The forgotten nodes: a narrative review

Introduction

The literature indicates that up to 50% patients operated for cure of colon cancer can develop systemic recurrence (1). Today, surgical options for ablation of liver and/or lung metastases are standard care in combination with other treatment modalities (chemo, biologic). On the other hand, loco-regional recurrence develops in 4–11.5% of patients (1,2). Depending on localization and nature of locoregional recurrence, it can be classified into four groups, namely, mesenteric (nodal), anastomotic, peritoneal and retroperitoneal (3). The same surgical options in combination with oncologic treatment are available for these patients. A single patient can develop loco-regional recurrence only or in conjunction with systemic, or only systemic. Up to date, it is hard to draw clear border between the two.

Complete mesocolic excision (CME), in the surgical treatment of colon cancer, has highlighted the concept of simultaneously removing complete and uninjured colic artery lympho-vascular bundles, in this manner preventing seeding of cancer cells at surgery (4). Our research team has analyzed these lympho-vascular bundles in detail, and defined lymphatic clearances of colic arteries as have been measured to 2.8–6.3 mm (5,6). These data have given rise to the definition of the level of dissection III (D3) volume of the right colon, later also postulated that this D3 volume is shared with the small bowel. This definition allows not only the standardization of lymph node harvest after surgery, but also for the accurate positioning of lymph nodes found on the staging computed tomography (CT) (7,8). Almost simultaneously, a call for the redefinition of lymph node stations according to fixed anatomical landmarks was made by Gundara et al. in 2013 (9). The curative potential of extended mesenterectomy has not been comprehensively evaluated from the aspect of evidence-based medicine until our recent study (10).

The objective is to present a patient that developed nodal recurrence in the D3 volume 3 years after initial right colectomy for cancer, present the preparations before surgery, the surgical principle of complete D3 volume removal in order to achieve R0 resection, a comprehensive video is attached. A brief overview of the literature is presented and discussed. We present this article in accordance with the Narrative Review reporting checklist (available at https://ales.amegroups.com/article/view/10.21037/ales-24-23/rc).

Methods

The literature review

The search strategy consisted in locating previously published studies (Table 1).

A preliminary search of MEDLINE through PubMed was made in order to identify articles focusing on our research interest. The key words in relevant articles or abstracts, and the indexed terms used to describe the articles were used to develop a full search strategy. The databases used to identify the studies were PubMed, the Cochrane Central Register of Controlled Trials and Embase. The complete research algorithm included: [(colorectal cancer) OR (colorectal carcinoma) OR (colon cancer) OR (colon neoplasm)] AND [“lymph node recurrence”]. The time frame was confined to 2005, and older publications were not considered. Duplicates were removed, as well as articles on recurrences not deemed as local, case reports, and articles on local recurrences of cancers not arising from the right colon, as shown in the flow chart (Figure 1). Articles published after 2005 in which it was clearly stated that the patients analyzed were operated in the 80s or 90s were also disregarded as well as articled that did not stratify patients by tumor location. Titles and abstracts were screened for selection by two authors (BVS and DI). The full texts of selected citations were then retrieved and assessed in detail to the inclusion criteria by the same two reviewers.

Figure 1 Flow chart for the literature review.

The search provided 15 articles that contain data on local recurrence after surgery for right sided colon cancer, and a comprehensive analysis of these is given in the discussion.

Patient history

An 86-year-old lady was referred to the Department of Digestive Surgery, Akershus University Hospital in March 2020 due to the find of a large lymph node in the central mesentery.

Her medical history included surgery for breast cancer 2014, atrial fibrillation (anticoagulation drug therapy), ischemic stroke with easy sequelae, type 2 diabetes, Graves’ disease, hypertension, asthma. She had undergone an appendectomy as a child.

She was diagnosed with a right flexure colon cancer in 2017. The standard preoperative work up in Norway consists of a thoracoabdominal CT, colonoscopy with biopsy and blood analyses. A stage III colon cancer was diagnosed and the patient was referred to surgery, with the recommendation to have both ovaries removed during the same procedure. Preoperative carcinoembryonic antigen (CEA) was 19 ng/mL.

