Published online Jan 14, 2027. doi: 10.3748/wjg.124537
Revised: July 22, 2026
Accepted: July 29, 2026
Published online: January 14, 2027
Processing time: 146 Days and 21.9 Hours
Serum pepsinogen (PG) is a potential biomarker for monitoring recurrence after total gastrectomy for gastric cancer (GC). Computed tomography (CT) imaging provides anatomical localization but has limited sensitivity for early recurrence. The complementary value of combining these two modalities and the impact of tumor differentiation on the diagnostic performance of PG require systematic eva
To evaluate the combined diagnostic value of serum PG and CT imaging for recurrence after total gastrectomy, and to assess the impact of histological differentiation on PG-based diagnosis.
Data from 110 patients who underwent radical total gastrectomy for GC were retrospectively analyzed. Using a comprehensive reference standard, positivity rates of serum PG levels and CT imaging for recurrence were compared. Receiver operating characteristic curves were generated to assess the individual diagnostic performance of each modality, and a combined predictive model was developed using multivariate logistic regression. Immunohistochemistry was performed to examine PG expression in tumor tissues and its relationship with histological dif
During the 1-year post-operative follow-up, recurrence was confirmed in 65 patients (59.09%). The positivity rate of serum PG was significantly higher than CT imaging overall (56.36% vs 40.00%; P = 0.0027) and in the recurrence subgroup (92.31% vs 63.08%; P = 0.0008). The area under the curve (AUC) for serum PG alone was 0.94, whereas that for CT imaging alone was 0.78. The combined logistic regression model achieved an AUC of 0.98. Both serum PG [odds ratio (OR) = 501.25; P < 0.0001] and CT imaging (OR = 58.22; P = 0.001) were independent predictors of recurrence. PG expression was higher in undifferentiated than in differentiated tumors (86.36% vs 14.29%; P = 0.0011). After excluding PG-negative differentiated recurrences, serum PG sensitivity increased from 92.31% to 98.36%.
Serum PG and CT imaging play complementary roles in functional assessment and morphological localization. Integrating these modalities with histological stratification provides a highly sensitive tool for diagnosing post-gastrectomy recurrence and supports personalized postoperative surveillance.
Core Tip: This study evaluated the combined diagnostic performance of serum pepsinogen (PG) and computed tomography (CT) imaging for detecting recurrence after total gastrectomy. We found that serum PG and CT imaging play complementary roles, with PG providing early functional warning by reflecting secretory tumor burden and CT imaging offering anatomical confirmation. Importantly, PG expression varied substantially by histological differentiation, and this heterogeneity directly influenced the diagnostic sensitivity of serum PG. These findings support a histology-stratified, PG-centered surveillance strategy that integrates functional and morphological information for personalized postoperative follow-up.
- Citation: Zhang JR, Xu XW, Liu JM, Zhu ZH, Mao CM. Serum pepsinogen combined with computed tomography imaging for diagnosing recurrence of gastric cancer after total gastrectomy. World J Gastroenterol 2027; 33(2): 124537
- URL: https://www.wjgnet.com/1007-9327/full/v33/i2/124537.htm
- DOI: https://dx.doi.org/10.3748/wjg.124537
Gastric cancer (GC) remains among the most common and lethal malignancies worldwide, with a particularly high incidence in East Asia, including China[1,2]. Although radical total gastrectomy can effectively resect the primary tumor and improve short-term outcomes for locally advanced disease[3,4], postoperative recurrence severely compromises long-term survival, with 5-year recurrence rates ranging from 40% to 60%[5]. Early and accurate detection of recurrence is therefore critical for timely intervention and improved prognosis.
