Extent of lymphadenectomy in small bowel neuroendocrine tumors: a scoping review of literature heterogeneity

Introduction

Background

Small bowel neuroendocrine tumors (NETs) have shown a steadily increasing incidence over recent decades, yet their management remains one of the least standardized areas of gastrointestinal surgery (1). Despite their indolent biology, these tumors display a tendency for early lymphatic dissemination, with lymph node (LN) metastases present in almost 90% of patients at diagnosis (2,3). The challenge of surgical treatment, therefore, lies not only in local control of the primary lesion but in achieving complete locoregional clearance of the malignant disease.

Rationale and knowledge gap

The lymphatic anatomy of the jejunum and ileum is uniquely rich, converging in a conical fashion toward the superior mesenteric artery (SMA) along their arterial counterparts (4-6). Late presentation, delayed diagnosis, and the aforementioned lymphatic architecture can explain the high frequency of mesenteric LN metastases. Anatomical studies demonstrate that complete nodal clearance often requires ligation of the small bowel tumor-feeding vessel at its origin with extension of the mesenterectomy both cranially and caudally along the tumor-feeding lymphovascular bundles, mirroring the principles of D2–D3 volume lymphadenectomy in colonic cancer surgery (7,8). Following this principle, understanding the complex lymphovascular anatomy of the small bowel is crucial, as it necessitates customized surgical approaches for different bowel segments, as reported in recent literature (4-6). In small bowel adenocarcinoma (SBA), large population-based datasets consistently show that survival correlates with the number of retrieved LNs and LN ratio, with at least eight nodes recommended for accurate staging, an approach mirrored in NETs, where official guidelines similarly endorse retrieval of ≥8 LNs (9-12).

Despite these data, current surgical practice remains highly heterogeneous. Many small bowel tumors are still treated in low-volume centers, often in emergency settings, with “pizza-pie” cone-shaped, wedge bowel resections that yield inadequate LN retrieval and compromise staging, locoregional control, and postoperative bowel length (13,14).

The literature shows significant variability in operative terminology and techniques. Some authors describe segmental small-bowel resection with lymphadenectomy; others mention central mesenteric dissection, reverse lymphadenectomy, or vessel-sparing resection, often referring to procedures that are conceptually similar but anatomically distinct (15-17). Only a few studies define lymphadenectomy using fixed vascular landmarks, such as the ileocolic artery (ICA) or the inferior pancreatic border (18,19). As a result, lymph-node yields reported range from 0 to over 70 nodes, reflecting technical differences rather than biological variation (20). Consequently, the existing literature is fragmented, with inconsistent operative techniques, lymphadenectomy extent, and reported numbers of harvested LNs, underscoring the need for a scoping review to map and contextualize this heterogeneity.

Objective

This review aims to critically evaluate the existing literature on the extent and reporting of lymphadenectomy in the surgical management of small bowel NETs and to descriptively summarize metadata on harvested lymph node yields (LNYs). Unlike prior literature that largely focuses on surgical indications or oncologic outcomes, this review specifically examines the anatomical extent, terminology, and reproducibility of lymphadenectomy across published surgical series (11,12,15,16). By highlighting substantial heterogeneity in operative terminology and technique, the review contextualizes prevailing surgical approaches and, based on available evidence and established anatomical principles, proposes a conceptual, framework for standardized reporting of lymphadenectomy extent, including D3-volume dissection, while explicitly acknowledging the need for prospective validation. We present this article in accordance with the PRISMA-ScR reporting checklist (available at https://ales.amegroups.com/article/view/10.21037/ales-2025-1-72/rc).

Methods

Information sources, search strategy and eligibility criteria

This scoping review was conducted to assess and evaluate the current literature on surgical techniques and the extent of lymphadenectomy in the treatment of patients with small bowel NETs. A comprehensive search of relevant studies, conducted from July 14 to July 20, 2025, was performed across major electronic databases, including PubMed, Scopus, Web of Science, and Embase, to identify articles published between January 1, 2005, and December 31^st, 2025. Only articles written in English and those relevant to the review’s objectives were included. Studies were selected based on their relevance and contribution to the understanding of the surgical management of small bowel NETs. Both clinical trials and retrospective cohort studies, as well as case series, were considered for inclusion. Records were screened for relevance based on their titles and abstracts, and subsequently, the full texts of the remaining articles were analyzed. Furthermore, the reference list of each selected article was analyzed to identify additional relevant studies. Articles were excluded if they lacked sufficient data or were not related to the specific focus of the review. The scoping review was conducted by T.V. and D.I. independently. When consensus was not obtained, B.V.S. resolved the disagreement. No formal review protocol was registered. A comprehensive summary of the electronic search strategy for PubMed/MEDLINE is provided in Table 1, and the flowchart of literature selection is provided in Figure 1.

