D3 lymph node dissection in right-sided colon cancer: routine requirement or selective application?

Introduction

Colorectal cancer (CRC) remains one of the most common and lethal malignancies worldwide (1). While much of the progress in CRC treatment has focused on rectal cancer, the nuances of right-sided colon cancer (RCC) warrant renewed attention especially in the context of lymphadenectomy and surgical radicality (2,3). Complete mesocolic excision (CME) with D3 lymphadenectomy has emerged as a promising technique extensively described within Asian surgical guidelines (4). It is practiced mainly in Japan where it is the standard surgical approach for tumors that invade beyond the muscularis propria (cT2 or greater), or in cases where lymph node metastases (LNM) are suspected, aiming to maximize oncological clearance and survival outcomes (4). However, this approach is less commonly adopted in Western surgical practice due to differing surgical philosophies and concerns regarding procedural morbidity (5).

This editorial examines the historical foundation, current evidence, and future direction for selective adoption of D3 lymphadenectomy in RCC, advocating for a more tailored, evidence-based surgical approach.

CME concept and definitions

In 1986, the introduction of the total meso-rectal excision (TME) by Heald and colleagues revolutionized rectal cancer surgery (6). TME is defined as the removal of the rectum and mesorectum while remaining adherent to embryological planes and ensuring thorough lymphadenectomy of the adjacent lymphatic stations. As a result of this approach, overall survival and local recurrence rates saw significant improvement establishing TME as the current global gold standard in treatment of rectal cancer (7,8).

Translating this concept to colon cancer, Hohenberger et al. in 2009, described CME (9). They emphasized sharp dissection along embryological planes (the “layer”) to allow intact removal of mesocolic tissue within its the meso-colic envelope, ensuring adequate longitudinal resection (Figure 1) (9). Notably, Japanese surgeons had already been practicing similar techniques since the 1970s (10). However, its introduction to Europe was largely championed by West et al. (11) who demonstrated that specimen quality coupled with the integrity of the mesocolic fascia and subsequently the lymph node yield had a direct impact on long-term survival outcomes (12). Furthermore, multiple meta-analyses have demonstrated that CME significantly lowers the rates of local recurrence, with one analysis also indicating a reduction in distant metastases (13,14). Collectively, this growing body of evidence supports the consideration of routine CME in the surgical management of all but the earliest stages of colon cancer (NO DEBATE) (15). BIG DEBATE rather, is centered around the extent of lymphadenectomy (D2 or D3).

Figure 1 Terms and definitions for this article. CME—removal of the mesocolon within its anatomical envelope by dissection along the embryologic plane between the visceral and parietal fascia. D1 lymphadenectomy—removal of epicolic, paracolic and along the marginal artery lymph nodes. These represent the lymph nodes groups highlighted with red: 201, 211, 221, 231, 241, 251. D2 lymphadenectomy—D1 lymphadenectomy and also removal of intermediate groups of lymph nodes highlighted with blue in the picture: 202, 212, 222, 232, 242, 252. D3 lymphadenectomy—removal of all nodal tissue from anterior circumference of the superior mesenteric vein. For the right hemicolectomy this will comprise the group of lymph nodes highlighted in yellow: 203, 213 and partially 223. For the extended right hemicolectomy, the group 223 requires complete dissection and removal. While performing a left sided resection with D3 lymphadenectomy we need to all nodal tissue between the aorta and the left colic artery comprising the lymph nodes 253. CME, complete mesocolic excision.

Controversy around extent of lymphadenectomy is attributed to two interrelated factors: firstly, a lack of consensus surrounding the definitions of “D2”, “D3”, and “CME”, which undermines the consistency and comparability of surgical data; and secondly, the lack of a universally accepted protocol for CME with D2 or D3 lymphadenectomy, resulting in variable surgical techniques and oncological outcomes (16). In this editorial, D1, D2, and D3 lymph nodes correspond to: pericolic nodes-D1 (marked in red), intermediate nodes-D2 (marked in blue), and central-D3 (apical) nodes (marked in yellow) (Figure 1) (17).

Current evidence supporting potential oncological rationale of D3 lymphadenectomy

There is now increasing evidence to support the use of D3 lymphadenectomy, signifying a shift in the surgical landscape of RCC management (18-20). However, it is important to note that most of this data are in the form of retrospective studies and level 1 evidence remains lacking. While historical studies such as Kotake et al. questioned its benefit in pT2 tumors, these findings were based on open techniques and preceded the widespread adoption of minimally invasive surgery (13,21). In contrast, recent data highlight both the feasibility and oncological value of D3 dissection. For example, a large retrospective study by Wang et al. [2023] demonstrated that D3 lymphadenectomy was independently associated with improved overall and cancer-specific survival in pT2 CRC patients (22). Similarly, Yoon et al. [2023] reported favorable long-term outcomes in patients with stage II/III RCC undergoing D3 resection (23). These findings underscore a growing shift toward more extensive nodal clearance, supported by advances in surgical techniques coupled with a deeper understanding of lymphatic spread in colon cancer which are explored in subsequent sections. This is particularly pertinent given reported recurrence rates of 5% for even stage I colon cancer (24). The JSCCR guidelines recommend D3 dissection not only for confirmed nodal metastases but also when there is suspicion of involvement based on imaging or intraoperative findings (4). Even in cT2 tumors, where central positivity may be as low as 1%, this still supports consideration of D3 resection to avoid missed metastases (4).