Current postoperative surveillance relies primarily on imaging modalities and serum biomarkers. Computed tomography (CT) imaging can delineate the location, size, and extent of recurrent lesions[6,7]; however, its sensitivity for identifying subcentimeter metastases and occult lesions is limited, and CT imaging often fails to reliably distinguish benign postoperative changes from early malignant recurrence, potentially causing diagnostic delays[8]. Serum biom
The rationale for this integration lies in leveraging the complementary strengths of different modalities to overcome their individual limitations[13-15]. In the context of postgastrectomy recurrence, serum PG levels may serve as an early molecular sentinel for minimal secretory tumor burden, whereas CT imaging confirms the presence and site of lesions, suggesting synergistic functional-morphological complementarity[9,16]. However, studies exploring the combined use of serum PG levels and CT imaging for this specific indication remain scarce, and the diagnostic performance and underlying mechanisms have not been fully elucidated. Moreover, GC exhibits substantial intertumoral heterogeneity, with divergent biological behaviors and molecular expression profiles across histological differentiation types[17]; however, the extent to which this heterogeneity influences the diagnostic accuracy of serum PG levels is poorly under
This retrospective study was approved by the Ethics Committee of the Affiliated Hospital of Jiangsu University (Approval No. KY2023K0603) and was conducted in accordance with the Declaration of Helsinki. The requirement for written informed consent was waived because of the retrospective nature of the study and the exclusive use of anonymized clinical data without altering patient management. Consecutive patients with GC who underwent radical total gastrectomy at the Affiliated Hospital of Jiangsu University between February 2023 and February 2025 were enrolled. All patients completed a standardized 12-month follow-up protocol comprising outpatient visits, telephone interviews, and inpatient re-examinations. Follow-up visits were scheduled monthly for the first six months after surgery. Thereafter, the follow-up interval was tailored to each patient’s clinical status and typically extended to every 2 to 3 months. This adjustment was guided by symptoms, trends in serum tumor markers (CEA and CA19-9), imaging fin
The reference standard for recurrence was defined as a comprehensive clinical assessment: Histopathological con
The inclusion criteria were as follows: (1) Histopathologically confirmed gastric adenocarcinoma after surgery, including special subtypes such as mucinous adenocarcinoma and signet ring cell carcinoma; (2) R0 radical total gas
Fasting venous blood samples (5 mL) were drawn in the morning after admission for follow-up. Serum was separated by centrifugation at 4000 × g for 10 minutes and stored at -20 °C until analysis. Serum PG I and PG II concentrations were measured using a chemiluminescence immunoassay on a fully automated analyzer (Snibe Co. Ltd., Shenzhen, China), in strict accordance with the manufacturer’s protocol. The assay involved the formation of sandwich immunocomplexes with ABEI- and FITC-labeled monoclonal antibodies; relative light units were automatically measured and converted to concentrations.
On the basis of our previously established cutoffs, a positive serum PG result was defined as a PG I > 26.93 ng/mL and/or a PG II > 0.96 ng/mL and was treated as a binary variable (positive = 1, negative = 0) in subsequent analyses[11].
CT imaging was performed with a 256-slice scanner (Revolution CT, GE Healthcare, United States). Both unenhanced and contrast-enhanced images were acquired. Contrast-enhanced scans were obtained after intravenous bolus injection of iodinated contrast medium, with images captured in the arterial, portal venous, and delayed phases. All image datasets were transmitted to the PACS for analysis. Two board-certified radiologists with more than 5 years of experience inde
Paraffin-embedded tumor sections (4 µm) were deparaffinized, rehydrated, and subjected to heat-induced antigen retrieval in citrate buffer (pH 6.0). Endogenous peroxidase activity was blocked with 3% hydrogen peroxide, followed by incubation with 10% normal goat serum to prevent nonspecific binding. The sections were incubated overnight at 4 °C with rabbit anti-human PG I and PG II primary antibodies (Snibe Co. Ltd., 1:300), followed by incubation with an HRP-conjugated goat anti-rabbit IgG secondary antibody for 30 minutes at 37 °C. Staining was visualized with DAB, and the sections were counterstained with hematoxylin.