Figure 1 Flowchart of literature selection.

Data charting

After the final screening, we extracted data from each study, including cohort size, tumor location and type, surgical techniques used [segmental bowel resection (SBR), right hemicolectomy, ileocecal resection (ICR)], extent of lymphadenectomy [lymph node dissection level (LNDL)], central vascular ligation (CVL), number of patients with positive LNs (Pts. LN+), number of patients with positive LNs in D1–D2 and D3–D4 volume separately (Pts.D1D2 LN+ and Pts. D3D4 LN+, definition for the D levels of dissection is given below), number of harvested LNs, and positive LNs to total LNs ratio, resection margin (R0), resected small bowel length, duration of surgery and oncologic outcomes [median overall survival (OS) and disease-free survival (DFS)]. Regarding tumor stage, when explicit ENETS/UICC/AJCC (12,21) stages were not reported, disease extent was reconstructed from reported TNM status, nodal involvement, and metastasis data, and harmonized into three categories: localized, regional, and distant disease. Data charting was performed independently by two reviewers using a predefined extraction form, with discrepancies resolved by consensus. No formal critical appraisal was performed, consistent with scoping review methodology.

Extent of lymphadenectomy

To evaluate consistency in operative technique terminology, all procedures and lymphadenectomies were gathered from the included literature and descriptively presented in Table 2 to gain insight into the terminology heterogeneity. Definitions of lymphadenectomy extent were assessed by two authors (D.I. and T.V.) and aligned, if applicable, with the Japanese LN dissection terminology, distinguishing between paraintestinal nodal clearance (D1), segmental-artery-oriented lymphadenectomy (D2), SMA/superior mesenteric vein (SMV) plane dissections (D3), and retropancreatic SMA lymphadenectomy (D4) (22). Hence, the D1–D4 classification was applied to enable a comparative description of lymphadenectomy extent; it is not a validated concept in small bowel surgery, such as in colorectal surgery. When studies described artery-oriented techniques, these were explicitly captured and reported. Additionally, if the data on harvested LNs were categorized by SMA root proximity, we identified which articles reported the number of LNs in levels D1/D2 and D3/D4, as well as the number of patients affected. If any authors provided a separate, unique classification of small bowel LNs, this was reported with a brief description of the author’s staging system.

Site of the tumor origin and bowel segments

VanDamme and Bonte note that the origin of the ICA represents an important anatomical transition point of the SMA: arteries originating cranially to the ICA origin are defined as jejunal arteries and supply the jejunum, whereas bowel arteries originating caudally to the ICA origin from the terminal part of the SMA are defined as ileal branches and provide the ileum (23). Notably, the most distal 30 cm of the ileum receives dual supply from the ileal branch of the ICA and the terminal ileal artery (TIA)/terminal SMA trunk. In addition, the region of the D3, D4 duodenum and proximal jejunum receives blood supply from the superior jejunal artery (commonly misnamed as the “first JA”) or the common inferior pancreaticoduodenal artery-jejunal artery (IPDA-JA) trunk. Based on these anatomical principles, we systematically recorded the anatomical location of each reported tumor using four standardized segments: distal duodenum/proximal jejunum, jejunum proper, ileum proper, and terminal ileum. During the final literature screening, studies involving distal duodenal tumors were excluded due to inconsistent reporting of the surgical procedures used for this bowel segment.

Statistical analysis and data synthesis

For each included study, data on the number of harvested LNs, small-bowel length, and operative time were extracted for pooling of the means when reported. Studies that did not provide analyzed parameters were excluded from quantitative pooling for the variable in question. When studies reported data as median with interquartile range (IQR) or range, the corresponding mean and standard deviation (SD) were estimated using the method described by Wan et al. (24). All calculations were performed in IBM SPSS Statistics (v.29), where mean values, SDs, and sample sizes were entered, and pooled means and SDs were obtained using the Aggregate and Compute functions, applying sample-size weighting to combine results from all studies reporting each variable. Quantitative data on the number of harvested LNs, length of the resected bowel, and operative time were reported descriptively for the scoping review, without performing a formal meta-analysis. These pooled values represent descriptively aggregated estimates derived from methodologically heterogeneous retrospective series and should not be interpreted as benchmarks, quality thresholds, or indicators of surgical adequacy.

