Comparison of apparent diffusion coefficients of resectable mid‑high rectal adenocarcinoma and distal paracancerous tissue
- Authors:
- Published online on: December 10, 2024 https://doi.org/10.3892/ol.2024.14843
- Article Number: 97
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Copyright: © Luo et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
Colorectal cancer is ranked as the third most prevalent malignancy globally and the second leading cause of cancer-related mortality. Rectal cancer alone contributes to approximately one-third of these cases, with adenocarcinoma comprising >90% (1–3). Total mesorectal excision remains the standard surgical procedure for resectable rectal cancer (4). Despite undergoing curative resection, there is still a recurrence rate of 5–10%, with the distal resection margin (DRM) serving a crucial role (5–7). It has been reported that histologically normal tissues adjacent to tumors undergo molecular alterations associated with tumorigenesis, which can be attributed to field cancerization (8,9). If the tissue exhibiting a precancerous state is not surgically excised, it has the potential to progress into invasive cancer (10). In rectal cancer surgery, an insufficient length of DRM is often associated with a high recurrence rate (5), whilst an excessive length of DRM may result in inadequate remaining rectum and increase the risk of postoperative complications (6). Therefore, it is important to preoperatively determine the optimal DRM for formulating surgical options.
The apparent diffusion coefficient (ADC), derived from the signal intensity of diffusion-weighted imaging (DWI), quantitatively evaluates the mobility of water molecules and indirectly reflects the biological characteristics of tissues (11–13). In general, the presence of low ADC values indicates a restriction in the diffusion of water molecules, which is commonly observed in several pathological conditions, such as inflammatory, fibrotic or neoplastic processes (11,14). It has been reported that an increase in both the mobility and quantity of water molecules during the transition from normal cells to cancerous cells leads to differences in water molecule diffusion within tissues at different stages of tumorigenesis (15). In addition, stem cells derived from adjacent tissues of the tumor have the potential to induce fibrosis and an inflammatory response (16), thereby affecting the ADC values of paracancerous tissues.
Chen et al (17) reported that ADC can be used to differentiate between tumor tissues, tumor-adjacent tissues and tumor-distant tissues in rectal adenocarcinoma (RA); however, the investigation of distal paracancerous tissues only involved the tissues located ~1 and 2 cm from the tumor margin. Currently, there is no exact standard for the length of DRM (18–20), to the best of our knowledge. Therefore, the aim of the present study was to evaluate differences in ADC values of resectable mid-high RA and distal paracancerous tissues located at several distances from the tumor margin in detail, providing a potential reference basis for preoperatively determining the optimal DRM.
Materials and methods
Patients
The study protocol was approved by the Institutional Review Board of the Affiliated Hospital of North Sichuan Medical College (Nanchong, China; approval no. 2024ER219-1), and the requirement for informed consent was waived owing to the retrospective nature of the present study.
From January 2017 to December 2022, clinical and imaging data from 129 consecutive patients with resectable RA who underwent preoperative pelvic magnetic resonance imaging (MRI) scans were collected from The Affiliated Hospital of North Sichuan Medical College (Nanchong, China). Inclusion criteria were as follows: i) Multi-b-value DWI sequences performed within 2 weeks prior to surgery; ii) no cancer-related treatment administered before undergoing multiple b-values DWI; iii) adenocarcinoma confirmed by pathology; and iv) the distal tumor margin (DTM) was positioned ≥3 cm above the dentate line, as the dentate line represents the transition between rectal columnar mucosa and anal squamous mucosa (21), which can result in significant variations in ADC values of the intestinal wall below and above it. Exclusion criteria were as follows: i) No visible tumors on MRI images (n=2); ii) tumors confirmed as mucinous adenocarcinoma, attributing to their high ADC resulting from the abundant mucinous content (n=5); iii) unsatisfactory image quality due to susceptibility or movement artifacts (n=7); iv) abnormal edema exhibited in the intestinal wall, leading to elevated ADC values (n=3); and v) incomplete MRI images or clinical records of patients (n=2). Finally, a total of 110 patients (62 male and 48 female patients; median age, 66 years; age range, 28–84 years) with RA confirmed by pathology were included in the present study for analysis.
All patients with RA underwent pelvic MRI including DWI 2 weeks before radical resection with regional lymph node dissection. The tumor differentiation, pathological tumor stage (pT) and pathological lymph node stage (pN) for rectal cancer were determined based on the postoperative histopathological examination. Tumors located within 15 cm from the DTM to the anal verge were categorized as rectal neoplasms, further classified into low (0–5 cm), middle (>5-10 cm) and high (>10-15 cm) rectal tumors based on their respective distances from the DTM to the anal verge (22). As the distance from the dentate line to the anal verge was 2–3 cm (21), and DTM was required to be >3 cm above the dentate line in the present study, patients with mid-high RA were included.
