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British Journal of Radiology (2008) 81, 91-98
© 2008 British Institute of Radiology
doi: 10.1259/bjr/96187638
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Pelvic phased-array MR imaging of anal carcinoma before and after chemoradiation

D M KOH, MRCP, FRCR 1 A DZIK-JURASZ, FRCR, PhD 1 B O'NEILL, MRCP 2 D TAIT, MD, FRCR 2 J E HUSBAND, DBE, FRCR, FRCP 1 and G BROWN, MD, FRCR 1

1 Academic Department of Radiology, 2 Department of Radiation Oncology, Royal Marsden Hospital, Sutton, UK

Correspondence: Dr D M Koh, Academic Department of Radiology, Royal Marsden Hospital, Cancer Research UK Magnetic Resonance Group, Institute of Cancer Research, Downs Road, Sutton, SM2 5PT. E-mail: dowmukoh{at}icr.ac.uk


   Abstract
Top
 Abstract
Introduction
 Methods and materials
 Results
 Discussion
 Conclusions
 References
 
The aim of this study was to evaluate the MR findings of anal carcinoma using an external pelvic phased-array coil before and after chemoradiation treatment. 15 patients with carcinoma of the anal canal underwent T2 weighted and short-tau inversion recovery (STIR) imaging before and after chemoradiation. Images were reviewed in consensus by two radiologists. At pre-treatment imaging, the tumour size and stage, signal intensity and infiltration of adjacent structures were recorded. MR imaging was repeated immediately after chemoradiation, every 6 months for the first year and then yearly. Tumour response was assessed by recording change in tumour size and signal intensity. Prior to treatment, the mean tumour size was 3.9 cm (range, 1.8–6.4 cm). Tumours appeared mildly hyperintense at T2 weighted and STIR imaging. There was good agreement in T staging between clinical examination and MR imaging (kappa = 0.68). In 12 responders with long disease remission, a greater percentage reduction in the size of MR signal abnormality in the tumour area was observed at 6 months (mean 54.7%; 46–62%) than immediately after treatment (mean 38.6%; 30–46%) (p = 0.002, t-test). 7/12 showed stabilization of T2 signal reduction in the tumour area after 1 year, and 5/12 showed complete resolution of signal alterations at 2 years. Pelvic phased-array MR imaging is useful for local staging of anal carcinoma and assessing treatment response. After treatment, a decrease in tumour size accompanied by reduction and stability of the MR T2 signal characteristics at 1 year after chemoradiation treatment was associated with favourable outcome.


   Introduction
Top
 Abstract
 Introduction
Methods and materials
 Results
 Discussion
 Conclusions
 References
 
Carcinoma of the anal canal is uncommon, accounting for less than 2% of large bowel malignancies and 1–6% of anorectal tumours [1]. Its incidence has been reported to be approximately 0.5 per 100 000 in men and 1.0 per 100 000 in women [2].

Anal carcinoma originates between the anorectal junction above and the anal verge below. Not surprisingly, the majority of anal canal cancers are squamous cell carcinoma [3]. Treatment using a combination of chemotherapy and radiotherapy is usually curative [4, 5]. However, radical surgery, such as abdomino-perineal resection, may still be necessary to treat local failure or recurrence after chemoradiation treatment.

Imaging performed prior to treatment provides assessment of the local disease extent and nodal involvement, which is helpful towards treatment planning. Although endoanal sonography has been used for local staging and disease prognostication [6], the introduction of the endoanal probe can be painful and the imaging field of view is limited. Mesorectal lymph nodes located far from the endoanal probe may be missed and inguinal nodes in the groin area cannot be simultaneously assessed. Such limitations are also encountered by the use of endoanal MR imaging alone [7].

More recently, MR imaging using an external pelvic phased-array coil has been found useful for demonstrating the local extent of pelvic disease both for primary anal cancers and for recurrent diseases [8]. Clear delineation of the anatomical boundaries of local disease enables optimal planning of radiation fields. Following chemoradiation treatment, an understanding of the MR pattern of tumour regression would allow careful non-invasive monitoring of treatment response. In addition, appreciation of the range of post-treatment appearances can also aid in the early detection of disease relapse. To our knowledge, the application of MR imaging for monitoring of effects of chemoradiation treatment has not been previously reported in the published literature. Hence, the aim of this study was to evaluate the MR imaging findings of anal carcinoma using an external pelvic phased-array coil before and after chemoradiation treatment.