Results

Of the 680 studies screened, 16 were included, comprising 2,103 patients (Table 3).

All studies exclusively investigated NETs, while SBAs were not represented in any cohort. Most studies were retrospective (15/16) and single-center (12/16); only two were multicentric (28,34) and one was prospective (27). The cohorts originated predominantly from European centers (14/16), with two North American registries. Study periods ranged from 2 to 27 years, reflecting heterogeneous inclusion windows and follow-up durations. The ENETS 2007 and AJCC 7th/8th staging systems were reported together in most series (9/16) (21). Several French and Italian groups instead classified disease morphologically or by SMA-based vascular extent (27,34,35). At diagnosis, the disease was localized in 8% (n=160), regional in 42% (n=783), and distant in 49% (n=993) of patients, indicating that approximately half presented with metastases.

Site of the tumor origin and bowel segments

Ten articles did not specify tumor location and included 1,552 patients (74%) (2,3,15,16,26,28,29,33-35). In 6 of 6 articles reporting tumor location, the ileum was identified as the site of origin in 93.7% (n=516) of patients with reported tumor location (n=551) (20,25,27,30-32). Two articles divided the ileum into the proximal (proper) ileum and the distal (terminal) ileum. The jejunum was reported as the site of tumor origin in 3 of 6 articles [5.4% (n=30) of 551 patients with reported tumor location] (25,30,31). One article divided the jejunum into the proximal and distal segments. Multiple SB tumors were identified in 21.9% (n=299) of patients with reported multifocality (n=1,368). None of the articles defined the anatomical boundaries of the small bowel segments or the tumor-feeding vessels of the affected segment, in accordance with the anatomical principles of Van Damme and Bonte. Data regarding the tumor origin site is presented in Table 3.

Survival outcomes

Survival outcomes were inconsistently reported across the 16 included studies (Table 4). Only four studies provided median DFS (20,25,30,31), while five reported 5-year OS (20,29-32). Several technically focused or registry-based analyses omitted survival curves or reported recurrence only descriptively (2,15,16,27,28,33,35). Median follow-up duration across studies ranged from 14 to 145 months, with considerable variation in censoring and definition of recurrence. Median DFS among curatively resected cohorts ranged from 88 to 138 months, with 5-year DFS ranging from 55% to 82%, depending on grading and follow-up duration. Five-year OS was uniformly high, typically 67–91%, and median OS was often not reached, reflecting the indolent course of well-differentiated midgut NETs. Pooling of mean survival values was not undertaken due to substantial heterogeneity in endpoint definitions [DFS vs. recurrence-free survival (RFS) vs. progression-free survival (PFS)], variable follow-up intervals, and differing study aims.

Evaluation of surgical techniques and lymphadenectomy extent

Across 16 studies, a total of 1,933 operated patients with small-bowel NETs were analyzed (Table 5). Segmental SBR was the most frequent procedure (493 cases, 25.5%), followed by right hemicolectomy (RC, 482 cases, 24.9%) and ICR (49 cases, 2.5%); 34 patients (1.8%) underwent palliative surgery, while the type of surgery was not reported for 822 (42.5%) patients.

The extent of lymphadenectomy was evaluated in 12 studies, most commonly D3 (15,26,29,31-35), while D4 dissections were identified in 3 (3,16,27), and one series reported a D2 dissection (30). In the remaining four studies, the operative descriptions were insufficient and did not permit classification according to the D-level system; therefore, the extent of lymphadenectomy could not be clearly defined (2,20,25,28). Three articles mentioned the concept of CVL of the tumor-feeding vessel (16,26,27).