Positive immunoreactivity was identified as a brownish cytoplasmic staining. Two experienced pathologists inde
Statistical analyses were performed using MedCalc version 15.2.2.0. Continuous variables are presented as the mean ± SD and were compared using the independent-samples t-test. Categorical variables are presented as n (%). Group comparisons for categorical data were conducted using the χ2 test or Fisher’s exact test, whereas the McNemar test with continuity correction was used to compare paired positivity rates between serum PG levels and CT images. Diagnostic performance was evaluated by receiver operating characteristic (ROC) curve analysis with calculation of the area under the curve (AUC). A multivariate logistic regression model was constructed with recurrence status (recurrence = 1, no recurrence = 0) as the dependent variable and binary serum PG level and CT imaging results as independent variables (Enter method). The predicted probabilities from this model were used to generate the combined ROC curve. All tests were two-sided, and P < 0.05 was considered to indicate statistical significance.
A total of 110 patients who underwent R0 radical total gastrectomy for gastric adenocarcinoma were enrolled in this retrospective study. The baseline demographic and clinical characteristics, including tumor location, pathological stage, and histological subtype, are summarized in Table 1. The mean age of the overall cohort was 66.13 ± 8.83 years (range: 34-88 years), and 84 patients (76.36%) were male. All patients received neoadjuvant therapy. Among the 110 patients, 65 (59.09%) experienced recurrence within the 1-year follow-up period, whereas 45 (40.91%) experienced no evidence of recurrence.
| Variables | Total (n = 110) | Recurrence (n = 65) | No recurrence (n = 45) | P value |
| Age (years), mean ± SD | 66.13 ± 8.83 | 67.11 ± 8.64 | 64.71 ± 9.01 | 0.1626 |
| Age range (years) | 34-88 | 34-88 | 37-81 | - |
| Sex | 0.3295 | |||
| Male | 84 (76.36) | 47 (72.31) | 37 (82.22) | |
| Female | 26 (23.64) | 18 (27.69) | 8 (17.78) | |
| Tumor location | 0.2434 | |||
| Cardia | 70 (63.64) | 46 (70.77) | 24 (53.33) | |
| Gastric body | 30 (27.27) | 15 (23.08) | 15 (33.33) | |
| Gastric antrum | 8 (7.27) | 4 (6.15) | 4 (8.89) | |
| Gastric angle | 1 (0.91) | 0 (0.00) | 1 (2.22) | |
| Pylorus | 1 (0.91) | 0 (0.00) | 1 (2.22) | |
| Pathological stage | 0.0004b | |||
| I | 18 (16.36) | 6 (9.23) | 12 (26.67) | |
| II | 19 (17.27) | 8 (12.31) | 11 (24.44) | |
| III | 58 (52.73) | 38 (58.46) | 20 (44.44) | |
| IV | 15 (13.64) | 13 (20.00) | 2 (4.44) | |
| Histological subtype | 0.1825 | |||
| Differentiated | 48 (43.64) | 32 (49.23) | 16 (35.56) | |
| Undifferentiated | 56 (50.91) | 28 (43.08) | 28 (62.22) | |
| Mucinous adenocarcinoma | 4 (3.64) | 3 (4.62) | 1 (2.22) | |
| Signet ring cell carcinoma | 2 (1.82) | 2 (3.08) | 0 (0.00) |
The overall positivity rate of serum PG levels was 56.36% (62/110), significantly exceeding the 40.00% (44/110) rate for CT imaging (McNemar χ2 = 9.03; P = 0.0027). In the recurrence subgroup, serum PG levels were positive in 92.31% (60/65) of the patients, whereas CT imaging was positive in only 63.08% (41/65) patients (McNemar χ2 = 11.17; P = 0.0008) (Table 2).
Longitudinal monitoring revealed that seven patients exhibited elevated serum PG levels early after surgery, whereas concurrent CT imaging revealed no evidence of recurrence or metastasis; all seven patients were subsequently confirmed to have developed recurrent disease on continued imaging follow-up (Figure 1). Conversely, five patients with CT imaging-documented recurrence remained serum PG negative.
ROC analysis revealed that serum PG levels alone yielded an AUC of 0.94 [95% confidence interval (CI): 0.88-0.98], with a sensitivity of 0.92 and a specificity of 0.96 (P < 0.0001). CT alone yielded an AUC of 0.78 (95%CI: 0.69-0.86), with a sensitivity of 0.63 and a specificity of 0.93 (P < 0.0001) (Table 3 and Figure 2).