MRI techniques
For each enrolled patient, imaging was performed using a 3.0 Tesla scanner (Discovery™ MR750; GE Healthcare) with a 32-channel phased-array torso coil in the pelvic region. The imaging sequences included axial T2-weighted (T2W) fast-recovery fast spin-echo with fat suppression sequence, sagittal T2W Propeller with fat suppression sequence, axial multi-b-value (0, 50, 100, 800, 1,000 and 1,500 sec/mm2) DWI based on echo-planar imaging sequence. The parameters of all sequences are listed in Table I. The patients were positioned in a supine posture during the scanning procedure. The scanning range was from the level of the lumbar 4–5 intervertebral disc to 10 cm below the pubic symphysis, ensuring coverage of the entire rectum.
Image analysis
DWI data were transferred to the Advantage Workstation (version 4.5; GE Healthcare), and ADC maps were automatically generated using the post-processing Functool software (version 10.4.04; GE Healthcare). All images were independently evaluated by two abdominal radiologists (radiologist 1 and radiologist 2, with 7 and 3 years of experience in this field, respectively), and any disagreements were resolved by another expert with 26 years of experience. The expert and two radiologists were blinded to the clinical and histopathology information of patients, except for the diagnosis of RA.
The ADC maps and values were derived from DWI using five different b-value pairs (0 and 50; 0 and 100; 0 and 800; 0 and 1,000; and 0 and 1,500 sec/mm2) based on the mono-exponential model formula: ADC=ln(S0/S1)/(b1-b0), where b represents the diffusion gradient value and S0 and S1 denote the signal intensity of tissue on DWI at b0 and b1, respectively (12,17). The Japanese guidelines recommend a DRM of ≥3 cm for rectal cancer located above the peritoneal reflection and 2 cm for those below it (19). Moreover, there have been very few reports of distal tumor infiltration extending <3 cm (5). Thus, a DRM of 3 cm is generally considered a safe resection margin for patients with rectal cancer. Subsequently, ADC measurements were performed on RA and three distal paracancerous tissues located at ~1 (D1), ~2 (D2) and ~3 cm (D3) from the DTM.
In the present study, the ADCs of RA, D1, D2 and D3 were measured using the single-slice region of interest (ROI) method. Firstly, location of RA was determined based on the T2W and DWI images, where the tumor presented as an irregular thickening of the intestinal wall with isointense or hyperintense signal on the T2W image and hyperintense signal on the DWI image (Fig. 1A-C). Secondly, the locations of D1, D2 and D3 were determined based on the sagittal T2W images (Fig. 1B), whilst the axial DWI images of D1, D2 and D3 were captured at the corresponding locations. Thirdly, on the axial high b-value DWI image, the maximum cross-section of the tumor was selected and an ROI was delineated along the tumor margin whilst carefully excluding necrotic, fatty and vascular regions (Fig. 1C). In accordance with the method described in a previously published report (17), ROIs of D1, D2 and D3 were delineated to cover more than a semicircle of the rectal wall, and the surrounding adipose tissue, blood vessels and luminal gas were excluded (Fig. 1D). After delineating the ROIs for the tumor, D1, D2 and D3 on axial high b-value DWI images, corresponding ROIs were automatically generated on the ADC maps to obtain ADC values for each region (Fig. 1E and F). The ADC measurement was repeated three times for each tissue, and the final value was determined by calculating the average of these three measurements. Additionally, the ADCs of RA, D1, D2 and D3 were independently measured by the aforementioned two radiologists to evaluate the interobserver agreement.
Statistical analysis
Statistical analyses were performed using SPSS software (version 25; IBM Corp.). P<0.05 was considered to indicate a statistically significant difference. The intraclass correlation coefficient (ICC) was used to assess the interobserver agreements for each ADC measurement. The ICC was classified into poor (0–0.20), fair (0.21–0.40), moderate (0.41–0.60), good (0.61–0.80) and excellent (0.81–1.00) agreements (23). If the agreement was good or excellent, the measurements of radiologist 1 were used for subsequent analysis. If the agreement was unsatisfactory, the average of the measurements taken by two radiologists (radiologist 1 and radiologist 2) were used for subsequent analysis.