Nodal metastases were present in 78.8% (n=1,523) of patients, 17.1% (n=330) were node-negative, and 4.1% (n=80) were unreported. Among those with nodal involvement, only a subset had clear allocation to D1–D2 (48.8%) or D3–D4 (49.7%) groups, while several series reported nodal positivity without specifying the anatomic dissection level. The pooled mean LNY was 13.7±6.1, with a lymph node ratio (LNR) ranging from 0.14 to 0.72. An R0 resection was achieved in 755 of 942 patients (80.2%) with available data. The pooled-mean resected bowel length was 70.6±55.6 cm, and the mean operative time was 203.8±106.2 minutes.

Description of the lymphonodal classification systems

We report three articles that explicitly classified the groups of LNs according to the anatomical levels:

• Pasquer et al., 2016 (Ann Surg Oncol)
  The LN groups were divided into three categories: group 1 along the small intestine, group 2 along the mesenteric vessels, and group 3 originating from the retropancreatic and mesenteric vessels. The concept of skip metastases was examined using the combined nodal involvement profiles of groups 1, 2, and 3 (27).
• Bartsch et al., 2022 (Cancers) (15)
  According to the modified Ohrvall classification, which the author uses (17), mesenteric LN involvement is divided into three anatomical levels:
  • Level 1 LNs: located from the small bowel wall up to the ICA origin
  • Level 2 LNs: extend from the ICA origin upward to the horizontal (third) portion of the duodenum and the inferior border of the pancreatic body, corresponding to intermediate central mesenteric metastases along the main SMA trunk
  • Level 3 LNs: lie between the horizontal duodenum/pancreatic border and the origin of the SMA at the aorta, representing the most central and cranial LNs; involvement at this level is generally considered unresectable due to SMA and first JA encasement.
• Lardière-Deguelte et al., 2016 (Neuroendocrinology) (34).
  • LN stage 0: no visible mesenteric LNs suspicious of malignancy.
  • LN stage I: proximity to the small intestine, without invasion of the SMA.
  • LN stage II: involvement of the distal branches of the SMA, next to their origin.
  • LN stage III: involvement of the trunk of the SMA, without involving the first jejunal arteries; III ‘up’: <3–4 free jejunal branches; III ‘down’: >3–4 free jejunal branches.
  • LN stage IV: involvement of the trunk of the SMA with involvement of the first JA.

Description of the techniques used for lymphadenectomy

Kaçmaz et al., 2021 (Diseases of the Colon & Rectum) (26)

The authors describe an open and laparoscopic technique centered on central mesenteric lymphadenectomy. A caudal-to-cranial dissection begins at the terminal ileum to mobilize the mesenteric root up to the duodenum and pancreas. Elevation of the transverse mesocolon exposes the SMA and SMV for identification of enlarged central mesenteric LNs. Segmental arterial and venous branches are ligated proximal to the LN, enabling en bloc mesenteric lymphadenectomy. Hereafter, the mesentery was additionally transected toward the proximal and distal sides of the primary tumor, thereby including all mesentery belonging to the involved small-bowel segment and visually or palpably enlarged nodes. For terminal-ileal tumors, central ligation of the ileocolic vessels and right hemicolectomy are performed.

Pasquer et al., 2015 & 2016 (Annals of Surgical Oncology) (16,27)

The authors from Lyon, France, describe a reverse lymphadenectomy technique focused on assessing and removing the central mesenteric LNs. After exposure of the mesenteric vessels, the retroperitoneum is opened, and a Kocher maneuver provides right-sided access to the proximal SMA, allowing safe CVL. Lymphadenectomy above the right colic vessels typically requires a right hemicolectomy. Dissection then proceeds along the left border of the SMA/SMV, preserving at least three jejunal branches. The devascularized bowel determines resection length, and lymphadenectomy is extended from the bowel margin to the central mesentery while preserving viable jejunal pedicles.

Norlén et al., 2012 (Annals of Surgical Oncology) (29)

The authors describe a centrally oriented mesenteric dissection based on the Uppsala (Öhrvall-Akerström) approach, emphasizing selective lymphadenectomy while preserving intestinal perfusion (17). After mobilizing the right colon, cecum, terminal ileum, and mesenteric root up to the horizontal duodenum and lower pancreatic border, the SMA and SMV are exposed beneath the pancreas and followed dorsally within the elevated mesentery. This allows careful dissection along the right side of the SMA, where nodal metastases frequently cluster, with sharp division of fibrotic adhesions and, when necessary, cleavage of the tumor from central vessels. Distal branches, such as the ICA, right colic, or ileal arteries, may be divided while preserving key arcades. Resection of the bowel is performed only after complete mobilization of the mesenteric mass, typically as a limited ileal resection or right hemicolectomy to preserve bowel length.