Multivariate logistic regression revealed both serum PG levels [B = 6.22; P < 0.0001; odds ratio (OR) = 501.25; 95%CI: 45.08-5573.97] and CT imaging (B = 4.06; P = 0.001; OR = 58.22; 95%CI: 5.14-660.11) as independent predictors of recurrence (Table 4). The regression equation was ln(P/(1-P)) = -3.75 + 6.22 × (serum PG) + 4.06 × (CT imaging), where both variables are binary and P is the predicted probability of recurrence. The combined model achieved an AUC of 0.98 (95%CI: 0.93-1.00), with a sensitivity of 1.00 and a specificity of 0.91 (P < 0.0001) (Table 3 and Figure 2).
To elucidate the biological basis of the observed complementarity, PG expression was assessed immunohistochemically in tumor tissues stratified by differentiation type. Among patients with recurrence, the percentage of PG-positive patients was significantly greater for undifferentiated GC (UGC) than for differentiated GC (DGC) [86.36% (19/22) vs 14.29% (1/7), P = 0.0011]. In DGC patients, PG expression was positive in only 1 of 7 (14.29%) patients, coinciding with the sole serum PG-positive DGC case; CT imaging was positive in 5 (71.43%) of these patients, highlighting the diagnostic advantage of CT in PG-low-expressing tumors. In contrast, UGC recurrence was characterized by high PG expression (86.36%), high serum PG positivity (81.82%), and a CT imaging positivity rate of 59.09%. In the small subgroup, mucinous adenocarcinomas (n = 2) were PG-negative and CT imaging-negative, whereas all signet ring cell carcinomas (n = 3) were PG-positive by both immunohistochemistry and serum assays, with CT imaging positive in two-thirds of the cases (Table 5 and Figure 3).
| Histological Type | n | PG expression+ | Serum PG+ | CT imaging+ |
| DGC | 7 | 1 (14.29) | 1 (14.29) | 5 (71.43) |
| UGC | 22 | 19 (86.36) | 18 (81.82) | 13 (59.09) |
| MADC | 2 | 0 (0.00) | 0 (0.00) | 0 (0.00) |
| SRCC | 3 | 3 (100.00) | 3 (100.00) | 2 (66.67) |
When the four patients with PG-negative DGC recurrence were excluded, the sensitivity of serum PG levels increased from 92.31% (60/65) to 98.36% (60/61), indicating that the histological differentiation type is a key determinant of serum PG diagnostic performance.
The high postoperative recurrence rate remains the primary obstacle to long-term survival after total gastrectomy for GC[5]. Routine surveillance currently relies on CT imaging, yet its sensitivity for early micro-metastases and subclinical lesions is limited, precluding true early warning[7,8]. A multimodal strategy that integrates functional and morphological information is therefore needed to optimize postoperative follow-up. This study evaluated the combined diagnostic value of serum PG levels and CT imaging in this context and, for the first time, elucidated their functional and morphological complementarity through the lens of heterogeneous PG expression in tumor tissues, providing a new framework for biology-informed, individualized surveillance.