   Methods and materials
Top
 Abstract
 Introduction
 Methods and materials
Results
 Discussion
 Conclusions
 References
 
The study was approved by our institution research review board and ethics committee. Written informed consent was obtained from all patients prior to the study.

Patient characteristics
15 consecutive patients with anal carcinoma were prospectively evaluated. The inclusion criteria were (a) biopsy-proven carcinoma of the anal canal, (b) patients were selected for primary chemoradiation treatment and (c) all patients had MR imaging before and after chemoradiation treatment. These patients were diagnosed with anal carcinoma between 1999 and 2001. Patients with contraindications to MR imaging were excluded.

There were seven men and eight women with a mean age of 66.2 years (range, 40–81 years). All patients were assessed clinically by digital examination at initial presentation by the primary physician and the tumour stage recorded according to the TNM classification system [9].

Chemoradiation treatment
All patients received a standard regime of chemoradiation comprising 45 Gy of radiotherapy in 25 fractions with or without an additional 15 Gy in 6 fractions to the perianal region. 5-Fluorouracil (100 mg m–2) and mitomycin C (7 mg m–2) was administered systemically in combination with the radiotherapy.

MR imaging
Baseline MR imaging was performed prior to treatment on a 1.5 T MR system (Magnetom Vision, Siemens, Erlangen, Germany) employing a pelvic phased-array coil with the patient in the supine position.

T1 weighted (repetition time (TR) = 128 ms, echo time (TE) = 20 ms, matrix = 256x256, 300 cm field of view (FOV), 6 mm thickness) and T2 weighted (TR >4000 ms, TE = 120 ms, matrix = 256x256, 300 cm FOV, 6 mm thickness) images of the whole pelvis were first acquired. These were supplemented with small FOV T2 weighted (TR >4000 ms, TE = 120 ms, matrix = 256x256, 140 cm FOV, number of excitations (NEX) = 4, 4 mm thickness) and short-tau inversion recovery (STIR) (TR = 4890 ms, TE = 60 ms, T1 = 150 ms, matrix = 256x256, 140 cm FOV, NEX = 2, 4 mm thickness) imaging in the axial and coronal planes at the level of the anal canal. Axial imaging was performed perpendicular to and coronal imaging acquired parallel to the long axis of the anal canal. The total MR examination time was approximately 30 min.

MR examination was repeated using the same imaging protocol after completion of chemoradiation and 6 monthly afterwards for the first year after treatment. If there was no clinical or radiological evidence of disease relapse, yearly surveillance MR imaging was undertaken for up to 3 years.

Image interpretation and analysis
The MR images were reviewed in consensus by two radiologists with more than 10 years' experience in pelvic MR imaging blinded to the clinical outcomes of the patients. The pre-treatment and post-treatment MR images were reviewed sequentially.

Pre-treatment MR imaging
Pre-treatment MR imaging evaluation of the anal carcinoma was evaluated for tumour size and stage, MR signal intensity, infiltration of adjacent structures and the presence of nodal disease.

Tumour size and stage. The maximum diameter of the tumour was measured in either the axial or coronal plane on the T2 weighted MR image to the nearest millimetre. The maximum dimension was used to determine the local tumour T stage as defined by the TNM staging system [9] (Table 1Go). The estimated tumour size by clinical evaluation was correlated and compared with the MR assessment of tumour size.


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  		Table 1. TNM staging of carcinoma of the anal canal

 
Tumour signal intensity. On T2 weighted imaging and STIR imaging, the signal of the tumour was visually compared with the signal intensity of gluteus muscles and recorded as predominantly hypointense, isointense or hyperintense relative to the muscle signal intensity.

Infiltration of adjacent structures. Tumour extension to involve adjacent structures was evaluated on the T2 weighted MR images [10]. The presence or absence of tumour involvement of the rectum, external anal sphincter, puborectalis muscle, levator ani muscle, superficial transverse perineal muscle, coccygeus muscle, ischiorectal fossa, anterior urogenital triangle (vagina/prostate), retropubic space, perianal subcutaneous tissue and perianal skin were assessed and recorded.

Nodal disease. A lymph node was considered malignant if it measured greater than 5 mm in maximum short axis diameter in the peri-rectal area or greater than 10 mm in maximum short axis diameter over the inguinal region or along the pelvic sidewall. Disease was classified using the TNM system.