The initial surgical procedure was described as challenging due to numerous adhesions that required time to be divided, but resulted in a right colectomy with intracorporeal anastomosis, yielding a bulky specimen. Vascular ligation was described as “central”. The specimen was removed through a lower midline mini-laparotomy. The bilateral oophorectomy was subsequently performed by the gynecology team. The postoperative period was uneventful and the patient was discharged. The only complaint that the patient had after the surgery was 4–5 loose stools daily.

The histopathology report described a right colonic flexure adenocarcinoma with moderate differentiation and infiltration into the pericolic tissue. The proximal and distal resection margins were characterized as free. There was no vascular or perineural infiltration. A total of 31 lymph nodes was harvested, two of which were metastatic nodes. Microsatellite instability was not tested at the time of the initial surgery. The tumor was classified as pT3N1b. Histopathology of the gynecologic specimen was benign.

The patient was referred to the oncologist, thereafter receiving 12 FLV (folinic acid, fluorouracil, vincristine) treatments (5FU 950 mg, calcium folinate 100 mg).

She underwent follow-up for 2 years without positive find on thoracoabdominal CT; during these two years the CEA value was sequentially: 5.8, 7.1, and 8.0 ng/mL.

A third CT in February 2020 (3rd CT) diagnosed an enlarged lymph node anterior to the superior mesenteric artery (SMA), 10 cm distal to its origin from the aorta (Figure 2). The short axis of the node was 13 mm. It was thereafter found retrospectively on the preceding CT scan when its short axis was measured to 6 mm. There were no other signs of disease dissemination. The thoracic CT was negative. Further, a whole body FDG PET scan (fludeoxyglucose-18 positron emission tomography) scan was carried out and showed a very high uptake of FDG (18 mm × 13 mm × 15 mm) anterior to the SMA at the level of the L2-3 vertebra, possibly representing a lymph node metastasis. Colonoscopy was performed visualizing a patent anastomosis without any sign of recurrence. The patient was discussed on the multi-disciplinary meeting and then referred to surgery. She signed the written consent form for the “Safe D3 right hemicolectomy for cancer through multidetector computed tomography (MDCT) angiography” trial (regional Ethical Committee approval REK Sør-Øst No. 2010/3354) and registered at clinicaltrials.gov (NCT01351714). The preoperative CT dataset (0.5 mm slice) was then anonymized and sent to the University of Geneva via a secure FTP server for the 3D reconstruction of the mesenteric anatomy.

Figure 2 3D reconstruction of the vascular anatomy. LyNo, lymph node; IMV, inferior mesenteric vein; access MCA, accessory middle colic artery; GTH, gastro-colic trunk of Henle; MCA stump, middle colic artery stump; JV, jejunal vein.

Definitions/investigations

The D3 volume: the D3 volume is defined through four lines connecting arterial origins and venous confluences. The first line lies 1 cm parallel and distal to the line connecting the ileo-colic artery (ICA) origin to the ileo-colic vein (ICV) confluence. The second line runs along the left-hand side of the SMA. The third line lies 5 mm parallel and cranial to the line connecting the origin of the middle colic artery (MCA) to the confluence of the gastro-colic trunk of Henle (GTH). The last line lies 1 cm parallel to the right of the superior mesenteric vein (SMV) right border. The D3 volume encompasses all tissue anterior to the superior mesenteric vessels and posterior to the SMV defined through these four lines (5,6).

The 3D vascular anatomy reconstruction: the identification, caliber (internal diameter) and course of the vascular structures within the root of the mesentery were analyzed according to the previously published detailed articles (11). The CT data set was analyzed using a 2D multiplanar reconstruction with a maximum intensity projection and a 3D volume-rendering technique using the Food and Drug Administration (FDA)-approved OSIRIX MD v.14.0 64-bit image-processing application, software (Pixmeo, Bernex, Switzerland). The root of the mesentery and adjacent structures were precisely depicted by means of the manual segmentation by serial application of region of interest (ROI) through editing tools: Open polygon, Pencil, and Repulsor. After attributing pixel values outside ROIs to air, the virtual 3D model was obtained by volume rendering (VR). The identification, caliber and course of the vascular structures within the root of the mesentery were defined and analyzed in accordance with the postulates for CT angiography of mesenteric vessels. The dataset was additionally analyzed by manual segmentation using the Mimics medical image processing software ver. 24.0, and 3-matic medical software, ver. 16.0 (both for Windows 10 Pro x64, Materialise NV, Leuven, Belgium). The tools used were Profile line thresholding, Single and Multiple slab editing with interpolation, Dynamic region growing, 3D Interpolate, and Boolean operations, resulting in a 3D object mask for the superior mesenteric vessels and other arteries and veins. The data were exported as images and video clips, the latter with a 180° rotation in vertical and horizontal planes.