Watzka et al., 2016 (Surgery) (30)

The Mainz group describes a radical systematic mesenteric lymphadenectomy, as defined first by Musholt et al. (36). For terminal-ileal tumors, lymphadenectomy up to the ICA origin is commonly required, an ileocecal resection, or right hemicolectomy. For jejunal or mid-ileal lesions, small bowel wedge resection with mesenteric lymphadenectomy up to the feeding vessel of the jejunal or ileal tumor is performed, preserving the essential vascular arcades and bowel length.

Bartsch et al., 2022 (Cancers) (15)

The Marburg group describes a vessel-sparing lymphadenectomy beginning with exposure of the SMA and SMV through a ventral mesenteric root incision. Dissection starts at the inferior pancreatic border and proceeds by incising the peritoneum along the SMA. Retrograde dissection along the SMA and SMV toward the tumor is performed. The ICA/ICV and intestinal arcades are preserved to maintain perfusion. Bowel resection is delayed until the mesenteric tumor mass is fully mobilized, maximizing lymphatic clearance while preserving bowel length.

Lardière-Deguelte et al., 2016 (Neuroendocrinology) (34)

The authors from Reims, France, tailor surgical resection to the extent of mesenteric LN involvement. For LN stages 0, I, II, and III “down”, SBR is sufficient, with possible extension to the cecum or right colon when the terminal ileum is involved; in these stages, removal of at least eight LNs is recommended. In LN stage III “up”, where 3–4 free jejunal collaterals are identified, central lymphadenectomy may be attempted after intraoperative clamping tests, typically requiring ileal resection extending to a right hemicolectomy to maintain perfusion, and again aiming to clear ≥8 nodes. Patients with LN stage IV disease are considered unresectable due to proximal vascular involvement.

Discussion

Evidence synthesis versus expert interpretation

The following sections integrate findings from the reviewed literature with anatomical principles and surgical experience. Interpretative proposals should be understood as hypothesis-generating concepts rather than evidence-based recommendations.

Key findings and summary of evidence

The levels of LN dissection

The most important finding of this scoping review is that there is no standard surgical technique commonly used by surgeons to treat small bowel tumors. Among the 16 studies reviewed, there was significant variation in the scope of mesenteric lymphadenectomy, ranging from limited D2 dissections to more extensive D3/D4 lymphadenectomies. The D-classification system is more commonly used in gastric and colorectal cancer surgery, as it was developed by the Japanese Gastric Cancer Association and the Japanese Society for Cancer of the Colon and Rectum (22,37). Up to date, this concept is not recognized in small bowel tumor surgery. However, in theory, D1–D4 levels were created to describe LN removal along the arterial trunks, regardless of the organ operated on. In this review, most series described a D3-level dissection reaching the pancreas on the SMA axis, while only a few approached D4 level, removing retropancreatic lymph LNs around the SMA root (3,16). However, the number of harvested LNs ranged from 4 to 71, with a mean of 13.7±6.1, raising concerns about the reproducibility of the surgical procedure and the pathological analysis of the specimens. More importantly, studies that did not specify the dissection level may have performed extensive mesenterectomies, as indicated by the high number of harvested LNs. This is especially true for the articles by Le Roux and Cives, where the extent of lymphadenectomy could not be determined (20,25). On the contrary, in cases where a low number of harvested LNs was reported, patients may have undergone the so-called “pizza-pie” technique (D1 dissection), in which the mesentery is removed conically toward the bowel wall in the shape of a triangle/pizza slice. This oncologically inadequate method removes only peritumoral nodes while sacrificing unnecessary bowel length, without ligating the tumor-feeding artery and leaving the central lymphatic basin intact.