Serum PG levels offer an earlier warning of recurrence than CT imaging. Several patients had elevated serum PG levels early after surgery, whereas CT results remained negative, with radiological confirmation emerging months later. This temporal gap is clinically meaningful and suggests that serum PG levels can detect minimal secretory tumor burden before lesions become radiologically visible. The underlying biology is straightforward, as GC cells retain PG-secreting capacity, and even minute recurrent foci below CT resolution can release PG into the circulation at detectable levels[11]. Serum PG thus acts as a “functional” biomarker, whereas CT imaging serves as a “morphological” tool. This distinction underpins their combined use: PG provides early molecular warning, and CT adds anatomical localization and con
Beyond the diagnostic limitations discussed above, the current reliance on CT-based surveillance is associated with additional clinical burdens that warrant consideration. Repeated contrast-enhanced CT examinations over the surveillance period result in cumulative radiation exposure, which is a nonnegligible concern for patients who require lifelong follow-up[18]. The financial cost of serial CT imaging also imposes a substantial economic burden on health care systems and patients, particularly in resource-limited settings where access to high-resolution CT scanners is constrained[19]. Furthermore, the false-negative rate of CT for early or occult recurrence, as observed in this study, may lead to delayed diagnosis and missed therapeutic windows. These limitations underscore the clinical need for a simple, noninvasive, and cost-effective biomarker that can complement CT-based surveillance. Serum PG level measurement, which requires only a peripheral blood draw and is performed on widely available automated immunoassay platforms, fulfills these criteria. Integrating serum PG levels into routine follow-up protocols could reduce the frequency of CT exa
Serum PG levels are not uniformly sensitive across all recurrences. Immunohistochemistry revealed marked differentiation-dependent heterogeneity in PG expression. Differentiated adenocarcinomas exhibit weak or absent PG synthesis and frequently yield negative serum results, whereas undifferentiated tumors retain robust secretory capacity. Mucinous adenocarcinoma and signet ring cell carcinoma represent two biologically distinct subtypes with divergent secretory profiles. Mucinous adenocarcinoma, characterized by abundant extracellular mucin, largely lacks chief cell differentiation, resulting in constitutively low PG expression and reduced sensitivity of serum PG levels[21]. In this cohort, both mucinous tumors were uniformly PG-negative on immunohistochemistry and serum testing and were undetected by CT, highlighting the diagnostic difficulty of this subtype. In contrast, signet ring cell carcinoma frequently retains gastric epithelial lineage features[22] and expresses PG isoenzymes, particularly PG II, facilitating serological detection[23]. All three signet ring cell carcinomas in this series were concordantly PG-positive on tissue staining and serum testing, with two of the three also detected by CT. Although constrained by the small sample size, these divergent patterns align with the literature and reinforce that the performance of PG-based surveillance is strongly influenced by histological phenotype. The “false-negative” serum PG level results in certain tumors therefore reflect intrinsic tumor biology rather than assay failure, confirming that no single biomarker covers the full spectrum of tumor subtypes[24,25]. This finding also explains biologically why CT complements PG in patients with PG-negative differentiated recurrences. The two modalities achieve genuine complementarity, with one capturing functional secretory activity and the other delineating morphological lesions. This synergy is quantitatively confirmed by the combined logistic regression model, which achieved an AUC approaching 1.0, substantially outperforming either modality alone. Compared with recent radiomics-based recurrence prediction models[13,26,27], the present model offers comparable or superior performance with lower cost, greater simplicity, and wider clinical applicability, as it relies primarily on serum PG levels. This multimodal strategy, centered on serum PG and complemented by CT, achieves synergistic functional warning and morphological confirmation.
On the basis of these findings, we propose a stratified surveillance algorithm centered on serum PG levels. All postgastrectomy patients should undergo serum PG measurements every 1 to 3 months. A persistent or rising PG level, even with a negative CT imaging examination, should prompt intensified surveillance or consideration of PET-CT; conversely, concurrent serum PG level elevation and positive CT imaging can directly establish a diagnosis of recurrence. Management should be further stratified according to postoperative pathological classification. For patients with tumors exhibiting high PG expression (such as undifferentiated or signet ring cell carcinomas), serum PG levels could serve as the primary monitoring tool, with CT imaging reserved for confirmation. For PG-low-expressing tumors (differentiated or mucinous adenocarcinomas), CT imaging and/or alternative markers such as CEA or CA19-9 should be the main methods[20,28,29]. The logistic regression model developed in this study can quantify an individual’s probability of recurrence, facilitating refined clinical decision-making. This strategy has the potential to maintain surveillance sensitivity while reducing unnecessary radiation exposure and health care resource consumption, offering clear translational me
Several limitations warrant consideration. The single-center retrospective design and moderate sample size may limit generalizability, and the combined model has not yet been externally validated. Additionally, certain baseline variables, such as the extent of lymphadenectomy and reconstruction technique, were not uniformly documented in the retro
The integration of serum PG and CT imaging provides a clinically valuable multimodal diagnostic approach that combines functional early warning with morphological confirmation. By accounting for heterogeneity in PG expression related to tumor differentiation, this strategy enables sensitive and comprehensive detection of recurrence after total gas
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