Roles of MRI evaluation of pelvic recurrence in patients with rectal cancer

Axial

Anastomotic pelvic recurrence is relatively frequent, especially in nonirradiated, anterior, and low-resection cases, which have higher rates of compromised margins and MRF involvement [28]. Postoperative MRI changes such as architectural distortion, staplers in anastomotic regions, fibrotic scar tissues, treatment-related changes, and inflammatory lesions make it challenging to differentiate viable neoplastic tissues [26].

Anastomotic recurrence can be classified as intraluminal, extraluminal, or combined. Intraluminal recurrence, usually at the anastomotic line, is less common and better visualized in endoscopic studies [34, 35].

MRI is important for anastomotic evaluation because extramural lesions may not be accessible by colonoscopy. Figure 2 shows pre- and postoperative images of a rectal tumor resected with an insufficient distal margin, with anastomosis recurrence characterized by growing solid lesions not seen on the previous postoperative MRI.

Fig. 2figure 2

Case of anastomotic recurrence. A Sagittal T2-weighted image: baseline mrT2N1 (yellow arrow), mesorectal fascia (MRF) clear and no extramural vascular invasion (EMVI). B Post-long-course chemoradiotherapy (CRT) restaging shows response tumor regression grade (TRG) 2 (yellow arrow). C Follow-up after mesorectal excision (ypT2N0), with clear circumferential resection margin (5 mm) and insufficient distal margin: 1.6 cm. D Four months after surgery. Colorectal anastomosis recurrence was detected by endoscopic examination (blue arrow). MRI to plan surgical resection. Absence of sacral, neural, lateral wall and other adjacent organs invasion. Rectosigmoidectomy for anastomotic recurrence resection was proposed

Figure 3 shows another example of recurrence in the anastomosis of a mucinous adenocarcinoma with a poor CRT response.

Fig. 3figure 3

A Baseline MRI showing mucinous adenocarcinoma, mrT2N2 stage, negative mesorectal fascia (MRF), and negative extramural vascular invasion (EMVI) (yellow arrow). B MRI 8 weeks after neoadjuvant chemoradiotherapy (CRT) displaying poor response with tumor regression grade (TRG 5) (green arrow). C MRI 6 months after rectosigmoidectomy revealing incomplete mesorectal resection and insufficient distal margin (0.7 cm). The colorectal anastomosis exhibits a discrete area with a high T2 signal, casting doubt on postoperative changes or mucin (blue arrow). D MRI 1.5 years post-surgery demonstrating recurrence at the anastomosis site. Tissue growth with a high T2 signal was suggestive of recurrent tumor (red arrow). Subsequent surgical planning involved posterior abdominoperineal resection (APR)

Radiologists must carefully inspect the anastomosis, identify suspicious solid tissues, and always compare them with previous examinations, if available, allowing for the detection of small growing lesions [36]. In such cases, DWI helps detect tumor recurrence [37]. Intravenous contrast agent is not required, although it may aid in the detection of recurrence when mucinous lesions are considered [27]. Additionally, the anastomotic location of rectal cancer recurrence is a key factor in assessing resectability. For surgical planning, it is important to describe the distance between the lesion and anal verge, and whether there is infiltration of the levator ani muscle. Therefore, check for endoscopy or digital rectal examination; and map lesions to plan surgical resection.

Lateral

Lateral pelvic lymph nodes represent a risk factor for lateral pelvic recurrence, especially in patients with low rectal cancer that has two lymphatic outflows: the mesenteric lymphatic drainage and internal iliac/obturator vessels [38]. These tumors are not routinely resected during TME or APR in Western countries. In addition to increasing the surgical time and risk of bleeding, radiation-induced injury can complicate resection and increase the risk of injury to the inferior hypogastric plexus [39, 40].

Internal iliac and obturator lymph nodes with a short axis ≥ 7 mm at initial staging are at increased risk for metastatic involvement [41, 42]. In the evaluation after neoadjuvant CRT, the value considered suspicious is > 4 mm on the short axis, and a multidisciplinary evaluation should be performed to evaluate surgical resection, as several studies have demonstrated a reduction in the rate of pelvic recurrence with lymphadenectomy of suspected lymph nodes. By contrast, Japanese studies have demonstrated that involvement of the external iliac lymph nodes is a risk factor for distant metastases, and not for pelvic recurrence [43, 44].

Komori et al [45] demonstrated a 7.3% rate of anatomopathological diagnosis for metastatic involvement of routinely resected lymph nodes without suspicious morphological changes (short axis diameter on CT < 10 mm). Furthermore, in the analysis of pathological lateral pelvic lymph node metastasis, 21.4% of the lymph nodes had a short axis diameter of 5–10 mm, while 5.2% had a diameter of < 5 mm. Thus, the study demonstrated that a cutoff of 5 mm is an important predictive factor for lateral pelvic lymph node metastasis; the 5 mm cutoff is even more relevant for patients who will not receive neoadjuvant CRT.