MR imaging following chemoradiotherapy
The MR images were assessed to evaluate the degree of tumour response by recording the following:

Tumour size. At each visit, the maximum diameter of the tumour was measured on T2 weighted imaging in either the axial or coronal planes. Where no definite tumour was identified at imaging, the maximum diameter of any focal signal change within the anal canal at T2 weighted imaging was recorded and charted.

Signal intensity and appearance. The signal intensity of tumour or focal signal change on T2 weighted imaging was recorded relative to the gluteus muscle. Any distortion in the anal canal or sphincter complex was also noted.

Infiltration of adjacent structure. Following chemoradiation, the degree of involvement of adjacent structures was assessed at 6 months after treatment.

Nodal disease. Regression or enlargement of malignant nodes seen on pre-treatment imaging was recorded.

Statistical analysis
The tumour size determined by clinical assessment was correlated with the measurements obtained by MR imaging. The tumour size measurements were also compared using the paired t-test. The degree of agreement between the local T staging of anal cancer by MR imaging and clinical assessment was determined by kappa statistics.

The mean maximum diameter of the tumour before and following chemoradiation was compared using the paired t-test. The percentage tumour size regression immediately after chemoradiation and at 6 months after chemoradiation was also compared using the paired t-test.


   Results
Top
 Abstract
 Introduction
 Methods and materials
 Results
Discussion
 Conclusions
 References
 
At histology, eight patients had well-differentiated squamous cell carcinoma; four had moderately differentiated squamous cell carcinoma; two had poorly differentiated squamous cell carcinoma and one had transitional basaloid cell carcinoma.

Clinical follow-up information was available in all patients for at least 3 years after chemoradiation treatment (excluding patient who died). Of the 15 patients, 11/15 had MR imaging follow up for 3 years following chemoradiation treatment and 2/15 had MR imaging for only 1 year because they were subsequently followed up elsewhere. Two patients underwent surgery after completion of chemoradiation and did not undergo further MR examinations.

12 patients showed a good response to chemoradiation and were alive and well at 3 years after treatment (Table 2Go). One patient had a poor response to chemoradiation and underwent abdomino-perineal surgical resection (Patient 4). Another patient showed initial response but had a significant residual mass after completion of chemoradiotherapy. An abdomino-perineal resection was performed but no viable tumour was found at histopathology (Patient 3). One patient died of disseminated disease at 12 months after completion of chemoradiotherapy treatment, with persistent disease in the pelvis (Patient 8).


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  		Table 2. Tumour size and signal characteristics at MR imaging before and after chemoradiation

 
Baseline MR imaging
Tumour size and stage
The mean maximum dimension of the tumour measured on T2 weighted MR imaging was 3.9 cm (range 1.8–6.4). The mean maximum tumour size by clinical assessment was 3.6 cm (range 1.0–7.0 cm). There was no significant difference in the maximum tumour size as determined by MR imaging or clinical assessment (paired t-test, p>0.05). A good correlation was found in the tumour size measurement by MR imaging and clinical assessment (r = 0.76, p = 0.001). On MR imaging, the tumour stage was found to be 7% T1 (1/15), 60% T2 (9/15), 7% T3 (1/15) and 26% T4 (4/15). There was good agreement in the T staging of the tumour by the MR imaging and clinical assessment (weighted kappa = 0.68, p<0.01) (Table 3Go). However, clinical examination appeared to under-stage two cases of T4 disease (invasion of urogenital structures) and two cases of stage T2 disease determined by MR imaging.


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  		Table 3. Agreement between clinical staging and MR imaging staging of anal carcinoma

 
Tumour signal intensity
14 out of the 15 tumours appeared hyperintense to gluteus muscle on both T2 weighted and STIR imaging. In the remaining case, the tumour was isointense to muscle on T2 weighted and STIR imaging, and was recognized by distortion of the anal canal. In seven patients, heterogeneity of signal intensity within the tumour was visible on both T2 weighted and STIR imaging.