The proposal of the D3 volume

Although the term “mesenteric dissection” or “central lymphadenectomy” is often used to describe clearance along the SMA/SMV, nearly all series seem to confine the procedure to the plane anterior to the vessels. As demonstrated by Spasojevic et al., the true D3 region is a three-dimensional lymphovascular volume enveloping the SMA/SMV with anterior and posterior components (8). Nodes situated posterior to the SMA/SMV form a part of this same compartment. In addition, Nesgaard et al. confirmed the presence of longitudinal lymphatic channels running both anterior and posterior to the SMV toward the SMA (7). Quantitative evidence from right colon surgery supports this volumetric concept. Banipal et al. reported a mean of 14±7 LNs within the D3 compartment and ≈27±11 within D1/D2, totaling around 41 nodes per specimen, indicating that roughly one-third of all mesenteric nodes lie centrally (38). The percentage of patients with positive nodes in the D3–D4 region in the evaluated literature approaches nearly 50%. Thus, an oncologically complete D3 resection must include the removal of the full D3 volume. While ENETS guidelines recommend retrieval of at least eight LNs for adequate staging, findings from the reviewed literature indicate that a substantial proportion of metastatic nodes may be located in more central mesenteric compartments. In the absence of prospective comparative data or survival analyses stratified by true D3-volume clearance, this observation raises hypothesis-generating questions regarding the anatomical adequacy of current recommendations rather than implying guideline inadequacy (12,38).

The current problem of lymphadenectomy reproducibility

Current ENETS guidelines recommend “systematic or “central lymphadenectomy” with the preservation of bowel length (vessel-sparing surgery), yet the terminology “locoregional”, “extended”, “central”, or “adequate” lymphadenectomy remains descriptive rather than anatomical (11). It fails to specify vascular landmarks for dissection or to indicate whether all D3 volume LNs are included, making the recommendation difficult to reproduce and to compare across centers. Only a minority of authors provided broad descriptions based on fixed anatomical landmarks, referring occasionally to the ICA, SMA/SMV, middle colic artery (MCA), inferior pancreatic border, or jejunal and ileal arterial branches (15,16,26,27,29,30,34). In contrast, the volumetric D-classification of Spasojevic et al. and the vessel navigated surgery offer measurable, anatomically oriented criteria that could guide standardization of lymphadenectomy in future ENETS updates (4-6,8). An additional source of heterogeneity is the inconsistent distinction between LN metastases and mesenteric tumor deposits, which are increasingly recognized in small bowel NETs as discrete mesenteric tumor nodules lacking nodal architecture but are rarely reported separately in surgical or pathological series (39).

Navigating the tumor-feeding vessels

The concept of CVL was addressed only indirectly in three studies, and the tumor-feeding vessels were not anatomically defined. Bartsch et al. described a vessel-sparing lymphadenectomy designed to preserve bowel length, which, although physiologically beneficial, does not replicate the oncologic principle of CVL established in colorectal surgery (15). Similarly, Pasquer’s “reverse lymphadenectomy” is difficult to reproduce, as the technique is clearly explained as oriented to the tumor-feeding vessel (16). However, clear 3D-CT vascularly reconstructed anatomical landmarks are essential for identifying and navigating jejunal and ileal arterial or venous branches and their variations to avoid vascular injury and subsequent bleeding (40-42). Preoperative 3-D CT angiography can delineate the feeding vessel and guide a dissection beginning at the ICA origin, exposing the SMA and SMV, counting the jejunal vessels cranially (or ileal vessels caudally), ligating the tumor-feeder, and performing a D3-volume lymphadenectomy both anteriorly and posteriorly to the mesenteric axis.

Bowel length and number of harvested LNs

Japanese colorectal guidelines recommend a 10-cm longitudinal bowel resection from the tumor to adequately include the regional pericolic lymphatic basin, thereby preserving bowel length (37). Similarly, extending small bowel resection margins more than 10 cm from the tumor longitudinally does not increase the number of positive harvested LNs (34). The mean length of the pooled small bowel was 70.6±55.6 cm (range, 60–435 cm), which raises questions about whether surgeons adopted a bowel-sparing surgical approach. On the contrary, the number of LNs removed depends on the extent of mesentery excision, specifically the D3 volume, while preserving the bowel length and vascular arcades to prevent short bowel syndrome (19).