Figure 4 shows an example of bilateral involved obturator lymph nodes on baseline MRI that underwent lymphadenectomy. The iliac lymph node on the left side was not resected owing to the risk of intraoperative bleeding. A follow-up assessment revealed an infiltrative lesion involving the iliac vessels on the right side. Muscle and bone involvement, as well as the distance of the tumor from these structures, must be reported. Lateral pelvic recurrence can extend to the anterior and posterior structures and must be carefully staged to assess resectability.

Fig. 4figure 4

A Baseline MRI showing mrT4N1 status, with infiltration of the levator ani muscle, positive extramural vascular invasion (EMVI), involvement of the mesorectal fascia (MRF), and intersphincteric plane, with suspicious bilateral pelvic lateral lymph nodes (yellow arrow). B MRI restaging after neoadjuvant chemoradiotherapy (CRT) with a poor response (mrTRG 4), demonstrating reduction in the size of the pelvic lateral lymph nodes (yellow arrow). C Patient underwent abdominoperineal resection (APR) and bilateral pelvic lymphadenectomy; however, the persistence of a suspicious left pelvic lateral lymph node is noted (yellow arrow). Suspicious poorly defined tissue suggestive of recurrence is evident in the right pelvic sidewall (green arrow). D and E show diffusion restriction with a high signal on diffusion-weighted imaging (DWI), and a low signal on ADC of the peritoneal implant (green arrow). F Follow-up MRI revealing unresectable pelvic sidewall recurrence 1 year after surgery, with involvement of the peritoneum, bladder, seminal vesicles, and presacral space (green arrow)

Figure 5 shows resected left lateral pelvic recurrence, evolving with another focus on the recurrent lesion on the left pelvic lateral wall.

Fig. 5figure 5

A Follow-up of a patient who underwent rectosigmoidectomy with coloanal anastomosis, revealing recurrence in the pelvic sidewall (yellow arrow). B The patient underwent abdominoperineal amputation with resection of the recurrent pelvic sidewall, showing usual postoperative changes (green arrow). C During follow-up, there was a progressive increase in serum levels of the tumor marker (CEA), and a nodular formation with intermediate signal intensity on T2-weighted imaging was visualized in the left pelvic sidewall (blue arrow), with diffusion restriction with a high signal on diffusion-weighted imaging (DWI) (D), and a low signal on ADC (E). F Positive fluorodeoxyglucose (FDG) uptake on positron emission tomography (PET/CT) (blue arrow), suspicious for neoplastic recurrence. G, H Follow-up MRI demonstrating growth of the neoplastic tissue (red arrow)

Figure 6 shows an example of a tumor deposit in the left rectoprostatic space that was not resected but evolved into an extensive unresectable lesion during follow-up.

Fig. 6figure 6

A, B Sagittal and axial T2-weighted image: baseline mrT4aN1c (yellow arrow), mesorectal fascia (MRF) positive and extramural vascular invasion positive (EMVI). C Tumor deposit in the rectoprostatic recess (blue arrow) and (D) suspicious lateral pelvic lymph node on the left (green arrow) were also characterized. E Post-long-course chemoradiotherapy (CRT) restaging demonstrates a response tumor regression grade (TRG) 3, with the persistence of the tumor deposit (blue arrow) and pelvic lateral lymph node on the left (not included in the image). F Follow-up after mesorectal excision with colorectal anastomosis revealed the presence of poorly defined tissue with intermediate signal intensity on T2-weighted imaging in the area where the previous tumor deposit and lateral pelvic lymph node were identified, raising suspicion regarding neoplastic recurrence (green arrow). G Positron emission tomography (PET)-computed tomography (CT) scan demonstrating increased radiopharmaceutical uptake in the region adjacent to the left colorectal anastomosis, corresponding to the suspicious tissue (green arrow). H At the 2-year follow-up, there was a notable progression of neoplastic tissue, characterized by infiltration of the rectum, prostate, left seminal vesicle, and pelvic lateral wall muscles (orange arrow). Notably, edema of the left internal obturator muscle is observed, likely related to denervation (red arrow)

Therefore, careful evaluation of the pelvic lateral lymph nodes is necessary in the initial staging, as well as in the follow-up of these patients, for early diagnosis to avoid progression and enable surgical resection [25].

Posterior

Posterior recurrence is characterized by involvement of the presacral fascia, sacrum, coccyx, and nerve roots. Presacral local recurrence is the most common type of local recurrence and has a poor prognosis [28].