Infiltration of adjacent structures
Tumours were better delineated with respect to adjacent structures on T2 weighted imaging since STIR imaging diminished the contrast between soft tissues, making it more difficult to define anatomical boundaries (Figure 1Go). The frequencies of involvement of adjacent structures following consensual assessment are tabulated in Table 3Go. Tumour extension frequently involved the sphincter complex (60%). The levator ani muscle was involved in 40%. Extramural spread of disease was usually anterior into the urogenital triangle (27%) to involve the vagina, bladder or urethra. There was inferior extension to involve the peri-anal subcutaneous tissue in 20%. Superior extension to involve the rectum and mesorectum occurred in 33% and 27% respectively. Lateral spread of tumour into the ischiorectal fossa was not observed in patients in our series (Figure 2Go).


Figure 1
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  		Figure 1. (a) T2 weighted and (b) STIR images of a stage T4 anal canal carcinoma. Note the mass arising from the right anal canal, which is mildly hyperintense compared with the gluteus muscle. The mass is infiltrating into the external sphincter (*) and puborectalis muscle (arrowhead). There is also tumour extension anteriorly involving the posterior vaginal wall (white arrows). Anatomical structures are better delineated on the T2 weighted image than on the STIR image.

 

Figure 2
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  		Figure 2. Local tumour extension.T2 weighted (a) axial and (b) coronal images showing a carcinoma arising from the right side of the anal canal. There is anterior tumour extension which is inseparable from the vagina (arrow). On the coronal image (b), note the lateral extension of tumour involving the right levator ani, puborectalis and external sphincter (arrow), but there is no further infiltration into the right ischiorectal fossa. Note also the superior tumour extension to involve the distal rectum (*).

 
Nodal disease
Two patients had stage N1 disease within the mesorectum. Two patients had stage N2 nodal disease along the left pelvic sidewall and inguinal area (Figure 3Go).


Figure 3
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  		Figure 3. T2 weighted MR image showing a large 4 cm left internal iliac nodal mass (arrow).

 
MR imaging following chemoradiotherapy
Tumour size
In the 12 patients who showed long-term remission after chemoradiation, there was initially a 38.6% mean reduction (95% confidence interval (CI) 30–46%) in the maximum diameter of the signal abnormality on T2 weighted imaging at the tumour site immediately after chemoradiation. However, a greater 54.7% mean reduction in the maximum diameter of the tumour (95% CI: 46–62%) was observed at 6 months after chemoradiation compared with the baseline imaging (p = 0.002, paired t-test). There was stabilization in the size of the residual change by 1 year after treatment in 7/12 (58%) patients (Figure 4Go). The remaining 5/12 (42%) showed complete regression of any signal change and no measurable abnormality was observed at 2 years after treatment. One patient did not respond to treatment and showed an increase in size of the tumour during treatment. Another showed 40% reduction in size of the primary tumour after chemoradiation, but substantial residual abnormality remained which prompted surgery. Disease progression was encountered in one patient who developed metastatic disease and persistent disease in the pelvis.


Figure 4
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  		Figure 4. Change in size of the visible abnormality onT2 weighted MR imaging at the site of the tumour before and after chemoradiation.

 
Signal characteristic and appearance
Immediately following chemoradiation, 7/12 patients showed hyperintensity and 5/12 patients showed isointensity at the tumour site at T2 weighted MR imaging. At 6 months, 10/12 responders showed hypointensity at the site of tumour, but 2/12 showed isointensity. There was, however, variable hypointensity at the site of treated tumour at 1 year following chemoradiation. This was accompanied by distortion of the anal canal in 33%, which may be attributed to fibrosis (Figure 5Go). Variable hypointense signal intensity persisted unchanged in 7/12 (58%) but complete resolution of the altered signal intensity occurred in 5/12 (42%) at 2 years, paralleling the reduction in size of the signal abnormality. In the three patients who relapsed or showed disease progression, there was persistent hyperintensity at the site of the tumour.


Figure 5
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  		Figure 5. Response to chemoradiotherapy.(a) Pre-treatment T2 weighted MR image showing hyperintense irregular thickening of the lower anal canal with extension into the right external sphincter. The tumour was stage T2 on MR imaging. (b) Immediately following chemoradiation, residual isointense signal intensity was noted at the site of previous tumour. (c) At 1 year following radiotherapy, there was further regression in the size of the abnormality accompanied by reduction in the signal intensity on T2 weighted MR imaging. (d) This appearance was unchanged on T2 weighted MR imaging obtained 2 years after treatment consistent with post-treatment fibrosis.

