirmed maintained high sensitivity and specificity of MRI in diagnosing appendicitis without its use [179].

Intravenous gadolinium-based contrast agents are contraindicated in pregnancy and should only be used in dire situations in pregnancy, when the additional information it can provide outweighs the theoretical risks to the fetus [10]. Typically, bowel assessment can be sufficiently conclusive without the use of a gadolinium-based intravenous contrast, given the excellent diagnostic information which can be garnered from the remainder of the MRI examination [11].

23.3 Acute Appendicitis

Acute appendicitis remains the most common nongynecologic cause of abdominal pain during pregnancy requiring surgery [12]. The diagnosis of appendicitis in pregnancy can be complex due to the inaccuracy of conventional clinical parameters for this diagnosis [13]. Furthermore, a perforated appendix in pregnancy can result in extremely high consequences [1415]. Therefore, a reliable and accurate imaging method for the diagnosis of appendicitis is needed. Currently, in pregnant patients suspected of having appendicitis, the American College of Radiology recommends the use of MRI following an inconclusive ultrasound assessment of the appendix [16]. The appendix can be detected by MRI in 92 % of the cases [17], with excellent sensitivity and specificity for the diagnosis of appendicitis about 90 % and greater than 95 %, respectively [1822], comparable to those of CT. Due to the extremely high negative predictive value of MRI for excluding appendicitis [11723], and the ability of MRI to identify alternative causes of right lower quadrant pain in pregnancy [24], the addition of MRI to the workup of pregnant females with right lower quadrant pain has been shown to decrease the frequency of negative laparoscopies [117]. The time-to-surgery delay from the addition of MRI has not been shown to increase the rate of appendiceal perforation, a critical complication [117].

23.3.1 Normal Appendix

A normal appendix is a blind-ending tubular structure originating from the cecal tip. Accepted normal dimensions are a single wall diameter of 2 mm or less and a total cross-sectional diameter of 6 mm or less. A normal appendix is typically intermediate in signal intensity on T1- and T2-weighted images, similar to that of muscle (Fig. 23.1) [21]. While a normal appendix may be collapsed or partially filled with fluid and/or gas, the presence of gas throughout the appendiceal lumen indicates patency, thereby virtually excluding the diagnosis of appendicitis regardless of appendiceal diameter. T1-weighted in-phase and opposed-phase gradient echo imaging is useful in identifying luminal gas, denoted by susceptibility artifact on longer echo time in-phase images (on 1.5 T magnet) (Fig. 23.2) [7].

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Fig. 23.1

Coronal T2-weighted single-shot FSE image of a 31-year-old female at 12-week gestation demonstrating a normal appendix (arrow)

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Fig. 23.2

Axial T1-weighted in-phase (a) and opposed-phase (b) GRE images in a 28-year-old 20-week pregnant patient demonstrate susceptibility blooming artifact (arrow) associated with appendiceal intraluminal gas on the longer echo time in-phase image, confirming a normal appendix

Often the limiting factor in reaching conclusive MRI results is definitive identification of the appendix. Progressive displacement of the appendix by the gravid uterus and compression of adjacent structures can make this step quite difficult, depending on patient habitus and gestational age. With progressive gestational age, there is a general trend for upward migration of the appendix [25]. Regardless of gestational age, the cecal tilt angle can be used as a reliable way to localize the appendiceal base. Seen best on sagittal or coronal single-shot FSE images, identifying the cecum angled greater than 90° relative to the longitudinal axis of the patient places the appendiceal base within the right upper quadrant [25]. Tactics for identifying the cecum include retrograde tracing of the colon, as well as localization of the ileocecal junction, with the appendix typically originating along the same side of the bowel wall, approximately 2.5 cm distally.

23.3.2 Acute Appendicitis Imaging Features

Acute appendicitis occurs when luminal drainage is obstructed. Inflamed appendiceal mucosa secretes fluid which accumulates within the lumen, displacing the normally present gas and progressively distending the appendix. Edema and inflammation within the appendiceal wall result in wall thickening which also contributes to an increased total appendiceal diameter.

On MRI, an acutely inflamed appendix is often filled with hyperintense fluid on T2-weighted imaging, with an appendiceal diameter of 7 mm or greater considered abnormal (Fig. 23.3). The edematous wall of the appendix and sometimes the cecal tip appear brighter on T2-weighted images than the bowel wall elsewhere (Fig. 23.4) [26]. On diffusion-weighted images, there may be restricted diffusion of an inflamed appendix [2], increasing the sensitivity for the detection of acute appendicitis (Fig. 23.5) [27]. An appendicolith may be present, appearing as a hypointense focus on all imaging sequences, but not reliably seen by MRI (Fig. 23.6).