The vascular anatomy description (Figure 3): the 3D vascular anatomy reconstruction anatomy presented the following data. The ICA stump crossed the SMV dorsally, 1.1 cm long, caliber 0.3 cm. The distance from the ICA origin to the MCA origin was 1.8 cm. The MCA stump crossed the SMV anteriorly disappearing behind the enlarged lymph node (1.96 cm × 0.98 cm). The MCA stump length was 1.65 cm and its caliber 0.3 cm. The level of the MCA origin was 2.02 cm distal to the level of the GTH confluence. A large jejunal vein (caliber 0.94 cm) crossed the SMA posteriorly, just cranial to the MCA origin. A large ileal vein crossed the SMA anteriorly, approximately 1 cm distal to the ICA origin, depicting the lower border of the D3 volume (Figure 3).

Figure 3 Preoperative CT image presenting the nodal recurrence. LyNo, lymph node; SMV, superior mesenteric vein; SMA, superior mesenteric artery; JV, jejunal vein; CT, computed tomography.

The operative plan: minimally invasive surgery using the Da Vinci robot. The anatomy was deemed favorable, as there was no large jejunal vein crossing the SMA (D3 volume) anteriorly in the dissection area, and the distance between the ICA and MCA origins was small. The stump of the MCA was to be removed in order to secure access to the SMV posterior to the lymph node.

The operative setup: pneumoperitoneum was created with direct placement of a visual 15 mm trocar in the left subcostal region laterally, this is the position of the assistant. Thereafter under visual control four 8 mm ports were introduced in the lower abdomen in a semilunar fashion. The robot was docked on the right side of the patient. Controls were with 2 instruments to the left. A Cadière forceps/grasper was positioned laterally and a Maryland bipolar forceps, camera and monopolar scissors medially.

The surgery prep/operative plan and setup (Video 1)

After the initial division of adhesions and orientation a horizontal incision is made in the mesentery in order to identify the distal segment of the SMV (the terminal ileal venous trunk). The incision was then widened towards the patients right in order to include the remaining colonic mesentery after the previous right colectomy. As the dissection continues cranially, the ileal vein confluence is visualized, thus depicting the distal edge of the D3 volume. Once this landmark has been identified, a longitudinal incision is made in the mesentery along the left-hand side of the SMA. This segment of the dissection is simplified through the fact that the preoperative reconstruction of the anatomy shows no large jejunal veins anterior to the SMA. Dissection continues proximally within the vascular sheath of the SMV and SMA. A vessel loop is placed around the SMV so that it can be utilized to manipulate the vessel in case such need arises. Dissection continues until the MCA origin is detected, and the artery divided after clipping it. The dissection then proceeds towards the SMV where two middle colic veins are found and clipped (Figure 4). The specimen is freed in the pancreatic notch and removed in total via a specimen bag, through the assistant’s port. Control of hemostasis. The patient was put on a three-day low-fat diet in order to prevent the development of chylous ascites. Leakage of chylous ascites is regularly noted during the surgery, and a postoperative 3-day diet is proved effective in preventing chylous ascites in similar patients (12).

Figure 4 Final view of the dissection area. (a) Superior mesenteric vein; (b) superior mesenteric artery; (c) the two middle colic veins clipped.

Histopathology

The specimen measured 6.0 cm × 3.0 cm × 2.5 cm. In the middle of the specimen a lymph node conglomerate was discovered by cutting through it. It was not possible to determine the number of lymph nodes within this conglomerate. The histopathology revealed an adenocarcinoma with vascular and perineural infiltration, and necrosis, in contrast to that of the first surgery where no vascular or perineural infiltration was found. The remaining four lymph nodes found did not contain metastases. The microsatellite instability (MSI) status was re-analyzed at a later point, showing a negative find.