 
Infiltration of adjacent structures
Following chemoradiation, there was a reduction in the apparent infiltration of adjacent structures, based on a reduction in the tumour size and associated signal intensity. At 6 months following chemoradiation, the degree of involvement of adjacent structures among the 13 patients with follow-up MR imaging is summarized in Table 4Go.


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  		Table 4. Assessment of infiltration of adjacent structures on MR imaging

 
Nodal disease
There was regression of all malignant nodes visualized at MR imaging prior to treatment. No suspicious nodes were detected after chemoradiation.


   Discussion
Top
 Abstract
 Introduction
 Methods and materials
 Results
 Discussion
Conclusions
 References
 
Squamous cell carcinoma of the anus is an uncommon cancer but is eminently curable using a combination of chemotherapy and radiotherapy [4]. MR imaging with a pelvic phased-array coil using T2 weighted and STIR imaging is useful for identifying tumours within the anal canal and can be used to define the extent of disease [8] prior to non-invasive therapy.

Prior to treatment, anal carcinomas appeared hyperintense on both T2 weighted and STIR imaging. However, T2 weighted imaging was better in demonstrating the relationship of the tumour to adjacent structures since there was greater homogenization of the soft tissue signal intensity on STIR imaging, making it more difficult to delineate normal anatomical boundaries. Thus, we would recommend the use of T2 weighted MR imaging rather than STIR imaging for the evaluation of anal carcinoma. By performing T2 weighted imaging in the axial and coronal planes, the anal canal can be practically assessed in less than 30 min.

In our study, we found good agreement (kappa = 0.68, p<0.01) in the local staging of tumour between clinical examination and MR imaging. Interestingly, there was no significant difference in the assessment of tumour size by both methods. This may reflect the relative superficial location of these tumours, making them amenable to direct measurements. However, clinical examination under-staged four cases compared with MR imaging. Although this did not affect treatment planning in our patients, it is conceivable that, with the increasing use of conformal radiotherapy, accurate delineation of local disease would be important for defining radiotherapy boundaries in the future.

T2 weighted MR imaging was able to define local tumour infiltration by visualizing tumour signal intensity extending into adjacent structures. In our study there was frequent involvement of the sphincter complex (external sphincter, levator ani muscle and the puborectalis muscle). In addition, tumour extension into the urogenital triangle was common (27%) and this may be explained by the relatively thin anatomical separation between the anal canal and the anterior urogenital triangle. Interestingly, tumour extension into the ischiorectal fat was not seen in our study population, suggesting that the levator ani muscle may act as a relative barrier to lateral tumour growth.

Following chemoradiation treatment, the majority of patients (12/15) in our study showed a good response to treatment. This was seen as a reduction in the tumour size accompanied by signal intensity change at T2 weighted MR imaging. Interestingly, in the 12 patients who responded favourably to chemoradiation treatment, there was greater size involution observed on MR imaging at 6 months following chemoradiation than on imaging performed soon after completion of treatment. This observation was perhaps not surprising since radiotherapy could provoke inflammatory reactions that were superimposed on the treated disease and may regress slowly.

In the 12 patients who had sustained remission (>2 years) following chemoradiation, the majority (58%) showed reduction and stabilization in the T2 signal intensity and the size of any residual change at 1 year after chemoradiation. However, continued and complete regression of any residual changes occurred in the remaining 42% at 2 years following chemoradiation. Hence, it would appear that stabilization of any visible residual abnormality more than 1 year after chemoradiation was associated with a favourable outcome. This is potentially important since criteria for non-invasive assessment of disease response using MR imaging have not been previously described. However, these observations were made in a relatively small number of patients and their clinical utility needs to be further verified in future studies.

Following chemoradiation, we found that the reduction in the size of tumour appeared to parallel the reduction in signal intensity on T2 weighted MR imaging. Extrapolating from observations made in rectal cancer following chemoradiation, the appearance of low signal intensity with the treated anal canal on T2 weighted MR imaging is likely to represent fibrosis [10]. However, it would be impossible for MR to detect foci of microscopic disease within these fibrotic tissues, and follow-up imaging is thus important for ensuring stability of appearance, and for the detection of early relapse.

