Dra. Asunción Torregrosa Andrés
Hospital de Manises. Valencia
Crohn’s disease is an ulcerating and fistulising chronic inflammatory disease that presents periods of exacerbation that alternate with other periods of inactivity. The most commonly impaired site is the small intestine, particularly the terminal ileum.
It is calculated that up to 80% of patients with ileal or ileocolic impairment will have a surgical resection of the affected tract due to complications in fistulising or stenosing disease, or a lack of response to the available medical treatments. Surgery is not curative, since relapse after ileocaecal resection is a characteristic of the disease, with an endoscopic recurrence as high as 73% the first year after surgery, which rises to 85% in the following three years, even in the absence of clinical symptoms1,2 that typically manifest in the ileocolic anastomosis and/or in parts of the intestine proximal to it (Fig. 1).
Ileocolonoscopy is considered the gold standard for assessing postoperative recurrence, and it is recommended that an ileocolonscopy be performed 6–12 months after surgery. Based on the Rutgeerts score1, which measures the presence and severity of postoperative endoscopic lesions , the objective of the test would be to identify patients with severe lesions, which has a predictive value for the appearance of clinical recurrence, the development of complications, and even the need for another surgery, which has implications in the selection of the most adequate treatment for high-risk patients2-4.
However, endoscopic techniques can only assess the mucosa, not transmural changes of the disease; in addition, they are less accepted by patients and are not exempt from risks. Also, the disease recurs in the anastomosis and in the intestine proximal to it, and endoscopy is oftentimes unable to assess the lumen beyond the anastomosis due to impassable stenoses (Fig. 2), which is why it is currently important to have noninvasive imaging techniques available that can assess both the intestinal wall and the mesentery, as well as most of the intestinal tract in a single study.
A systematic review of 68 articles by Panés et al. concludes that the techniques that allow for obtaining transversal slices, such as ultrasound, computed tomography (CT) and magnetic resonance imaging (MRI), have a high accuracy for the evaluation of Crohn’s disease, reliably evaluate the severity and complications of the disease and offer the possibility of controlling the disease progression5.
Therefore, the initial diagnostic test to assess the presence of inflammatory activity would depend on the availability of techniques in various sites, as well as the experience of the radiologists with each one of them, considering the limitation of the use of CT due to the radiation dose that it provides, especially in young patients.
MAGNETIC RESONANCE ENTEROGRAPHY IN THE POSTOPERATIVE FOLLOW-UP OF CROHN’S DISEASE
The use of MRI in the assessment of patients with Crohn’s disease is on the rise, in terms of diagnosing, follow-up and assessing postoperative recurrence, as is demonstrated by the great number of scientific publications on the topic and the fact that it is increasingly being incorporated in daily clinical practice by inflammatory disease units6. Without a doubt, the most powerful reasons why MRI is increasingly in demand are its high capacity for tissue differentiation and, particularly, its lack of ionising radiation, along with its ability to assess the abdominal cavity, and therefore the entire gastrointestinal tract, in one single study. There are works in the literature that study the use of MR enteroclysis in the postoperative recurrence of Crohn’s disease4, which achieves a sensitivity of 100% and a specificity of 89% in detecting moderate or severe relapse, and it is even preferred over endoscopy in regards to the ability of the former to assess the entire intestinal tract in a single examination. However, based on previous studies in which diagnostic accuracy is demonstrated to be similar to MR enteroclysis for detecting Crohn’s disease and its complications7,8, MR enterography with an intake of 1–1.5 L of a mannitol or polyethylene glycol (PEG) solution is the most used MRI technique, for it is less agressive than enteroclysis and requires less time in the room with absolutely no radiation.
Just as in patients who did not undergo surgery, MR enterography does not provide clear semiological criteria for the detection of inflammatory activity, both intestinal, such as mural thickness, the presence of oedema, ulcers and hyper-enhancement of the affected intestine after administering contrast, as well as mesenteric, such as perienteric oedema, lymphadenopathy and the presence of abscesses.
In relation to the study of stenoses, it is recommend that multi-phase sequences be used that enable visualisation of the fixed loop, which does not change during the sequence (Video 1), with the possible presence of prestenotic dilatation (Fig. 3), which could undergo homogeneous enhancement after contrast administration, as well as mural oedema in T2-weighted sequences with fat suppression that reflect a higher or lower inflammatory component9.
However, there is great variability in the MRI technique used. Although today the use of MR enterography is being generalised, there is evidence in recent literature of the considerable use of the enteroclysis technique based on sites, as well as evidence of variability between the oral contrast used, the intake volume and time of the contrast. The combination of MR sequences and the use of intravenous contrast is also more homogeneous. It is important to globally apply a MR enterography that enables the comparison of results and the validation of scoring systems.