The patient was discharged from the hospital on the second post-operative day. The case was discussed on the multidisciplinary meeting after the histology report where it was decided not to offer additional therapy. She is now alive without recurrence at 7 years after primary right colectomy and 4 years after redo lymphadenectomy.

Discussion

What is distinctive in this case is that the complete D3 volume of the right colon was removed through robotic access, following a previous right colectomy for cancer. The specimen was placed in glacial acetic acid and delivered to the pathology lab. Specimen size measured after the procedure (and after shrinking in glacial acetic acid) measured 6.0 cm × 3.0 cm × 2.5 cm. Shrinkage after fixation differs according to the tissue but is usually considered to be 14% (13) making the fresh specimen 7.2 cm × 2.85 cm, which correlates well with the measured size of the D3 volume (6). Another point of interest is the case that the patient did not receive chemotherapy after the surgery for nodal recurrence, while she did receive it after primary surgery. The most interesting issues are considered below.

The first point of discussion is the incidence of nodal recurrence after surgery for colon cancer. The literature does not contain many articles that address this specific point, most articles set the various modes of local recurrence together and on occasion report on subgroups (14-16). Local recurrence rates after right colectomy are reported up to 10%, while residual lymph node metastases between 0.3–0.8% (17,18). On the other hand, a recent study has reported on the incidence of retroperitoneal node recurrence in 2–6% (19). It is highly possible that nodal metastases are often synchronous with other modalities of local and/or systemic recurrence (e.g. carcinomatosis) and are therefore under-reported (3,15). On the other hand, defining nodal recurrence as mesenteric and retroperitoneal does not seem to be precise enough. Based on our anatomical and clinical studies we strongly believe that nodal recurrence should be described according to anatomical landmarks, namely level of dissection 3 (D3 volume), level of dissection 2 nodes. Moreover, our group has demonstrated lymph nodes posterior to the superior mesenteric vessels that can easily be confused with preaortic nodes due to the topography of the SMA and the aorta. It is possible that such nodes should be considered as local (D3 volume) due to their topography (anterior to the aorta and posterior to the superior mesenteric vessels) and should be treated as local metastases. A third group of nodes are extra-anatomical nodes, occurring in other segments of the mesentery (i.e., small bowel mesentery).

A second point that needs to be addressed is the extent of the redo surgery. Should the goal be removal of a single lymph node or should a wider anatomically predefined volume be removed? If the answer is the latter, then this volume should be linked to the primary tumor feeding artery, in our case the MCA. Isolated cancer cells and micro-metastases have been found in macroscopically unaffected central lymph nodes (20,21); further, established metastases that measure less than the radiologist’s threshold (5 mm) were also found. It is possible that if this approach is chosen R0 resection can be achieved with fewer local re-recurrences (10,22,23). A recent publication by Banipal et al. have analyzed 42 patients with lymph node metastases in the D3 volume at primary surgery. The procedure performed was D3 right colectomy with extended mesenterectomy anterior/posterior to the mesenteric vessels. The patients were classified into two groups at histopathology, namely 29 patients with R0 and 13 patients in the R1/2 resection. The former group had as projected 5-year survival rate of 73% while the latter had only one patient (MSI+, treated with immunotherapy) that survived (10).

The least problematic subject to discuss is the vascular anatomy. The central mesentery represents a surgical minefield where multiple arteries originate from both sides of the SMA. These branches cross the SMV and its branches, including frequent variants and malformations. The 3D vascular reconstruction defines the lymphadenectomy, in the same time providing the solution when complications occur, shortens operating time and minimizes bleeding (24,25).

Mode of access is at the surgeon’s preference. While mesenteric surgery can be performed through laparotomy or laparoscopy, we prefer robotic access due to the stability of the platform, the superior vision, magnification and the dexterity of the instrumentation. Monopolar scissors are preferred for dissection, especially within the arterial sheath of the SMA (26).

Lymph node metastases in central (D3 volume) lymph nodes at primary surgery or as local recurrence are often categorized as systemic disease both by surgeons and oncologists. As this patient did not receive chemotherapy after the redo surgery and is alive and tumor free seven years after primary and four years after the redo surgery it seems safe to say that this was not the case in our patient. The fact that she received 12 FLV treatments after primary surgery can be linked to the type of chemotherapy since the treatment of patients under 70 is routinely XELOX (6 cycles of capecitabine plus oxaliplatin) or XELOX/ FOLFOX/FLOX (12 cycles of capecitabine or 5-fluorouracil and oxaliplatin) and is not prescribed to patients older than 75 years in Norway (24). It has been shown that chemotherapy often delays the onset of recurrence rather than preventing it (23).