Currently, the routine use of MR imaging for the management of anal cancer is still not widely practised [11]. Treatment and follow-up is still predominantly reliant on clinical evaluation of local disease. The ACT II Trial is a randomized phase III clinical trial that is currently in progress for patients with carcinoma of the anal canal or margin. The objective of this trial is to improve complete response rates and recurrence-free survival without significantly increasing the rates of acute drug toxicity using combination chemoradiation. However, MR imaging has not been specified as a method for the assessment of tumour stage or tumour response. Based on our study findings, we believe that MR imaging should be considered as an imaging tool for the assessment of tumour stage prior to treatment and for the assessment of treatment effects. MR imaging may also facilitate more accurate radiotherapy delivery by providing detailed maps of local disease extent.

There are a few limitations to the current study. Firstly, this study was conducted in a small population and it is uncertain as to what degree our findings can be generalized. However, because carcinoma of the anal canal is rare, it would be difficult to perform a larger prospective study without involving multiple clinical centres. The ideal setting for future studies would be to apply MR imaging in future multicentre clinical trials in anal cancer, which would allow the technique to be widely evaluated. Secondly, the delineation of local disease extent and the regression of tumour after treatment were based on imaging and clinical findings without histopathological confirmation. However, sampling of the tumour area following treatment is not performed routinely and it may be difficult to justify repeated invasive biopsies. Furthermore, even if biopsies were taken, these would still be subject to sampling error. Thirdly, the MR classification of tumour appearance was made according to the visual inspection of the predominant signal intensity. However, as most tumours show some degree of heterogeneity, it was difficult to adequately reflect this by current assessment. Nevertheless, we found that, by comparing with the baseline imaging, a reduction in tumour size, accompanied by a reduction or stability of the MR T2 signal characteristics at 1 year after chemoradiation treatment, was associated with a favourable outcome. However, larger prospective studies in the future would be useful to ascertain the predictive value of the MR observations.


   Conclusions
Top
 Abstract
 Introduction
 Methods and materials
 Results
 Discussion
 Conclusions
References
 
Pelvic phased-array MR imaging was useful for the local staging of anal carcinoma and for the monitoring of treatment response. Prior to treatment, there was good agreement between clinical examination and MR imaging for the local staging of tumour. Following chemoradiation, a reduction in tumour size accompanied by reduction and stabilization of the T2 signal intensity at the site of tumour at 1 year after treatment were associated with a favourable outcome.

Received for publication November 17, 2006. Revision received April 12, 2007. Accepted for publication April 30, 2007.


   References
Top
 Abstract
 Introduction
 Methods and materials
 Results
 Discussion
 Conclusions
 References
 

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  4. UKCCCR Anal Cancer Trial Working Party. UK Co-ordinating Committee on Cancer Research. Epidermoid anal cancer: results from the UKCCCR randomised trial of radiotherapy alone versus radiotherapy, 5-fluorouracil, and mitomycin. Lancet 1996;348:1049–54.[CrossRef][Medline]
  5. Ryan DP, Mayer RJ. Anal carcinoma: histology, staging, epidemiology, treatment. Curr Opin Oncol 2000;12:345–52.[CrossRef][Medline]
  6. Giovannini M, Bardou VJ, Barclay R, Palazzo L, Roseau G, Helbert T, et al. Anal carcinoma: prognostic value of endorectal ultrasound (ERUS). Results of a prospective multicenter study. Endoscopy 2001;33:231–6.[Medline]
  7. de Souza NM. Current and future perspectives on the role of internal coils for magnetic resonance imaging of the anal sphincter and rectum. Abdom Imaging 2002;27:432–41.[CrossRef][Medline]
  8. Roach SC, Hulse PA, Moulding FJ, Wilson R, Carrington BM. Magnetic resonance imaging of anal cancer. Clin Radiol 2005;60:1111–19.[CrossRef][Medline]
  9. Sobin LH, Wittekind C, eds. TNM classification of malignant tumours (UICCS). Houston: John Wiley and Sons, 2002.
  10. Stollfuss JC, Becker K, Sendler A, Seidl S, Settles M, Auer F, et al. Rectal carcinoma: high-spatial-resolution MR imaging and T2 quantification in rectal cancer specimens. Radiology 2006;241:132–41.[Abstract/Free Full Text]
  11. Indinnimeo M, Cicchini C, Stazi A, Ghini C, Mingazzini P, Laghi A. Analysis of a follow-up program for anal canal carcinoma. J Exp Clin Cancer Res 2001;20:199–203.[Medline]



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