Specific surgical approaches for each bowel segment

Another major limitation across the literature is the lack of precise localization of the primary tumor within the small bowel. The jejunum and ileum lack fixed anatomical boundaries, and none of the reviewed series differentiated between resections of the proximal jejunum, proper jejunum, proper ileum, and terminal ileum: operations that correspond to four distinct vascular and interconnected lymphatic territories (4-6). Hence, the TIA represents the terminal branch of the SMA, arising just below the ICA origin, and provides dominant perfusion to proper ileal tumors (5). As the TIA can be ligated without consequence this renders ileal tumors as a single vessel disease when compared to its jejunal counterpart which can have multiple feeding arteries. The optimal operation thus includes ligation of the TIA at its origin distal to the ICA origin, followed by lymphadenectomy along the ICA and first JA, preserving the paraintestinal arcade. Additionally, jejunal tumors, supplied by one of the jejunal arteries, require dissection guided by the central ligation of the specific tumor-feeding vessel (D2) with the mesenterectomy along the adjacent arteries (4). The same concept applies to the distal duodenum and proximal jejunum, which are supplied mainly by the superior JA. However, distal duodenal NETs were excluded to maintain anatomical and surgical homogeneity. This exclusion underscores an important gap in the literature. These tumors arise in a transitional anatomical zone with variable lymphatic drainage, leading to inconsistent surgical approaches and reporting. Future studies should analyze distal duodenal tumors separately and define lymphadenectomy extent using clear vascular and lymphatic landmarks (6).

Given the material presented above, our research group has recently published three articles on tentative surgical techniques for radical surgery of the aforementioned segments of the small bowel (4-6). We have postulated “en bloc” surgery containing the D1/D2 and the D3 volume. For each bowel segment, the D1/D2 volumes are separate based on the tumor’s feeding vessel, whereas the D3 volume is common. This allows adequate “en bloc” but bowel-sparing surgery due to sparing of the adjacent arteries while performing the lymphadenectomy around them (Figure 2). These surgical techniques allow the removal of potentially positive central LNs, which, according to data from this scoping review, occur in approximately 50% of patients.

Figure 2 Conceptual proposal of bowel-sparing lymphadenectomy for small bowel tumors. This figure represents a surgical concept synthesized from anatomical principles and selected literature and does not depict a guideline-endorsed or prospectively validated technique in small bowel surgery. In the upper left corner: the proposed technique for the resection of distal duodenal and proximal jejunal tumors; in the lower left corner: the proposed technique for the resection of the proper jejunal tumor; on the right: the proposed technique for the resection of the ileal tumor. D2, proposed D2 volume; D3 volume, proposed D3 volume of dissection; GTH; IA, ileal artery; ICA, ileocolic artery; ICV; JA, jejunal artery; LNs, lymph nodes; MCA, middle colic artery; SJA, superior jejunal artery; SMA/SMV, superior mesenteric artery/vein; TIA, terminal ileal artery; TIVT.

Strengths and limitations

This review offers a comprehensive overview of the current literature on small bowel tumor management, evaluating the extent of lymphadenectomy and percentage of lymphonodal mesenteric metastases in the D3 volume. Its flexibility enables the use of different research methods and evidence, aiding in identifying gaps in the current surgical oncology of the small bowel. However, the lack of a systematic approach introduces bias and may omit relevant studies. Unlike systematic reviews, it lacks quantitative data synthesis, making it more difficult to assess the overall evidence. Its flexible, subjective structure can also influence the selection of studies and interpretation of the surgical procedures evaluated. An important limitation of the reviewed literature is its strong predominance of retrospective series from high-volume European tertiary centers with established expertise in small bowel lymphadenectomy. This likely overestimates the feasibility and safety of extensive dissections when extrapolated to low-volume centers or emergency settings. In addition, this review does not determine the oncologic superiority of any extent of lymphadenectomy, nor does it assess the risks or functional consequences of more extensive mesenteric dissection. The impact on bowel function and quality of life remains unclear. Prospective studies are needed to evaluate survival outcomes together with functional and patient-reported measures.

Conclusions

Current literature on small bowel tumor treatment is inconsistent, with varied terminology and undefined extent for lymphadenectomy. The techniques are reported inconsistently and lack standardization or reproducibility, which limits cross-study comparisons and evidence synthesis. Given the high percentage of positive central LNs in the mesenteric root, it is necessary to introduce standardized D3-volume lymphadenectomy guided by personalized vascular anatomy reconstructions that enable safe and bowel-sparing surgery for small bowel tumors.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the PRISMA-ScR reporting checklist. Available at https://ales.amegroups.com/article/view/10.21037/ales-2025-1-72/rc

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Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://ales.amegroups.com/article/view/10.21037/ales-2025-1-72/coif). The authors have no conflicts of interest to declare.

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