In patients that are treated with total colectomy and an ileoanal pouch, due to the preoperative diagnoses of indeterminate colitis or ulcerative colitis, and that later are re-evaluated as Crohn’s patients, follow-up is also established to rule out the recurrence of the disease or the appearance of complications and the normal findings must be known in order to differentiate them from the pathological findings. An Ileoanal pouch is made by a laterolateral anastomosis of the last ileal loop that, in turn, is anastomosed with the anus. The suture line must be identified with both RM and CT, which will appear hyperdense in the CT and hypointense in T1-T2 sequences in MRI, and it could produce paramagnetic elements in some sequences such as the diffusion weighted imaging (DWI).
Therefore, these patients can present a recurrence of the disease, whose more specific signs are the presence of stenosis, abscesses or fistulae10, which have to be differentiated from pouchitis or the non-specific inflammation of the pouch wall (Fig. 4).
Also, patients who have undergone a final colostomy due to severe perianal disease, and who do not respond to treatment, may experience a relapse, more often in the stoma and in the colon next to it, which can be assessed by endoscope and ultrasound with no problems due to easy accessibility. MR enterography, and, in particular, the diffusion weighted sequence have great sensitivity for its assessment (Fig. 5).
COMPUTED TOMOGRAPHY AND ULTRASOUND IN THE POSTOPERATIVE FOLLOW-UP OF CROHN’S DISEASE
Until the past few years, CT has been the technique of choice for assessing the activity in patients with Crohn’s disease, especially in the diagnostic management of extraluminal complications of the disease. It has high sensitivity and specificity in detecting enteroenteric or enterocutaneous fistulae and abscesses. However, the use of ionising radiation makes its repeated use less ideal, especially in young patients, given the risk of developing abdominal neoplasias that entail cumulative radiation11. Still, due to its great temporal-spatial resolution and great availability, it is a technique that is greatly used for detecting activity in patients with suspected postoperative recurrence. The best sensitivity and specificity values in regards to inflammatory activity and the presence of complications are obtained when the CT is performed with oral contrast administration for the distension of the small intestine loops. In this way, there are authors that prefer nasojejunal intubation for introducing oral contrast, or CT enteroclysis, while others prefer CT enterography due to its high comfort level and safety, in which intestinal distension is achieved by intaking a 1–1.5 L volume of contrast. Thus, the most used substances are methylcellulose in the case of CT enteroclysis, and mannitol or PEG in CT enterography.
The findings assessed with CT for diagnosing the recurrence in patients with ileocolic resection are:
• Wall thickness with hyper-enhancement and stratification.
• Pre-anastomotic dilatation.
• Increase in the number and size of the vasa recta.
• The presence of hyper-uptaking lymphadenopathy.
• The presence of abscesses and/or fistulae (Fig. 6).
In the work of Soyer et al., it was found that the stratified enhancement and thickness >3 mm of the anastomosis are two independent variables for differentiating normal and pathological anastomosis, with a specificity of 100% in the relapse diagnosis for the former12; also, the stratified enhancement and the “comb sign” are two variables for differentiating inflammatory recurrence and fibrostenosis.
It is not clear what role CT colonography can play in diagnosing postoperative recurrence. Biancone et al. studied a short series of 16 patients with this technique and with optic colonoscopy. They found it useful in patients with postoperative stenosis with difficulty in endoscopic follow-up13. In clinical practice, it can be an alternative technique to endoscopy in select cases of patients with colonic stenoses that do not allow passage of the endoscope or in patients who reject endoscopy.
Barium swallow is one of the techniques available for detecting the recurrence of inflammatory activity, and it has been traditionally used in the study of patients with suspected or confirmed luminal Crohn’s disease. Its most notable characteristics are the excellent visualisation of the mucosal pattern and information on the intestinal dynamics; however, it currently has been displaced in virtue of sectional techniques, due to their higher capacity to assess not only the mucosa but also the rest of the intestinal wall as well as the extraluminal component of the disease, with these radiological techniques being subject to the interest and degree of experience of the radiologist, as well as the variability in interpreting the images. Patel et al.14 published a study that compares the sensitivity and specificity of intestinal transit and CT with oral contrast in detecting inflammatory relapse in the neo-terminal ileum, achieving values of 90%, 85%, 77% and 69%, respectively, reaching 95% and 69% when both tests are combined. These authors conclude the study by indicating the use of barium swallow for a better capability than CT in detecting aphthous ulcers, while the latter is more useful in detecting extraluminal complications such as abscesses.
Ultrasound is a noninvasive technique that does not use ionising radiation, is well tolerated by patients and has shown good accuracy in assessing and detecting postoperative recurrences15. Its capability to detect and locate the disease is the factor that most influences its diagnostic accuracy2. Due to its great availability, it is one of the most used imaging techniques, although it is a dependent operation and assessing deep segments can be difficult. It can be performed conventionally by assessing wall thickness and the degree of the Doppler signal of the wall of the affected loop, the stenosis and/or dilatation of the loops and the impairment of the mesentery (Fig. 7), as well as complications such as fistulae and abscesses.