While Metcalfe et al. report overall local recurrence in 10.5%, they find nodal recurrence in 24 (3.5%) of 689 patients, while an additional 1.6% (11 pts) had local recurrence including nodal recurrence (27). Chesney et al. report nodal recurrence in 16 (14%) patients, and multiple sites in 15 (13%) of 117 patients (28). Harji et al. report 2 patients of 42 with nodal recurrence (29). Other authors report on anastomotic recurrence, peritoneal and pelvic, not mentioning nodal recurrence (30). Wisselink et al. report the on the changed pattern of local recurrence in the three recent studies from 4.4% to 6.7% (31-33) when compared to the earlier studies (3.1% to 19.0%), in this manner suggesting a significantly lower local recurrence rate after the implementation of CME. They also report that median time of local recurrence diagnosis is 19 months after surgery (34). Struys et al. (35) conducted a systematic review of the literature and found that the median overall recurrence rate was lower in the CME/D3 group (14%) when compared to that in the standard/D2 group (19%). However, there was no significance in the difference of nodal recurrence (1.7% in the CME/D3 group, and 1.2% in the standard/D2 group). The median incidence of locoregional, preventable lymph node recurrence was 0% in the CME/D3 group and 0.4% in the standard/D2 group (35). A recent population-based study from the Netherlands provides a 5-year cumulative incidence of locoregional recurrent disease only as 2.4% in patients with primary colon cancer, not providing further stratification (36). Cho et al. report a locoregional recurrence rate of 4.4%, mostly diagnosed in the anastomosis, not mentioning nodal recurrence (37).

The limitations faced were the small number of recovered pertinent articles for the issue of nodal recurrence. This limitation is due to the requirement to assess the current occurrence of nodal recurrence, namely after the introduction of the CME/D3 surgical techniques.

Conclusions

The incidence of local nodal recurrence seems to be significantly lower than in the time prior to the introduction of CME/D3 surgical technique. Nevertheless, there seems to be room for further improvement. We present a surgical technique of D3 extended mesenterectomy as an option for the treatment of nodal recurrence in the central (D3 volume) lymph nodes after right colectomy for cancer through minimally invasive access (robotic) surgery.

Acknowledgments

Special thanks to Kosta Ignjatovic for composing the original background music of the video “The Forgotten Nodes”.

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://ales.amegroups.com/article/view/10.21037/ales-24-23/rc