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Fig. 23.3

Coronal (a) and sagittal (b) single-shot FSE images in a 28-year-old female at 16-week gestation demonstrate a fluid-filled, dilated appendix (arrow) with thickened walls and adjacent fat stranding compatible with acute appendicitis

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Fig. 23.4

Axial single-shot T2-weighted images without (a) and with (b) fat suppression in a 34-year-old female at 23-week gestation demonstrate a dilated appendix with thickened and edematous wall (arrow) with adjacent edema and fat stranding confirming acute appendicitis

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Fig. 23.5

(a) Axial T2-weighted FSE images without and (b) with fat suppression of a 41-year-old female pregnant with twins at 29-week gestational age demonstrate a thick-walled appendix (arrow) with mural edema, fluid within the lumen, and adjacent periappendiceal fat stranding compatible with acute appendicitis. (c) Axial DWI (b = 800 s/mm2) shows markedly high signal within the appendix compatible with restricted diffusion (arrow)

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Fig. 23.6

(a) Sagittal single-shot FSE T2-WI demonstrating upward cecal displacement in a 21-year-old woman at 24-week gestational age with cecal tilt of approximately 140°. This angulation assisted in identifying the inflamed appendix within the right upper quadrant in this patient, with hypointense appendicoliths in the appendiceal base (arrow) on the (b) coronal single-shot FSE T2WI

Periappendiceal inflammation is indicated by stranding within the adjacent fat, appearing hyperintense on T2-weighted images which is particularly accentuated with fat suppression (Figs. 23.323.4, and 23.5). While inflammation surrounding the appendix is usually a reliable sign of acute appendicitis, a small amount of free fluid is often seen within the right paracolic gutter during normal pregnancy, and this finding should be interpreted cautiously and in the context of other findings.

When the imaging appearance and clinical picture for appendicitis are equivocal, the risk of appendiceal perforation is likely low, and consideration may be given to close monitoring and potentially repeat imaging. If the appendix remains inflamed and not responsive to antibiotic therapy, subsequent imaging may show more definitive, evolved findings of appendicitis.

23.3.3 Perforated Appendicitis

Perforation is most frequently seen in the third trimester and is associated with marked negative effect on fetal outcome, including premature delivery. Unfortunately, the accuracy of all imaging modalities, including MRI, in identifying microperforation remains poor, with up to half of all cases of perforated appendicitis being misdiagnosed as simple appendicitis both by MRI and ultrasound [28]. Diagnosis of perforation can be suggested when the appendiceal wall appears discontinuous with a large amount of surrounding periappendiceal inflammation and fluid (Fig. 23.7). Confident diagnosis of perforation can be made when extraluminal gas or a periappendiceal fluid collection is identified. Diffusion-weighted imaging shows promise in prospective diagnosis of perforation when these definitive findings are absent. The degree of diffusion restriction has been shown to parallel increasing inflammation, with perforated appendices demonstrating significantly lower ADC values (0.79 mm2/s) than simple appendicitis (1.11 mm2/s) and normal appendices (1.85 mm2/s) (Fig. 23.8) [2].

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Fig. 23.7

(a) Axial, single-shot FSE T2-weighted image in this 36-year-old, 29-week pregnant woman demonstrates extensive fluid and edema surrounding an inflamed appendix, findings which are more readily apparent with (b) fat suppression which also highlights an irregular, discontinuous appendiceal wall (arrow). Although no discrete extraluminal fluid collection was identified, findings were highly suggestive of perforated appendicitis. Intraoperative and histopathologic evaluation confirmed acute gangrenous appendicitis with perforation

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Fig. 23.8

Axial single-shot FSE T2-weighted images (a) without and (b) with fat suppression in a 32-year-old woman at 30 weeks of gestation demonstrate a dilated appendix with a fluid-filled lumen, mural thickening, edema, and periappendiceal stranding (arrow). Corresponding axial (c) DWI (b = 800 s/mm2) and (d) ADC map demonstrate hyperintense signal throughout the appendix on DWI and hypointensity on ADC with the cecal tip as having the greatest restriction of diffusion (ADC = 7.2 mm2/s) (arrow). Acute appendicitis with microperforation was confirmed surgically

23.3.4 Mimics of Appendicitis

Pitfalls in diagnosing appendicitis include misidentification and misinterpretation of the appendix. Many tubular structures within the right lower quadrant can be similar in caliber to the appendix. Identification of the cecal origin and blind-ending appendiceal tip allows for differentiation of the appendix from collapsed small bowel loops. Small vessels may be mistaken for a normal appendix, while engorged vessels of pregnancy, if confused for the appendix, may result in a false-positive diagnosis of appendicitis. The 2D time-of-flight (TOF) sequence is essential for differentiating the appendix from right lower quadrant vessels, such as the gonadal vein and pelvic varices. TOF images will depict blood flowing within vessels as high signal and the appendix with stationary contents as low signal (Fig. 23.9).

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Fig. 23.9

(a) Axial single-shot FSE T2-weighted image in a 27-year-old patient at 26-weeks gestation shows a cluster of round and tubular structures in the posterior right lower quadrant, each a candidate for the appendix (arrow). (b) 2D TOF GRE image at the same level demonstrates hyperintense signal within these structures indicative of flow confirming that these structures are all vessels (arrow)

Chronic inflammation of the appendix may also present as mural thickening of the appendix and mimic acute appendicitis (Fig. 23.10). The lack of appendiceal luminal distention with fluid, mural edema, and adjacent periappendiceal inflammation along with the identification of intramural fat on chemical shift T1-weighted or fat-suppressed sequences within the appendix can help distinguish between acute and chronic inflammation of the appendix.