Locally recurrent tissues usually have a higher signal intensity than muscle on T2-weighted imaging. However, granulation tissue, hematoma, and radiation-induced inflammatory changes are indistinguishable from tumor recurrence [46]. Thus, attention is required for focal heterogeneous lesions, marked contrast enhancement, early invasive behavior, and asymmetric appearance, which are suspicious for local recurrence [28, 47, 48].

Furthermore, an increase in lesion size over time on serial follow-up imaging is helpful in differentiating postoperative and postradiation therapy changes from tumor recurrence [25].

When staging posterior recurrence, it is important to describe the involvement of the retrorectal space, presacral fascia/space, sacral bone level, and infiltration of the sacral nerve roots (irregular thickening, increased T2 signal, enhancement, diffusion restriction) and muscles (signs of chronic muscle denervation: atrophy and fat replacement; acute changes: edema) [49, 50].

Even in the absence of bone infiltration, the level of presacral fascial infiltration—which may contraindicate surgical treatment—must be described [25]. Figure 7 shows a case of posterior recurrence with an extensive lesion affecting the sacrum and extending bilaterally to the lateral wall.

Fig. 7figure 7

A Sagittal and (B) axial T2-weighted images; the patient underwent abdominoperineal amputation for low rectal cancer with positive circumferential resection margin, developing poorly defined tissue in the posterior pelvic space (yellow arrows), suspicious for neoplastic recurrence. C Positron emission tomography (PET)-computed tomography (CT) demonstrating increased glycolytic metabolism (fluorodeoxyglucose (FDG)) in the presacral tissue and internal iliac arteries, consistent with neoplastic disease (green arrows). No distant metastasis was observed; however, surgery was contraindicated due to the patient’s clinical condition. D Follow-up evidence of an unresectable lesion infiltrating the sacrum and invading the bilateral superior sacral foramen, left lumbosacral plexus, and spinal canal. The lesion extends into the presacral space, causing retraction of the bladder and internal iliac vessels to the left (red arrows). E and F also show extension into the lateral pelvic spaces (blue arrows)

Anterior

Anterior recurrence is the least common type of recurrence, and its prognosis is generally better than presacral and lateral recurrence [28]. It is important to evaluate the extent of tumor recurrence involving the bladder, uterus, vagina, prostate, and seminal vesicles for adequate surgical planning; moreover, extended radical resection is often required to optimize the likelihood of achieving a tumor-free resection margin [51].

Imaging pitfalls

Figure 8 shows some MRI patterns that may mimic neoplastic lesions that make the early diagnosis of recurrence challenging. Overdiagnosis may lead to unnecessary procedures; thus, it is important for radiologists to familiarize themselves with these imaging aspects to facilitate the evaluation of follow-up images. For example, areas of steatonecrosis can appear as viable neoplastic tissue on MRI; CT can aid the diagnosis, as the detection of macroscopic fat components is straightforward on CT.

Fig. 8figure 8

A, B The patient underwent rectosigmoidectomy (pT2N0). MRI 9 months after surgery revealed a nodular lesion with intermediate T2 signal anterior to the mesocolon (yellow circle). Suspected tumor recurrence. C, D Computed tomography (CT) demonstrating a fatty nodular lesion consistent with steatonecrosis (yellow circle). E Steatonecrosis focus reduced after 4 years of follow-up, and the absence of pelvic recurrence was observed. F Another case of a patient who underwent abdominoperineal amputation with omental flaps. Solid tissue on the surgical resection bed was misinterpreted as recurrence (green arrow). G Comparison of CT scans shows omental flaps mimicking pelvic recurrence (green arrow). H Follow-up examinations reveal tissue shrinkage with increased fibrotic content. Stability was observed for 5 years, supporting no signs of recurrence and indicating a pattern of postsurgical changes (green arrow)

Awareness of the surgical technique performed is also helpful; for example, omental flaps, which are used to decrease morbidity associated with reducing the size of the remaining dead space with well-vascularized tissue after APR, can also simulate recurrence [52]. Another surgical technique is the double-stapling technique, which is routinely used for anastomosis during TME. This technique has been sporadically associated with implantation cysts (Fig. 9) and should be considered in the differential diagnosis of cystic lesions and local recurrence [53]. Differentiation may be more difficult in cases of mucinous adenocarcinoma, and stable behavior on follow-up scans suggests the benign nature of this condition.