High risk factors that might benefit from D3 lymphadenectomy

Curative intent surgery remains the cornerstone of managing CRC, particularly for patients with stage 1–3 disease with approximately 70% of colonic malignancy being routinely managed with surgical resection followed by an adjuvant chemotherapy regimen where indicated (25). Despite advances in surgical technique and adjuvant therapies, recurrence remains a significant challenge, occurring in up to 50% of patient’s post-curative surgery, either as locoregional or systemic disease (25,26).

The concepts outlined in sections below collectively underpin an increased recurrence risk, as well as decreased overall and disease-free survival, therefore, providing the underlying rationale for extended lymph node dissection.

Tumour deposits (TDs) & extramural venous invasion

TDs were first described in the early 20th century as discontinuous nodules of tumor in the pericolic fat. Only in recent decades, have they been increasingly recognized for their prognostic significance, distinct and independent from LNMs (27). Several retrospective studies and meta-analyses have reliably demonstrated their association with increased rates of local recurrence, distant metastasis, and poorer overall and disease-free survival (27-31). Although the origins of TDs remain unclear, it is believed that they are a continuation of vascular spread, representing metastases in transit (32). This is in keeping with their frequent association with extramural venous invasion (EMVI) which is a well-established independent prognostic marker for oncological outcomes (33,34).

In practice, the prognostic utility of both markers is limited due to their restricted incorporation in the current TNM classification: EMVI is not required for stage grouping but is acknowledged as a high-risk factor with indications for adjuvant treatment in node negative stage 2 disease. TDs fare worse- they are only incorporated in the N1c category which stipulates they should only be accounted for in the absence of LNMs (35). This contributes to under-reporting and an underestimation of their true prevalence (28,36). Identifying TDs and EMVI preoperatively on imaging could guide the surgical approach. In select patients, this may support the use of CME with D3 dissection to achieve (I) a comprehensive clearance of deposits and involved vascular structures; and (II) a reduction in tumor spillage in select cases, thereby improving oncological outcomes (37).

The COMET trial is a multicenter prospective study aiming to validate the use of CT and MRI to detect TDs preoperatively in CRC, as well as confirm the impact of TDs on long term prognosis (38). Notably, it’s protocol was updated to include colon cancers, a subgroup often neglected in prior imaging research when compared to its counterpart rectal cancers. It is also accepted from multiple previous studies that EMVI can be reliably recognized on preoperative CT with imaging being more sensitive than histopathology (39,40).

Nodal yield and the adequacy of lymphadenectomy

Lymph node yield and consequently the extent of lymph node dissection are well established factors influencing oncological outcomes in CRC (41-43). Chen et al. suggest that harvesting at least 15 lymph nodes is associated with a 20.6% reduction in mortality, with a reduction in recurrence across all stages, independent of tumour stage or patient demographics (44). Conversely, an inadequate nodal harvest can lead to under-staging allowing for microscopic residual disease to persist within the mesentery, increasing the risk of locoregional recurrence and resulting in neglected opportunities for adjuvant treatment, particularly in stage II disease, where occult nodal involvement may otherwise go undetected (44). In RCC specifically, Bertelsen et al. reported that the risk of central (D3) LNMs can range from 1% to 22%, with a higher prevalence noted in T3 and T4 tumors, particularly in stage III disease (36).

The survival benefits from increased lymph node yield, observed even in early-stage disease, likely reflects a combination of improved staging accuracy, removal of occult micro-metastases, and more complete oncological clearance (41-44).

In these settings there is good evidence supporting the oncological value of performing D3 lymphadenectomy. In the Wang et al. study of 616 patients with pT2 CRC, it was found that D3 lymphadenectomy significantly improved both overall survival [hazard ratio (HR) =3.3, P=0.024] and cancer-specific survival (HR =7.2, P=0.011) (22). Similarly, the Yoon et al. study evaluating 295 patients with clinical stage II/III RCC across three centres demonstrated significantly higher 5-year disease-free survival in the D3 group (90.2%) versus the D2 group (80.5%, P=0.028), with lower local recurrence (23). While the overall survival differences were not statistically significant, the consistent improvement in disease-free survival reinforce the concept that more extensive nodal clearance can improve oncologic outcomes, particularly where standard imaging underestimates disease burden or where residual disease is present (22,23).

Lymphatic drainage variations

Skip metastases and variations in vascular anatomy represent additional considerations supporting the rationale for D3. Skip metastasis is detected in up to 18% of patients with CRC (35). These are defined as involvement of intermediate (D2) or central (D3) nodes in the absence of D1 node positivity. This finding challenges the conventional model of sequential lymphatic spread and emphasizes the potential for under-staging if central nodal basins are not adequately assessed or removed during surgery (36).