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Fig. 23.10

(a) Axial and (b) sagittal single-shot FSE T2-weighted images demonstrate a thickened, hyperintense appendiceal wall. Note that the lumen is collapsed. While this may be mistaken for mural edema, chemical shift imaging confirms that the bright signal on T2WI is intraluminal fat, denoted by loss of signal in the appendiceal wall on (c) out-of-phase GRE T1WI compared to the (d) in-phase sequence (arrow). Presence of intramural fat can be seen due to the sequela of prior or chronic inflammation

23.3.4.1 Appendiceal Endometriosis

Endometriosis, a condition where ectopic endometrial tissue implants outside of the uterus, is a common disease and has potential for widespread involvement, including sites distant from the uterus. The appendix is involved in 2.8–4.1 % of cases of endometriosis and in 0.4 % of the general population [2930]. While usually asymptomatic, endometriosis may result in vague abdominal discomfort, and catamenial appendicitis has been speculated as cause of appendiceal pathology, thought to account for twice the frequency of appendectomies with no histologic findings of acute obstructive appendicitis in reproductive-aged women, as compared to age-matched males [3132]. True acute appendicitis secondary to endometriosis involvement can also result and should be considered as a cause for right lower quadrant pain in young women, particularly with known endometriosis [33]. Rarely, 0.03–0.08 % of pregnancies have been reported to be complicated by appendiceal endometriosis [34]. Endometrial implant growth responsive to hormonal influences of pregnancy may be responsible for the greater risk of perforation in these patients during the first two trimesters, with a hypothesized correlation between the degree of mural involvement of endometriosis and risk of perforation [3537].

Soft tissue implants along the serosal surface of the appendix, typically hypointense to myometrium on T2- weighted images and isointense on T1-weighted images, may be seen in the setting of endometriosis. Cystic foci of hyperintensity on T2WI or hemorrhagic foci depicted by hyperintensity on T1WI are seen in a minority of cases (Fig. 23.11) [38]. Endometriosis implants can be characterized as superficial in one-third of cases and deep invasive in two-thirds of cases [39]. With invasion into the muscularis layer, secondary muscle hypertrophy, fibrosis, and retraction can be seen.

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Fig. 23.11

Axial 3D fat-saturated spoiled GRE T1-weighted images of a woman presenting with right lower quadrant pain demonstrates high signal within the appendix compatible with endometriosis involvement of the appendix (arrow), which was confirmed surgically

Chronic, potentially cyclically active endometriosis of the appendix may also produce alternative appendiceal changes such as mucocele, periappendiceal inflammatory mass, intussusception, or ischemia [37].

Certainly, awareness of the potential for bowel involvement of endometriosis elsewhere besides the appendix is necessary. Bowel endometriosis is the most common site of extragenital involvement. The most common segment of the bowel involved is the rectum (52–65.7 %), followed by the sigmoid (17.4–19.4 %), the ileum (4.1–16.9 %), the appendix (5–6.4%), and the cecum (4.7–6.2 %) (Fig. 23.12) [38].

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Fig. 23.12

(a) Coronal 3D fat-saturated spoiled GRE T1-weighted, (b) coronal, and (c) axial single-shot FSE T2-weighted images demonstrate an endometrial implant with associated endometrioma along the serosal surface of the descending colon (arrow). The implant demonstrates classic features of hyperintensity on T1WI, with shading on T2WI within the cystic component, denoting chronic blood products

23.3.4.2 Mucocele

Dilation of the appendix by intraluminal accumulation of mucin is an infrequent event, accounting for only approximately 0.3 % of appendiceal pathology [40]. Presentation is most often acute or chronic right lower quadrant pain. Etiologies can be classified into four histological groups ranging from benign to malignant entities: simple mucocele (20 %) which is a post-obstructive mucous retention cyst, mucosal hyperplasia (20 %), mucinous cystadenoma (50 %), and mucinous cystadenocarcinoma (10 %) [41].

Given depth of mural involvement, mucinous cystadenocarcinoma is the most frequent cause of mucocele to be complicated by pseudomyxoma peritonei; however, all histologic subtypes may result in pseudomyxoma peritonei, particularly with perforation [4142]. This complexity has resulted in much controversy and variability in the classification of mucoceles histologically [43]. Numerous classification schemes have been proposed attempting to accurately predict prognosis [41]. Consequently, preoperative diagnosis of appendiceal mucocele is crucial. When suspected preoperatively, resection with laparotomy is preferred over laparoscopy to minimize the risk of iatrogenic perforation and rupture [40].

On MRI, an appendiceal mucocele is a well-defined cystic structure, arising from the cecal tip, typically within the right iliac fossa, but can be variable in location during pregnancy. Extent of appendiceal distention usually correlates with underlying cause, with simple mucoceles and mucosal hyperplasia typically not exceeding 2 cm in diameter. Mucinous cystadenomas and cystadenocarcinomas can reach up to 6 cm in diameter [41]. The contents of a mucocele on MRI are usually homogeneously high in signal intensity on T2-weighted images (Fig. 23.13). High protein content results in variable signal intensity on T1-weighted images, but typically intermediate [44]. Unlike acute appendicitis, mucoceles typically lack periappendiceal stranding and mural thickening unless complicated by superimposed inflammation or rupture [45]. Presence of nodularity should raise suspicion for a mucinous cystadenocarcinoma, and internal vascularity can be further assessed with ultrasound as enhancement is typically not assessed in the setting of pregnancy. Correlation with features from other imaging modalities such as curvilinear mural calcifications on CT and concentric “onion skin” appearance on ultrasound may increase the specificity for the diagnosis of a mucocele. When perforated, the MR imaging features of ruptured mucocele are virtually indistinguishable from perforated acute appendicitis [46].