The ADCs of RA, D1, D2 and D3 were compared using the Friedman test. In cases where the P-values indicated statistically significant differences, post hoc multiple pairwise comparisons between different tissues were performed using the Bonferroni correction test. The results were visually represented using boxplots. Subsequently, variables that demonstrated statistically significant differences in pairwise comparisons underwent receiver operating characteristic (ROC) analysis to assess the efficacy of ADCs in distinguishing between different tissues. In addition, considering that advanced-stage RA may have more cell proliferation compared with early-stage RA, and there may be differences in the length of safe DRM between the two stages, the Mann-Whitney U test was used to analyze the ADCs of different tissues between pT1-2 and pT3-4 stages.
Results
Patient characteristics
A total of 110 patients with RA were included in the present study, comprising 62 (56.4%) male patients and 48 (43.6%) female patients. The median age was 66 years (range, 28–84 years). There were 31 (28.2%) tumors located in the high rectum and 79 (71.8%) tumors located in the middle rectum. The tumor differentiation was observed as well-differentiated adenocarcinoma in 39 (35.4%) patients, moderately differentiated adenocarcinoma in 65 (59.1%) patients and poorly differentiated adenocarcinoma in 6 (5.5%) patients. Regarding the pathological stage, there were 27 (24.5%) patients classified as pT1-2 and 83 (75.5%) patients classified as pT3-4. Additionally, there were 65 (59.1%) patients classified as pN0 and 45 (40.9%) patients classified as pN1-2.
Interobserver agreements of ADCs at different b-value pairs
The interobserver agreements for the ADC values of RA, D1, D2 and D3 are presented in Table II. The interobserver agreements for the ADC values at different b-value pairs were excellent (all ICCs >0.80). Therefore, the measurements obtained by radiologist 1 were used for subsequent analysis.
 | Table II.Evaluation of interobserver agreements for apparent diffusion coefficient values of the tumor, distal paracancerous tissue located ~1, 2 and 3 cm from the tumor margin at different b-value pairs. |
Comparisons of ADCs between RA, D1, D2 and D3
The ADC values of RA, D1, D2 and D3 obtained from different b-value pairs are summarized in Table III. The Friedman test demonstrated significant differences in ADCs between the four different tissues at all b-value pairs (all P<0.001). Post hoc multiple pairwise comparisons using the Bonferroni correction test were performed to further assess the differences in ADCs between different tissues (Fig. 2). The tumor exhibited lower ADC values compared with D1, D2 and D3 at all b-value pairs (all P<0.001). Furthermore, at b-value pairs with the maximum b-value of ≥800 sec/mm2 (0 and 800; 0 and 1,000; and 0 and 1,500 sec/mm2), the ADC of D1 was significantly lower compared with those of both D2 and D3 (P<0.001). However, no significant differences in ADCs were observed between D1, D2 and D3 at b-value pairs with the maximum b-value of ≤100 sec/mm2 (0 and 50, and 0 and 100 sec/mm2; P>0.05). There were no significant differences in ADCs between D2 and D3 at all b-value pairs (all P>0.05).
| Table III.Comparison of apparent diffusion coefficients between the tumor, distal paracancerous tissue located ~1, 2 and 3 cm from the tumor margin at different b-value pairs. |
ADCs of RA, D1, D2 and D3 between different pT stages
The ADC values of RA, D1, D2 and D3 obtained from different b-value pairs at pT1-2 and pT3-4 stages are summarized in Table IV. Only when b=0 and 1,000 sec/mm2, and b=0 and 1,500 sec/mm2, the ADC values of pT1-2 staged tumors were significantly higher compared with those of pT3-4 staged tumors (P<0.05). However, no statistically significant differences in ADC values between tumors with different pathological stages were demonstrated at the other b-value pairs (P>0.05). Furthermore, there were no statistically significant differences in ADC values of D1, D2 and D3 between tumors with different pathological stages at all b-value pairs (all P>0.05). Therefore, further subgroup analysis was not performed.
| Table IV.Comparison of apparent diffusion coefficients of the tumor, distal paracancerous tissue located ~1, 2 and 3 cm from the tumor margin between different pathological tumor stages. |
ROC analyses of ADCs for differentiation between RA, D1, D2 and D3
The efficacy of ADCs in distinguishing between different tissues was assessed using ROC analysis for variables that showed statistically significant differences, based on the aforementioned results. This analysis yielded several metrics, including the cut-off value, sensitivity, specificity, accuracy and area under the ROC curve (AUC), which are presented in Table V. ADCs at the maximum b-value of ≥800 sec/mm2 exhibited superior discriminatory capability in distinguishing RA from D1 (Fig. 3A), RA from D2 (Fig. 3B) and RA from D3 (Fig. 3C) compared with those at the maximum b-value of ≤100 sec/mm2. Particularly at b-values of 0 and 1,500 sec/mm2, ADC cut-off values of 1.009×10−3 mm2/sec, 1.050×10−3 mm2/sec and 1.070×10−3 mm2/sec demonstrated superior ability in distinguishing RA from D1, from D2 and from D3 (AUCs: 0.982, 0.992 and 0.996, respectively). Additionally, ADC cut-off values of 1.522×10−3 mm2/sec (b=0 and 800 sec/mm2) and 1.539×10−3 mm2/sec (b=0 and 1000 sec/mm2) exhibited optimal diagnostic performance in differentiating D1 from D2 (AUC, 0.652; Fig. 4A) and D1 from D3 (AUC, 0.692; Fig. 4B).