Peer Review File: Available at https://ales.amegroups.com/article/view/10.21037/ales-24-23/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://ales.amegroups.com/article/view/10.21037/ales-24-23/coif). R.B. serves as an unpaid editorial board member of Annals of Laparoscopic and Endoscopic Surgery from February 2023 to January 2025. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All clinical procedures described in this study were performed in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for the publication of this article, and accompanying images and video.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Brown KGM, Koh CE. Surgical management of recurrent colon cancer. J Gastrointest Oncol 2020;11:513-25. [Crossref] [PubMed]
2. Sjövall A, Granath F, Cedermark B, et al. Loco-regional recurrence from colon cancer: a population-based study. Ann Surg Oncol 2007;14:432-40. [Crossref] [PubMed]
3. Bowne WB, Lee B, Wong WD, et al. Operative salvage for locoregional recurrent colon cancer after curative resection: an analysis of 100 cases. Dis Colon Rectum 2005;48:897-909. [Crossref] [PubMed]
4. Hohenberger W, Weber K, Matzel K, et al. Standardized surgery for colonic cancer: complete mesocolic excision and central ligation--technical notes and outcome. Colorectal Dis 2009;11:354-64; discussion 364-5. [Crossref] [PubMed]
5. Nesgaard JM, Stimec BV, Soulie P, et al. Defining minimal clearances for adequate lymphatic resection relevant to right colectomy for cancer: a post-mortem study. Surg Endosc 2018;32:3806-12. [Crossref] [PubMed]
6. Spasojevic M, Stimec BV, Dyrbekk AP, et al. Lymph node distribution in the d3 area of the right mesocolon: implications for an anatomically correct cancer resection. A postmortem study. Dis Colon Rectum 2013;56:1381-7. [Crossref] [PubMed]
7. Nesgaar JM, Stimec BV, Bakka AO, et al. Right Colectomy with Extended D3 Mesenterectomy: Anterior and Posterior to the Mesenteric Vessels. Surg Technol Int 2019;35:138-42. [PubMed]
8. Gaupset R, Nesgaard JM, Kazaryan AM, et al. Introducing Anatomically Correct CT-Guided Laparoscopic Right Colectomy with D3 Anterior Posterior Extended Mesenterectomy: Initial Experience and Technical Pitfalls. J Laparoendosc Adv Surg Tech A 2018;28:1174-82. [Crossref] [PubMed]
9. Gundara JS, Gill AJ, Hugh TJ, et al. Redefining the apical lymph node at right hemicolectomy. Eur J Surg Oncol 2013;39:662-5. [Crossref] [PubMed]
10. Banipal GS, Stimec BV, Andersen SN, et al. Are Metastatic Central Lymph Nodes (D3 volume) in right-sided Colon Cancer a Sign of Systemic Disease? A sub-group Analysis of an Ongoing Multicenter Trial. Ann Surg 2024;279:648-56. [PubMed]
11. Nesgaard JM, Stimec BV, Bakka AO, et al. Navigating the mesentery: a comparative pre- and per-operative visualization of the vascular anatomy. Colorectal Dis 2015;17:810-8. [Crossref] [PubMed]
12. Agustsdottir EES, Stimec BV, Stroemmen TT, et al. Preventing chylous ascites after right hemicolectomy with D3 extended mesenterectomy. Langenbecks Arch Surg 2020;405:1017-24. [Crossref] [PubMed]
13. Shin J, Shin S, Lee JH, et al. Lymph node size and its association with nodal metastasis in ductal adenocarcinoma of the pancreas. J Pathol Transl Med 2020;54:387-95. [Crossref] [PubMed]
14. Goldberg RM, Fleming TR, Tangen CM, et al. Surgery for recurrent colon cancer: strategies for identifying resectable recurrence and success rates after resection. Eastern Cooperative Oncology Group, the North Central Cancer Treatment Group, and the Southwest Oncology Group. Ann Intern Med 1998;129:27-35. [Crossref] [PubMed]
15. Taylor WE, Donohue JH, Gunderson LL, et al. The Mayo Clinic experience with multimodality treatment of locally advanced or recurrent colon cancer. Ann Surg Oncol 2002;9:177-85. [Crossref] [PubMed]
16. Akiyoshi T, Fujimoto Y, Konishi T, et al. Prognostic factors for survival after salvage surgery for locoregional recurrence of colon cancer. Am J Surg 2011;201:726-33. [Crossref] [PubMed]
17. Kishiki T, Kuchta K, Matsuoka H, et al. The impact of tumor location on the biological and oncological differences of colon cancer: Multi-institutional propensity score-matched study. Am J Surg 2019;217:46-52. [Crossref] [PubMed]
18. Augestad KM, Bakaki PM, Rose J, et al. Metastatic spread pattern after curative colorectal cancer surgery. A retrospective, longitudinal analysis. Cancer Epidemiol 2015;39:734-44. [Crossref] [PubMed]