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Fig. 23.13

(a) Axial single-shot T2WI with fat suppression and (b) coronal single-shot FSE T2WI in a 36-year-old, 14-week pregnant patient demonstrating a markedly distended appendix with hyperintense material (arrow). The degree of appendiceal distension without associated wall thickening or periappendiceal inflammation is highly suggestive of a mucocele. Pathology confirmed mucinous cystadenoma without carcinoma

Mucocele of the appendix has been shown to have an association with additional malignancies. The incidence of colorectal cancer in this population is approximately six times greater than the general population, approximately 17 % [41]. Breast, ovarian, and renal tumors have also been observed at a higher frequency in patients with appendiceal mucoceles [4748]. Awareness of these associations is critical for appropriate subsequent screening.

23.4 Inflammatory Bowel Disease

Inflammatory bowel disease (IBD) as the cause of abdominal pain in the pregnant population should be considered in both those women already carrying the diagnosis and women not previously diagnosed, as the childbearing years coincide with the peak age of onset of both Crohn disease and ulcerative colitis [49]. There are known effects of pregnancy on the activity of IBD. Historically, it has been believed that overall IBD activity during pregnancy approximates that of nonpregnant patients. The activity of disease at conception is used as a predictor of activity during pregnancy: when quiescent at conception, about a third of patients are expected to experience relapse, while two-thirds of patients with active disease at conception are expected to continue to have active disease during pregnancy [5051]. More recently, it has been elucidated that, indeed, no statistically significant difference in the course of Crohn disease is expected in pregnancy as compared to nonpregnant women, confirming no effect of pregnancy on Crohn disease. Patients with ulcerative colitis, however, have a greater than twice risk of relapse during pregnancy as compared to their nonpregnant counterparts, particularly during the first and second trimesters, as well as during the first 6 months postpartum. The pathophysiology of this progression may relate to smoking cessation or placental cytokine secretion, although it is not entirely clear [52]. Particular attention has been paid to the effects of vaginal delivery on perianal disease. While the trend and recommendation is to avoid vaginal delivery with active perianal disease, there has been no evidence of vaginal deliveries inciting development or exacerbation of perianal Crohn disease or protective effect of Cesarean section in progression of disease. In the absence of active perianal disease, Crohn disease patients can follow general population guidelines for mode of delivery, but episiotomy should be avoided [5355].

Effects of IBD on pregnancy have also been extensively studied. The degree of IBD activity at conception and throughout gestation correlates with pregnancy outcome, with only active IBD increasing the risk for poor fetal outcomes, including preterm birth, low birth weight, and fetal loss [5556].

23.4.1 Crohn Disease

Given the potential significant morbidity to both mother and fetus in active Crohn disease, prompt and accurate diagnosis is necessary to initiate management and plan surgical intervention when necessary. While endoscopic evaluation of the colon and distal ileum can be performed, cross-sectional imaging often is necessary for small bowel assessment and identification of penetrating complications [57].

MR enterography (MRE) has long been established as a safe and accurate method of assessing Crohn disease [58]. Conventional MRE evaluation for bowel inflammation relies on intravenous contrast use for assessment of enhancement as a marker of vascularity and perfusion [59]. The combination of extent and pattern of bowel enhancement, together with other MRI features such as wall thickness, edema, and mucosal ulcerations, has been shown to correlate with endoscopic findings and the widely used Crohn Disease Endoscopic Index of Severity [60]. Subsequently, a simpler scoring system using only mural thickness and signal of the bowel wall on T2-weighted sequences has been shown to correlate with both the MRI Activity Index and a histopathological score of terminal ileitis [61]. In the general population, MRE has been shown to have a sensitivity of 91 % and specificity of 71 % for the identification of active inflammatory bowel disease [62].

In the setting of pregnancy, there are several limitations which may result in a less than optimal MR imaging evaluation of the maternal bowel. Motion degradation is a frequent difficulty encountered with imaging the pregnant patient. This is due to a combination of multiple moving parts (fetus, amniotic fluid, maternal bowel, and maternal breathing) coupled with relatively long acquisition times for the individual sequences. Additionally, intramuscular glucagon, an antiperistaltic agent typically used with MRE in nonpregnant patients to help decrease bowel motion, is considered a pregnancy class C drug by the FDA and usually should be avoided as it could potentially have adverse effects upon the fetus. The avoidance of intravenous gadolinium-based contrast use in pregnancy also further hampers the assessment of Crohn disease on MRI.

These limitations can partly be overcome by the use of fast, motion-insensitive sequences and respiratory-triggering techniques. Furthermore, the administration of inert oral contrast agents such as dilute barium (VoLumen; E-Z-EM, Bracco Diagnostics, Monroe Township, NJ) which have no known detrimental effects on the fetus can potentially be helpful in the distention and imaging assessment of the small bowel. Approximately 900 ml of such an oral agent is recommended followed by 500 mL of water to the best of the patient’s ability and tolerance.