Fig. 9figure 9

A Sagittal and B axial T2 following adjuvant chemoradiotherapy (CRT). A cystic formation was observed at the anastomosis site with peripheral intermediate T2 signal, raising suspicion for residual tissue/recurrence. The high T2 signal could potentially correspond to mucin. C, D MRI at the 6-month follow-up revealed persistent cystic formation, which remained stable with no evidence of growth. Diffusion-weighted imaging (DWI) (E) and ADC (F) do not exhibit any diffusion restrictions. G Positron emission tomography (PET)-computed tomography (CT) showing negative fluorodeoxyglucose (FDG) uptake at the location of cyst formation. Cystic formation was interpreted as a postsurgical change

Figure 10 shows another postoperative case of mucinous adenocarcinoma that evolved with extensive collection in the presacral space extending to the ischioanal fossa, and was associated with multiple fistulous tracts with colorectal and perianal anastomoses. After surgical resection of the rectal stump and the diagnosis of mucinous recurrence, the patient ended up with a recurrence of collections with a mucinous component. It should be noted that it can be difficult to differentiate fluid collection from recurrence; in this case, solid areas with enhancement aided in the diagnosis of recurrence [54].

Fig. 10figure 10

A A patient with mucinous adenocarcinoma of the rectum treated with surgery and radiotherapy underwent rectosigmoidectomy. They developed an extensive collection in the presacral space (yellow arrow) extending into the ischioanal fossae in the late postoperative period, associated with multiple fistulous tracts involving the colorectal and perianal anastomosis. B Axial T1 postcontrast image demonstrating collection in the presacral space (yellow arrow). C and D show enlargement of the collection, even after drainage (red arrow). E, F The patient underwent resection of the rectal stump with terminal colostomy, with persistence of the anal canal and diagnosis of mucinous recurrence in the surgical specimen, evolving with recurrence of the pelvic collection with high signal intensity on T2-weighted imaging and solid enhancing areas, suspicious for mucinous neoplastic recurrence

Figure 11 depicts a case of local resection of a rectal tumor with extrinsic growth of a small nodular area on the posterior wall along the scar of the resection bed. This case reinforces the importance of comparison with previous examinations for the early diagnosis of recurrent neoplastic tissue. Imaging techniques, such as endoscopic examination, CT, and PET-CT, can aid in early recurrence detection; however, according to some authors [54], PET-CT should be avoided for 6 months following pelvic radiation therapy to avoid incorrect interpretation, as inflammatory changes following radiation therapy can also affect PET findings. FDG-PET also performs poorly when evaluating recurrent, mucin-filled tumors [53] (Table 4).

Fig. 11figure 11

A Sagittal and B axial T2-weighted images. A patient with distal rectal cancer underwent local resection (pT2). MRI revealed a low signal intensity scar (yellow arrow) with no evidence of mesorectal disease. C, D Follow-up MRI at 5 months revealed missed changes within the mesorectal fat posterior to the scar (blue arrow). E, F Follow-up MRI at 1 year demonstrating missed scar recurrence extending along the mesorectal fat (green arrow). Changes from fat stranding to a nodular lesion along the mesorectal fat near the scar should raise suspicion of recurrence after local resection. Endoscopic studies failed to detect extraluminal recurrence. G, H Posterior follow-up at 1 year and 6 months revealed a mucosal lesion (red arrow). Local recurrence was detected using endoscopy with a positive mesorectal fascia. Treatment with chemoradiotherapy and total mesorectal excision was indicated

Table 4 Differentiating pelvic recurrence from other benign lesionsResectability and unresectability criteria

Patients with pelvic recurrence have worse prognoses, with an impact on morbidity and mortality. The involvement of the sacrum and/or sacral nerves may cause sacral nerve pain, perineal ulcers, fistulas, bleeding, bowel and/or urinary tract obstruction, and sepsis [55]. These conditions are difficult to treat, and chemotherapy provides minimal benefits [56].

Surgical treatment may involve total pelvic exenteration and/or distal sacrectomy, and should only be considered in carefully selected populations [12]. This surgery can provide pain control, prolong survival, and possibly cure the disease [57]; however, careful systemic staging is recommended whenever local recurrence is diagnosed as it is a risk factor for metastatic disease [58].

It is important to describe in the report all the anatomic landmarks to guide the surgical team in evaluating potentially resectable lesions and helping in surgical planning. The suspicion of ureteric involvement is important for surgeons, and the involvement of the levator muscles or other pelvic floor structures does not preclude resection [25].

The main MRI-determined unresectable lesions that contraindicate surgical treatment for pelvic recurrence are [12, 59, 60] (Fig. 12):

A.

Proximal sacral invasion (S1/S2): proximal lesion resection leads to sacral instability.

B.

Invasion of the nerve roots of the sacral plexus.

C.

Tumor encasement of bilateral iliac vessels.

D.

Extension of tumor into the sciatic notch.

E.

Extensive pelvic sidewall involvement.

Fig. 12figure 12

A, B Axial T2 images demonstrating unresectable posterior pelvic recurrence, with extensive involvement of the presacral space, sacrum (up to the level of S1), sacral plexus invasion, and bilateral iliac vessel invasion

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