19. Zarzavadjian Le Bian A, Genser L, Tabchouri N, et al. Abdominal lymph node recurrence from colorectal cancer: Resection should be considered as a curative treatment in patients with controlled disease. Surg Oncol 2020;35:206-10. [Crossref] [PubMed]
20. Banipal GS, Stimec BV, Andersen SN, et al. Interactions of occult tumor spread and surgical technique on overall and disease-free survival in patients operated for stage I and II right-sided colon cancer. J Cancer Res Clin Oncol 2021;147:3535-43. [Crossref] [PubMed]
21. Banipal GS, Stimec BV, Andersen SN, et al. Comparing 5-Year Survival Rates Before and After Re-stratification of Stage I-III Right-Sided Colon Cancer Patients by Establishing the Presence/Absence of Occult Tumor Cells and Lymph Node Metastases in the Different Levels of Surgical Dissection. J Gastrointest Surg 2022;26:2201-11. [Crossref] [PubMed]
22. Malik YG, Lyckander LG, Lindstrøm JC, et al. Stratification of Stage III colon cancer may identify a patient group not requiring adjuvant chemotherapy. J Cancer Res Clin Oncol 2021;147:61-71. [Crossref] [PubMed]
23. Moen TM, Stimec B, Ignjatovic D. The Use of a Vascular Roadmap at Surgery Evens out Surgeons Expectations on Operating Time, Blood Loss, Lymph Nodes Harvest and Operative Difficulty when Performing Right Colectomy with Extended D3 Mesenterectomy. Chirurgia (Bucur) 2022;117:579-84. [Crossref] [PubMed]
24. Willard CD, Kjaestad E, Stimec BV, et al. Preoperative anatomical road mapping reduces variability of operating time, estimated blood loss, and lymph node yield in right colectomy with extended D3 mesenterectomy for cancer. Int J Colorectal Dis 2019;34:151-60. [Crossref] [PubMed]
25. Gachabayov M, Lee H, Kajmolli A, et al. Impact of robotic total mesorectal excision upon pathology metrics in overweight males with low rectal cancer: a pooled analysis of 836 cases. Updates Surg 2024;76:505-12. [Crossref] [PubMed]
26. Helsedirektoratet (2019). 2020 (24.01): Norweigan guidelines for colorectal cancer. Available online: https://www.helsedirektoratet.no/retningslinjer/kreft-i-tykktarm-og-endetarm-handlingsprogram
27. Metcalfe KHM, Knight K, McIntosh S, et al. Disease recurrence after right hemicolectomy in Scotland: Is there rationale to adopt complete mesocolic excision (CME)? Surgeon 2022;20:301-8. [Crossref] [PubMed]
28. Chesney TR, Metz JJ, Nadler A, et al. Long-term outcomes of resection for locoregional recurrence of colon cancer: A retrospective descriptive cohort study. Eur J Surg Oncol 2021;47:2390-7. [Crossref] [PubMed]
29. Harji DP, Sagar PM, Boyle K, et al. Surgical resection of recurrent colonic cancer. Br J Surg 2013;100:950-8. [Crossref] [PubMed]
30. Jarrar A, Sheth R, Tiernan J, et al. Curative intent resection for loco-regionally recurrent colon cancer: Cleveland clinic experience. Am J Surg 2020;219:419-23. [Crossref] [PubMed]
31. Liska D, Stocchi L, Karagkounis G, et al. Incidence, Patterns, and Predictors of Locoregional Recurrence in Colon Cancer. Ann Surg Oncol 2017;24:1093-9. [Crossref] [PubMed]
32. Elferink MA, Visser O, Wiggers T, et al. Prognostic factors for locoregional recurrences in colon cancer. Ann Surg Oncol 2012;19:2203-11. [Crossref] [PubMed]
33. Park JH, Kim MJ, Park SC, et al. Difference in Time to Locoregional Recurrence Between Patients With Right-Sided and Left-Sided Colon Cancers. Dis Colon Rectum 2015;58:831-7. [Crossref] [PubMed]
34. Wisselink DD, Klaver CEL, Hompes R, et al. Curative-intent surgery for isolated locoregional recurrence of colon cancer: Review of the literature and institutional experience. Eur J Surg Oncol 2020;46:1673-82. [Crossref] [PubMed]
35. Struys M, Ceelen W. Incidence of lymph node recurrence after primary surgery for non-metastatic colon cancer: A systematic review. Eur J Surg Oncol 2022;48:1679-84. [Crossref] [PubMed]
36. Boute TC, Swartjes H, Greuter MJE, et al. Cumulative Incidence, Risk Factors, and Overall Survival of Disease Recurrence after Curative Resection of Stage II-III Colorectal Cancer: A Population-based Study. Cancer Res Commun 2024;4:607-16. [Crossref] [PubMed]
37. Cho MS, Baek SJ, Hur H, et al. Modified complete mesocolic excision with central vascular ligation for the treatment of right-sided colon cancer: long-term outcomes and prognostic factors. Ann Surg 2015;261:708-15. [Crossref] [PubMed]