Despite these limitations, MRE has been shown to play a key role in the management of pregnant patients with Crohn disease. Findings depicted on MRE not only can stratify patients into those necessitating emergent surgical management and those in whom interventional procedures for Crohn disease can be delayed until postpartum, but also aid in delivery decisions [57].

23.4.1.1 Crohn Disease Imaging Features

Crohn disease can involve any segment of the bowel in a continuous or skip fashion, but most frequently involves the terminal ileum.

Uncomplicated active Crohn disease can be identified as a segment of circumferentially thickened, edematous bowel wall (Fig. 23.14). Wall edema results in hyperintense signal on T2-weighted images, particularly well visualized on fat-suppressed sequences. Mural stratification on T2-weighted images where a central layer of hyperintense signal is flanked by intermediate signal intensity within the bowel wall is often a feature seen in active inflammation [63]. Free fluid and edema in surrounding soft tissues are indicative of a transmural inflammatory process. Luminal narrowing is seen both with active disease (Fig. 23.14) and the sequela of chronic inflammation with secondary stricturing and fibrosis (Fig. 23.15). The latter may be identified by the lack of associated mural edema and adjacent fat stranding, as well as dilation or obstruction of upstream bowel. Dynamic multiphase, multislice, cine T2-weighted imaging is useful in assessing bowel peristalsis and distensibility, with diseased, inflamed, or fibrotic segments typically being relatively adynamic as compared to uninvolved loops of bowel.

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Fig 23.14

(a) Coronal and (b) sagittal single-shot FSE T2-weighted images in a 33-year-old woman at 30-week gestational age and (c) coronal single-shot FSE T2-weighted image in a 37-year-old woman at 25-week gestational age demonstrate active segmental small bowel inflammation within the right upper quadrant with circumferential wall thickening and mural edema (white arrows). Upstream bowel dilation and gaseous distention are also noted (black arrow)

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Fig. 23.15

A 27-year-old female with history of Crohn disease, at 16-week gestation presenting with acute onset of violent nausea and vomiting. (a) Coronal single-shot FSE T2WI demonstrates a distended loop of small bowel with fecalized content indicative of stasis (asterisks). (b) Sagittal SSFP illustrates tethering and stricture at the distal terminal ileum (arrow) due to chronic inflammation, resulting in partial small bowel obstruction

Mucosal ulcerations can also be detected on MRI as regions of mural irregularity on T2-weighted images [64]. While best depicted on contrast-enhanced imaging, vasa recta engorgement within areas of mesenteric fatty proliferation, a finding known as the comb sign, can also be seen on noncontrast SSFP sequences [6364].

Diffusion-weighted imaging may be particularly useful in pregnancy as it can be used to identify sites of active inflammation in Crohn disease without the need for intravenous contrast administration (Fig. 23.16). DWI has been shown to correlate with multiple traditional MRE findings of active inflammation such as wall thickening and mesenteric edema. DWI has also been shown to correlate with arterial hyperenhancement as well as the striated pattern of arterial enhancement indicative of acute rather than chronic inflammatory bowel disease [65]. Furthermore, replacing contrast-enhanced MRI sequences with DWI has been shown to be equally accurate in the assessment of Crohn disease activity in the pediatric population [66].

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Fig. 23.16

A 26-year-old patient at 7-week gestation with preexisting Crohn disease presented with right lower quadrant pain. (a) Coronal single-shot FSE T2-weighted image, (b) axial single-shot FSE T2-weighted image with fat suppression, and (c) axial ADC map demonstrate changes of terminal ileitis with marked mural thickening, mural edema, extensive surrounding inflammatory change, and fluid with restricted diffusion (arrows), in keeping with transmural inflammation from active Crohn disease. Gravid uterus (U) is also noted

Extramural complications of Crohn disease can often be well depicted on MRE. Blind-ending sinus tracts and communicating fistulous tracts appear as fluid-filled linear areas of signal abnormality on T2-weighted or SSFP sequences and highlighted with fat suppression techniques. A stellate configuration of complex internal tracts may also be noted with associated bowel tethering and retraction [67]. Heterogeneous, ill-defined, soft tissue mass-like areas with increased signal on T2-weighted imaging within the mesenteric or perienteric fat are typical of phlegmons (Fig. 23.17). Abscesses appear as walled-off extraluminal fluid collections, sometimes containing air (Fig. 23.18) [4564].

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Fig. 23.17

Coronal single-shot FSE T2-weighted images in a 37-year-old woman pregnant with twins at 11-week gestational age demonstrating terminal ileitis (arrow) with adjacent phlegmon (arrowhead)

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Fig. 23.18

(a) Axial SSFP image and (b) single-shot FSE T2WI with fat suppression in a 37-year-old, 11-week pregnant patient with Crohn disease demonstrate a gas-containing extraluminal fluid collection in the right lower quadrant (arrows), consistent with an abscess

23.4.2 Ulcerative Colitis

Ulcerative colitis is an idiopathic, mucosally based inflammatory bowel disease which characteristically involves the rectum and can spread proximally to involve variable amounts of colon in a contiguous fashion. Proctitis is practically universal in active ulcerative colitis, while pancolitis is seen in 35–45 % of patients, and involvement of the terminal ileum (“backwash ileitis”) in only 5 % [68].