| Table V.Receiver operating characteristic curve analyses of apparent diffusion coefficients for the differentiation between the tumor and distal paracancerous tissue located ~1, 2 and 3 cm from the tumor margin at different b-value pairs. |
Discussion
In the present study, the disparities in ADCs between RA and distal paracancerous tissues (~1, 2 and 3 cm from the tumor margin) were evaluated, and the diagnostic performance of ADCs in distinguishing between these tissues was assessed.
As demonstrated in the present study, the tumor exhibited lower ADC values compared with distal paracancerous tissues at all b-value pairs, which was consistent with the results of a previous study (17). A possible explanation for this finding is the higher cellular density and irregular cell morphology within the tumor, which results in narrower and distorted intercellular spaces that restrict the diffusion of water molecules (24,25). Consequently, the tumor exhibits lower ADC values compared with D1, D2 and D3. Furthermore, the present study demonstrated that ADCs at the maximum b-values of ≥800 sec/mm2 (AUCs, 0.963 to 0.996) exhibited superior discriminatory capability in distinguishing the tumor from distal paracancerous tissues compared with those at the maximum b-values of ≤100 sec/mm2 (AUCs, 0.838 to 0.843). Particularly at b-values of 0 and 1,500 sec/mm2, ADC demonstrated optimal diagnostic efficacy in distinguishing RA from D1, D2 and D3 (AUCs, 0.982 to 0.996). The results may be due to the fact that when calculating ADC at the higher maximum b-values, it predominantly reflects the diffusion of water molecules; conversely, when computing ADC at the lower maximum b-value, it primarily reflects microcapillary perfusion (26).
Diffusion and perfusion are distinct physical and biological phenomena, both serving as indicators for several physiological or pathological processes (25). The diffusion coefficient has been reported to be a more effective diagnostic parameter than the perfusion coefficient in distinguishing the tumor from paracancerous tissue (27). Additionally, the findings of the present study indicated that the ADC values of pT1-2 staged tumors were significantly higher compared with those of pT3-4 staged tumors at certain b-value pairs (b=0 and 1,000 sec/mm2, and b=0 and 1,500 sec/mm2), which is consistent with previous studies (28,29). This may be due to the increased density of tumor cells and reduced extracellular space as the tumor progresses, leading to greater restriction of water molecule diffusion.
In the present study, the ADC of D1 was lower compared with those of D2 and D3 at the maximum b-values of ≥800 sec/mm2. Chen et al (17) also reported a decrease in ADC values of D1 compared with D2 in their assessment of distal paracancerous tissues, but the ADC values between D1/D2 and D3 were not compared and cases of lower rectal cancer were not excluded. The result of the present study may be attributed to molecular alterations during tumorigenesis that can lead to abnormal increases in water molecule mobility and quantity (15). In addition, the molecular alterations associated with tumorigenesis are more pronounced in paracancerous tissues located closer to the tumor compared with tumor-distant tissues (8,9). Furthermore, previous research has demonstrated that the more severe the intestinal inflammation and fibrosis, the lower the ADC value (30). Stem cells derived from the adjacent tissues of the tumor have the potential to induce fibrosis and an inflammatory response (16), indicating that inflammation and fibrosis are more pronounced in paracancerous tissues located closer to the tumor compared with tumor-distant tissues. Hence, the diffusion of water molecules is more restricted in D1 compared with D2 and D3. However, there were no significant differences in ADCs at the maximum b-value of ≤100 sec/mm2 between D1, D2 and D3 in the present study. This may be because microcapillary perfusion cannot accurately discern the subtle differences within these tissues.