Anatomical variation due to arterial supply, particularly in watershed areas of the ascending and transverse colon, is of interest (36). Metastases to gastrocolic and infra-pyloric lymph nodes were reported in up to 4% of patients with locally advanced disease at the hepatic flexure, indicating lymphatic connections to the greater omentum and pancreatic regions (36). To address this variability, preoperative imaging plays a crucial role. Recent meta-analysis suggests that preoperative navigation using CT reconstruction helps better delineate the complex vascular anatomy of the right colon (45) and improves the quality of lymph node dissection during laparoscopic or robotic procedures (46).

In the Wang et al. study, the benefit of D3 dissection was observed even in early-stage (pT2) cancers, suggesting that central LNMs or micro metastases may be present even in the absence of D1 involvement (22). Similarly, the Yoon et al. retrospective study demonstrated that performing central D3 lymphadenectomy using an anatomical approach that systematically addresses lymphatic variability resulted in lower disease recurrence rates and superior disease-free survival compared to D2 dissection (23). These findings may suggest that omitting the central nodal basin risks leaving behind occult disease, particularly in cases of atypical lymphatic drainage and skip metastasis (47).

Reported data on D3 lymphadenectomy

Recent data have demonstrated that D3 lymphadenectomy can be performed safely and reproducibly using minimally invasive approaches (20,48-50). For example, a meta-analysis by Balciscueta et al. demonstrates the technical reproducibility of D3 dissection, reporting significantly higher lymph node yields and improved mesocolic specimen quality, without an associated increase in perioperative morbidity (20). There is a glaring lack of level 1 evidence to support D3 lymphadenectomy and several prospective trials have now been initiated to further evaluate D3 lymphadenectomy, and a summary of these key studies (3,38,51-56) is presented in Table 1.

Challenges with D3 lymphadenectomy

While the authors believe that in selected cases CME with D3 lymphadenectomy may offer superior oncological outcomes compared to conventional resection, this is not without increased postoperative morbidity (3,20). Although most of the reported data do not show any significant morbidity rate, higher incidence of vascular injury has been reported (36). Freund et al. reported SMV injury rates of 1.6% when performing central ligation of originating vessels which can be attributed to factors such as anatomical variation, excessive traction of the SMV during dissection or if the SMV is misidentified as the middle colic vessels (57,58). While procedural morbidity exists, current evidence supports relatively low complication rates for CME with D3 lymphadenectomy when performed in experienced hands (20,48,49). Mazzarella et al. performed a systematic review of 5,931 CME procedures and found a pooled complication rate of 1.88% indicating a favorable safety profile for D3 dissection when conducted at high volume centers by skilled teams (48). These findings suggest that although there is a steep learning curve and technical challenges associated with D3 dissection, it can be safely executed where appropriate expertise is present. The adoption of robotic platforms may further enhance the feasibility and safety of D3 + CME. A recent meta-analysis demonstrated that robotic D3+CME is associated with low post op complications rates, minimal conversion to open rate, superior lymph node harvest and favorable overall survival and disease-free survival rates when compared to the laparoscopic approach (50).

Another commonly cited barrier to adopting D3 dissection in the west is the perception that outcomes from Asian cohorts are not generalizable due to differences in body habitus, however, the landmark study by Hohenberger (9) demonstrated early on that the differences in BMI between regions does not affect the feasibility of D3.

The routine justification of CME with D3 lymphadenectomy for every patient remains challenging due to the increased risk of major vascular injury and subsequent postoperative morbidity. While current data primarily indicates a higher lymph node yield as a main benefit, a direct link to improved oncological outcomes is not yet definitively established. This is largely because of the complex interplay of tumour characteristics and biology, individual immune responses, and the efficacy of neoadjuvant treatments are difficult to precisely predict or quantify in observational studies. Given the inherent risk of bias in existing data, large scale, randomized controlled trials are essential. These trials should rigorously assess the oncological feasibility of CME with D2/D3 lymphadenectomy.

Conclusions

CME represents a surgical philosophy grounded in embryological planes and anatomical precision. When combined with D3 lymphadenectomy, this technique offers the potential for enhanced oncological clearance in selected patient populations such as those with advanced stage tumors, EMVI, and TDs. However, routine application of D3 dissection across all colon cancers remains contentious. Importantly, when performed by trained surgeons using standardized protocols and preoperative vascular mapping, D3 dissection does not appear to increase perioperative morbidity. These findings highlight the need for widespread education, structured training, and consensus on standardized CME with D3 protocols to facilitate broader adoption.

Acknowledgments

None.

Footnote

Provenance and Peer Review: This article was commissioned by the editorial office, Journal of Gastrointestinal Oncology. The article has undergone external peer review.

Peer Review File: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-371/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2025-371/coif). The authors have no conflicts of interest to declare.

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