Colonic assessment for ulcerative or Crohn colitis with MRI has been shown to be feasible with excellent sensitivity, specificity, and accuracy. In the ideal situation colonic cleansing and distension would take place prior to MRI evaluation [69]. The need for oral or rectal preparation may be obviated by the addition of DWI, with preserved accuracy, especially for ulcerative colitis [70]. Diffusion-weighted imaging has also been shown to have the same accuracy as post-contrast sequences in identifying colitis. As a result, MR imaging assessment of the colon in the pregnant patient can be performed in the absence of exogenous oral, rectal, or intravenous contrast administration without sacrificing diagnostic ability [70].

The imaging appearance of ulcerative colitis varies based on severity and chronicity of inflammation. Along the spectrum of mild to severe disease, imaging features may be as minimal as subtle wall thickening and reduced distensibility or as extensive as more dramatic wall thickening (although less prominent than in Crohn disease regardless of severity), mural edema, and loss of the normal haustral folds. Ulcers, the defining feature of the disease (sine qua non), may be readily apparent as gentle mucosal undulations or deep mucosal defects. Intervening edematous but intact mucosa can have a polypoid appearance, a finding known as pseudopolyps. With severe disease pericolonic findings of edema, engorged vasa recta and pericolonic lymph nodes may be noted, but the serosal surface typically remains smooth and well defined. This is in contrast to Crohn disease, which due to its transmural nature, results in serosal irregularity. Sequela of long-standing colitis may be denoted as a featureless colon lacking haustra, with smooth, tubular narrowing and rigidity. Fibrofatty proliferation surrounding involved colon can be seen, most often widening the perirectal space [68].

23.5 Ischemic Bowel

Ischemic bowel is most often seen in the setting of generalized atherosclerosis as a predisposing condition, narrowing the typical population of consideration to the elderly. It has become recognized that young adults also can develop a form of ischemic bowel, typically transient, benign, self-limited, and without recurrence. These patients present in a similar fashion with left-sided abdominal pain, nausea, vomiting, and bloody diarrhea. While often healthy, some young adults presenting with ischemic bowel have underlying vasculitis, diabetes, or coagulopathy. Medications can predispose patients to transient ischemic bowel, and in the young female subset, oral contraceptives have been found to increase the relative risk by sixfold. Although the physiology is not proven, given the reported cases of ischemic bowel associated with the use of Premarin as well, estrogen is thought to be the culprit, resulting in a hypercoagulable state. Given this hypothesized method of action, it is reasonable to consider pregnancy as another state in which ischemic bowel may occur outside of the typical elderly population [7172].

MRI was first suggested as a feasible imaging modality for diagnosing ischemic bowel as assessed at 7 T in rats [73]. Subsequently, however, clinical MRI has been compared to both CT, endoscopic, and pathologic findings, confirming its accuracy [74]. Despite lack of specificity, MRI with intravenous contrast can identify ischemic bowel in the correct clinical setting with adequate pretest consideration. MRI can discriminate patients who require urgent surgical intervention from those who can be managed supportively. MRI can also be used to follow patients with ischemic bowel. In these roles, MRI can serve as a potential substitute for invasive procedures or imaging studies utilizing ionizing radiation in the diagnosis and follow-up of ischemic bowel.

The appearance of ischemic bowel on MRI is nonspecific, often mimicking the appearance of other inflammatory or infectious conditions of the bowel. Ischemic bowel appears as segmental bowel wall thickening and mural edema, with surrounding edema and/or fluid. Mural stratification, with a central layer of hyperintensity surrounded by intermediate signal on either side on T2-weighted imaging (“target” or “halo” sign), may be present (Fig. 23.19). The ischemic segment of the bowel may also be dilated [6775]. The distribution and length of bowel involvement can be variable. A particularly vulnerable segment of the colon in ischemic bowel is the splenic flexure due to tenuous and sometimes absent marginal artery of Drummond connecting the superior and inferior mesenteric arterial systems. The rectosigmoid junction is also at risk due to the tenuous supply at the inferior mesenteric artery and hypogastric artery anastomosis [74].

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Fig. 23.19

(a) Coronal and (b) axial single-shot FSE T2-weighted images in a 39-year-old woman at 25-week gestation presenting with excruciating abdominal pain demonstrate multiple, dilated loops of fluid-filled small bowel in the left abdomen with mural stratification (arrow), as well ascites. Intraoperatively, small bowel volvulus from an adhesion was identified resulting in ischemic bowel

23.6 Bowel Obstruction

Intestinal obstruction during pregnancy is a rare occurrence, ranging in incidence from 1 in 1500 to 1 in 66,000. The consequences are, however, immense. Complications include the need for bowel resection (23 %), preterm labor (62 %), maternal mortality (6 %), and fetal mortality (20–26 %) [7678]. Unfortunately, common symptoms of bowel obstruction such as nausea, vomiting, and constipation overlap with those seen in normal pregnancy, and therefore clinical suspicion of bowel obstruction must be maintained in pregnant patients when abdominal pain and tenderness is reported.