At some sites, ultrasound tests are performed with luminal distension via the oral intake of fluid, which can increase their sensitivity and specificity to detect lesions in patients with suspected or confirmed Crohn’s disease. These are an alternative for assessing postoperative recurrence in these patients16. However, Castiglioni et al. compared both ultrasound techniques, and the sensitivity and specificity did not significantly increase when oral contrast was administered in order to recommend the routine use of the contrast within the clinical context of the postoperative recurrence17.
In the work done by Martínez et al., the ultrasonographic parameters that show a high correlation with the presence of clinical or biological activity are the wall thickness and the increase of the colour Doppler signal in the intestinal wall18.
Rispo et al. found a sensitivity of 79% and a specificity of 95% for the recurrence diagnosis in the first year after surgery, reaching 94% and 100%, respectively, when detecting severe cases19 taking a cut-off value of >5 mm for the measurement of the intestinal wall thickness.
Moreover, since the emergence of second-generation ultrasound contrast, contrast enhanced ultrasound (CEUS) is becoming an extremely useful technique in assessing the activity of inflammatory bowel disease in general, and particularly in the case of postoperative recurrence (Fig. 8). Furthermore, with the development of systems that calculate the enhancement percentage of the intestinal wall, the presence of microvascularization resulting from inflammation can be inferred20.
CORRELATION BETWEEN ENDOSCOPIC AND RADIOLOGIC TECHNIQUES
After surgical resection, it is important to detect patients with an early recurrence of the disease in order to establish a medical treatment that prevents the appearance of symptoms, so that endoscopic recurrence does not translate to clinical recurrence. Patients must quit smoking and receive pharmacological treatment within two days following the operation21.
For monitoring treatment, the use of imaging techniques is currently preferred because endoscopy is less accepted by patients and has limitations when exploring segments of the proximal intestine and in the presence of stenosis in anastomosis.
In the first study that compared ultrasound to endoscopy in operated patients, Andreoli et al. obtained a sensitivity of 81%, a specificity of 86% and a diagnostic accuracy of 83% for diagnosing relapses of the disease by applying a cut-off value of >5 mm of the wall thickness. They recommend ultrasound as the technique of choice and ileocolonoscopy for doubtful cases15.
Also, ultrasound with oral contrast in expert hands is valued as an alternative technique to endoscopy in detecting recurrent disease after surgical resection. Calabrese et al. obtained a sensitivity of 92.5 %, a positive predictive value (PPV) of 94% and a diagnostic accuracy of 87.5% when they compared ultrasound with oral contrast to endoscopy (assessed via the Rutgeerts Score)16.
In regards to ultrasound with intravenous contrast, Paredes et al. performed a study on 60 operated patients with Crohn’s disease who underwent both CEUS and endoscopy, with an ultrasound score of 2, which included a wall thickness >5, a wall enhancement >70% or the presence of fistulae. The study presented a sensitivity, specificity and diagnostic accuracy of 97.9%, 91.7% and 96.7 %, respectively, for detecting severe recurrence20.
MR enteroclysis has a predictive value for the relapse of the disease in patients undergoing ileocolic resection according to Koilakou et al. These authors validate the recurrence rate based on the technique proposed by Sailer22, in which they obtained 100% sensitivity and 89% specificity for detecting a moderate to severe degree of involvement when patients were grouped in MR0‑MR1 (absence or mild impairment that would be treated with conventional drugs) and MR2-MR3 (moderate to severe impairment that would need immunosuppressant therapy or even another surgery)4.
The Gallego et al. group compared MR enterography to ileocolonoscopy in operated patients and found a good correlation between both techniques for the activity assessment, by applying an MR activity index and grouping the patients into two groups, without activity or mild, and with moderate to severe activity, in relation to their worst prognosis and the need for more aggressive treatments23.
Minordi et al. found a good correlation between the CT and endoscopy postoperative recurrence findings and were able to differentiate between mild to moderate recurrence (that would be amenable to medical treatment) and severe recurrence (that would require surgery), without finding significant differences between CT enterography and CT enteroclysis for intestinal distension, and therefore, for activity detection24.
In reviewing Panés et al. it was postulated that the degree of abnormalities in radiologic results is similar to the severity of endoscopic lesions with a 2b evidence level and and a B recommendation grade5.
In conclusion, given the high frequency of recurrence of Crohn’s disease after surgery and the need for monitoring of the medical treatment in these patients, it is logical to believe in the need for imaging techniques that do not use ionising radiation, but that do use ultrasound, according to the availability and experience of the radiologist, given its high sensitivity and specificity, preferably with intravenous contrast or MR enterography, leaving CT use for emergency situations or for a strong suspicion of abscesses. However, it would be interesting to achieve a greater homogeneity in regards to the method of performing imaging techniques, especially MRI, as well as the relapse diagnostic criteria for the disease.
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