Currently, there is no exact standard on DWI for the definition of the length of DRM. The present study demonstrated that there were no significant differences in ADCs between D2 and D3 at all b-value pairs, suggesting that D2 and D3 may possess similar biological characteristics, such as microstructure, cell sequencing and tissue composition. Therefore, we hypothesize that the safe DRM in mid-high RA surgery may be reduced to 2 cm. According to the National Comprehensive Cancer Network guidelines, patients with mid-high rectal cancer are recommended to have a DRM length of 4–5 cm (20). Japanese guidelines recommend a minimum distance of 3 cm for DRM in cases of rectal cancer located above the peritoneal reflection and 2 cm for those below it (19). Furthermore, there have been very few reports of distal tumor infiltration extending <3 cm (5). From a clinical perspective, a DRM of 3 cm is generally considered a safe resection margin for patients with rectal cancer. A previous metabolomic study by Zhang et al (18) may support the finding of the present study, which also suggests that a DRM of 2 cm may be considered as a safe resection margin. With the advancement of medical technology, the length of DRM in rectal cancer surgery has been progressively reduced. Manegold et al (31) reported that R0 resection of rectal cancer following preoperative chemoradiotherapy achieved excellent outcomes, even with DRM <1 cm, without impacting recurrence-free survival of patients. However, a meta-analysis reported that for patients with rectal cancer undergoing surgery alone, DRM <1 cm may not be deemed safe (32).
In addition, the results of the present further indicated that the ADCs at the maximum b-values of ≥800 sec/mm2 exhibited a certain diagnostic value in discriminating between D1 and D2/D3 (AUCs, 0.617 to 0.692). The ADCs at b-values of 0 and 800 sec/mm2 or b-values of 0 and 1,000 sec/mm2 demonstrated improved diagnostic performance in differentiating between D1 and D2 (AUC, 0.652 or 0.651), and the ADC at b-values of 0 and 1,000 sec/mm2 exhibited optimal diagnostic performance in differentiating between D1 and D3 (AUC, 0.692). Although ADC could not achieve an excellent diagnostic performance in distinguishing between D1 and D2/D3, it may still have clinical importance for preoperative surgical decision-making in resectable mid-high RA.
The present study has several limitations. Firstly, it was a single-center retrospective study, and a prospective study across multiple institutions and scanners is needed to validate the findings. Secondly, patients with RA who had not undergone preoperative chemoradiotherapy were assessed, and further studies are needed for patients who have undergone this therapy. Thirdly, the results of the present investigation on distal paracancerous tissues located at several distances from the tumor margin has not been verified by comprehensive comparison with the corresponding histopathology and molecular alterations of these tissues. Relevant research should be performed in the future to support the findings of the present study.
In conclusion, the results of the present study demonstrated that there were differences in ADCs between RA, D1 and D2/D3, and ADC could distinguish RA from D1, D2 and D3, and differentiate D1 from D2/D3 to a certain degree. However, no significant differences were demonstrated in ADCs between D2 and D3, indicating that they may possess similar biological characteristics and that the safe DRM in RA surgery may be reduced to 2 cm. The findings suggest that ADC may potentially serve as a valuable tool for evaluating the optimal distal resection range, contributing to the development of surgical strategies to reduce the risk of local recurrence and postoperative complications.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
The data generated in the present study may be requested from the corresponding author.
Authors' contributions
TWC, HYZ, XMZ participated in the design of the study. HL, YQG, YSW and HLQ contributed to data analysis. TWC, HL and YQG drafted and revised the article, gave final approval of the version to be published, agreed to the submitted journal and agreed to be accountable for all aspects of the work. TWC, HL and YQG proofread the manuscript. TWC submitted the manuscript. All authors have read and approved the final version of the manuscript. TWC and HL confirm the authenticity of all the raw data.
Ethics approval and consent to participate
The present study was approved by the Ethical Committee of the Affiliated Hospital of North Sichuan Medical College (Nanchong, China; approval no. 2024ER219-1). The ethics committee waived the need for informed consent due to the retrospective nature of the present study.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Glossary
Abbreviations
Abbreviations:
|
ADC |
apparent diffusion coefficient |
|
DWI |
diffusion-weighted imaging |
|
MRI |
magnetic resonance imaging |
|
T2W |
T2-weighted |
|
RA |
rectal adenocarcinoma |
|
D1 |
distal paracancerous tissue located ~1 cm from the tumor margin |
|
D2 |
distal paracancerous tissue located ~2 cm from the tumor margin |
|
D3 |
distal paracancerous tissue located ~3 cm from the tumor margin |
|
DRM |
distal resection margin |
|
DTM |
distal tumor margin |
|
ROI |
region of interest |
|
ICC |
intraclass correlation coefficient |
|
ROC |
receiver operating characteristic |
|
AUC |
area under the receiver operating characteristic curve |
|
pT |
pathological tumor stage |
|
pN |
pathological lymph node stage |
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