Mechanical obstruction of the bowel occurs with increasing frequency with progressive gestational age in pregnancy [79]. Causes include adhesions, volvulus, intussusception, carcinoma, hernia, and appendicitis. Adhesions are by far the most common etiology (58 %), particularly in those with prior surgical history [80]. Volvulus also has a disproportionately high incidence during pregnancy of 24 %, as compared to only 3–5 % of nonpregnant women [8182]. Volvulus of the sigmoid colon is one of the only causes of obstruction that may potentially be successfully managed without surgery by decompression and detorsion via endoscopic or colonoscopic techniques [83].

MRI, and in particular single-shot T2-weighted imaging, has been shown to be an excellent imaging modality in determining the location and severity of small bowel obstruction without utilizing oral or intravenous contrast agents [8485]. Multiplanar SSFP imaging without oral or intravenous contrast has also been demonstrated to be useful in depicting small bowel obstruction in pregnancy and determining the level of obstruction [86].

On MRI, intestinal obstruction results in bowel dilatation with decompression of downstream bowel loops. An abrupt transition point may be identified at the culprit site (Fig. 23.20). Obstructed bowel loops are fluid filled, with multiple air-fluid levels usually identified in the obstructed segments. Bowel wall and mesenteric edema is often present, as well as ascites (Fig. 23.21).

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Fig. 23.20

(a) Axial and (b) coronal single-shot FSE T2-weighted images of a 34-year-old woman patient with prior colectomy for ulcerative colitis and at 16-week gestational age demonstrate diffusely dilated, fluid-filled loops of small bowel and large amount of ascites compatible with small bowel obstruction. Abrupt transition to decompressed bowel was noted at the right lower quadrant ileostomy site (arrow)

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Fig. 23.21

(a) Sagittal and (b) coronal single-shot FSE T2-weighted images along with (c) axial single-shot FSE T2-weighted image with fat suppression in a 36-year-old woman pregnant with twins at 33-week gestational age depict distended, fluid-filled loops of small bowel within the right lower quadrant (asterisk) with mural edema and surrounding ascites. Etiology of obstruction was confirmed intraoperatively to be due to adhesions

23.7 Neoplasm

Neoplasms of the bowel are rare in pregnancy, but can be diagnosed and staged with MRI [87]. For instance, despite being one of the most common malignancies worldwide, only 1 % of gastric adenocarcinomas are diagnosed during pregnancy. Prognosis is poor even in operable scenarios. MRI can contribute to prognostic calculation and management decisions by allowing characterization of the primary tumor in its morphology (fungating, excavating, ulcerating, or infiltrating). In addition, MRI can determine the T stage based on depth of invasion and assess for nodal involvement, with accuracy equal or greater than that of CT (Fig. 23.22) [88].

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Fig. 23.22

Coronal single-shot FSE T2WI demonstrates extensive infiltrative mass of the distal stomach (arrows) in this Cambodian 47-year-old patient at 28-week gestation

The incidence of colorectal cancer during pregnancy is exceedingly rare, complicating approximately 0.002 % of pregnancies [89]. Despite its rarity, colorectal cancer is among the top eight most common malignancies during pregnancy. Both the diagnosis and management are extremely challenging, often guided by fetal gestational age. Typical presenting symptoms of vague abdominal pain, anemia, rectal bleeding, changing bowel habits, nausea, and vomiting are often masked by pregnancy, resulting in delayed diagnosis and poor prognosis [90]. Mean survival of women diagnosed with colorectal cancer during pregnancy is only 5 months [91]. The rectum is the most frequent site of involvement, typically presenting during the second or third trimesters at stage 3 [92].

Choice of diagnostic imaging modality in suspected colorectal cancer will be affected by regard for fetal well-being. As such, CT is avoided due to its ionizing radiation. Ultrasound may have utility in local staging of a known rectal cancer but is unreliable in a global overview. A gentle flexible rectosigmoidoscopy may be preferred, with some potential utility of noncontrast-enhanced MRI [93]. For initial preoperative evaluation of rectal cancer by MRI, a critical sequence is high-resolution T2-weighted imaging in an orthogonal plane to the tumor. This sequence allows for the identification of tumor as soft tissue which is slightly hyperintense to the bowel wall, but hypointense to the surrounding fat (Fig. 23.23) [94]. This sequence can also be used to determine the extent of tumor invasion into the wall and extramural tissues enabling tumor staging. MRI can also reliably assess tumor proximity to the mesorectal fascia and involvement of the pelvic side walls and anal sphincter, findings which are critical for determining treatment options [95]. Diffusion-weighted imaging may be useful in localizing tumor, but is limited due to its high sensitivity to bowel gas susceptibility. Diffusion-weighted imaging may be most useful in identification of pelvic lymphadenopathy, but falls short at being able to accurately distinguish malignant from hyperplastic benign nodes [95].

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Fig. 23.23

(a) Axial and (b) sagittal single-shot FSE T2-weighted images in a 42-year-old female at 25-week gestational age demonstrating a mid-rectal mass (asterisk) extending beyond the muscularis propria into the adjacent mesorectal fat (arrows). Findings are consistent with stage 3 rectal cancer

If the decision is made to terminate the pregnancy to allow for optimized maternal treatment, imaging options can be expanded to include all those available to the nonpregnant population, including the use of intravenous gadolinium-based contrast agents which would highlight areas of abnormal enhancement.

23.8 Diverticulitis

Acquired colonic diverticula are the sequela of increased intraluminal pressure and weakening of the colonic wall resulting in mural outpouchings. Diverticular disease is common in the Western aging population, reaching a prevalence of 75 % in patients over the age of 80, a fifth of whom may manifest superimposed obstructive diverticulitis [96]. In young adults, diverticulosis is rarely present, thereby making diverticulitis an exceedingly rare event [97]. In pregnancy diverticulitis has only been reported in several individual cases. Regardless, diverticulitis can be seen at any age, including in the reproductive years, especially given the current obesity epidemic and ubiquitous low-fiber diet in the Western Hemisphere.

MRI in the general population for detection of diverticulitis and associated complications has excellent sensitivity and specificity of 86–94 % and 88–92 %, respectively [63]. MRI features of diverticulitis are similar to that seen on CT. Short segment colonic wall thickening with surrounding pericolic fat stranding is seen involving a segment containing at least one diverticulum, often at the epicenter of the inflammatory process (Fig. 23.24). Extraluminal fluid collections and extraluminal gas are findings indicative of perforation, though the sensitivity for the detection of small foci of gas is limited on MRI. Fistulae can also form as a complication of diverticulitis and often can be defined with multiplanar T2-weighted sequences as hyperintense linear tracts [9899].

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Fig. 23.24

(a) Sagittal single-shot FSE T2-weighted and (b) axial SSFP images in a 29-year-old female at 9-week gestational age with right lower quadrant pain demonstrate pericecal inflammation surrounding an inflamed diverticulum (arrow), compatible with cecal diverticulitis

23.9 Primary Epiploic Appendagitis

Fat-containing sacs of the peritoneum distributed in a linear fashion along the free taenia and taenia omentalis from the cecum to the sigmoid colon are known as epiploic appendages. Despite unknown function, their multiplicity, pedunculated morphology, and precarious vascular supply via colic arterial branches predispose these appendages to torsion and infarction. This event most typically occurs in the left lower quadrant in obese patients in the second to fifth decades of life [100]. Although symptomatic, this condition is most often self-limiting, treated medically with pain management, and expected to resolve within 1 week of symptom onset.

Currently, there is a paucity of literature regarding the incidence, management, and outcome of epiploic appendagitis during pregnancy. It certainly should remain on the differential consideration for potential gastrointestinal cause of pain during pregnancy, given that the diagnosis of this entity could result in the avoidance of surgery.

On MRI, acute epiploic appendagitis can be identified as focal inflammation with fat stranding adjacent to the colon, with epicenter along the antimesenteric pericolonic fat (Fig. 23.25). An ovoid lesion up to several centimeters in size, following signal characteristics of fat (hyperintensity on T1-weighted imaging with drop of signal with fat suppression), is highly suggestive. A peripheral rim of visceral peritoneum is typically evidenced by hypointensity on T1- and T2-weighted imaging. A central low-signal dot on either T1- or T2-weighted imaging could reflect a thrombosed supplying artery or central necrosis [100].

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Fig. 23.25

Axial (a) out-of-phase and (b) in-phase T1-weighted GRE and (c) single-shot FSE T2-weighted images demonstrate an ovoid lesion adjacent to the sigmoid colon within the left anterior pelvis with internal signal characteristics following fat and a peripheral rim of hypointensity (arrow), compatible with epiploic appendagitis

Identification of a pericolonic inflammatory process centered on a fat-containing lesion warrants consideration of a short differential diagnosis. Firstly, focal infarction of the greater omentum has both similar clinical and imaging features. A distinguishing characteristic is the typical omental location, medial to the colon, as well as larger size of omental involvement as compared to epiploic appendagitis. Omental infarction, when uncomplicated, also can be managed conservatively. Secondly, inflammation of an epiploic appendage secondary to another process, such as diverticulitis or appendicitis, is less of a trivial consideration. In secondary epiploic appendagitis, despite identification of a fat-containing antimesenteric lobule with surrounding inflammatory changes, note should be made of the epicenter being the adjacent bowel, with degree of wall thickening, edema, and inflammation being the dominant finding [101].

23.10 Conclusion

The diagnosis of both common and rare gastrointestinal tract entities is complicated in pregnancy and often hinges upon diagnostic imaging. MRI, because of its lack of ionizing radiation, mutliplanar capabilities, and excellent soft tissue contrast, is emerging as a primary imaging modality in the evaluation of the bowel pathology during pregnancy. Pregnancy, however, also presents many challenges for imaging the maternal bowel with MRI, some of which can be circumvented with the use of short, tailored MRI protocols with breath-hold independent, ultrafast sequences. Utilization of relatively newer sequences such as DWI has also enabled improved identification and characterization of bowel diseases without the need for intravenous or oral contrast. With future advances in MRI sequence development, the ability of MRI to accurately diagnose various bowel conditions in pregnancy will undoubtedly continue to grow.

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