Published online Jun 27, 2024. doi: 10.4240/wjgs.v16.i6.1618
Revised: April 11, 2024
Accepted: April 23, 2024
Published online: June 27, 2024
Processing time: 163 Days and 18.9 Hours
Patients with resectable gastric adenocarcinoma accompanied by vascular cancer thrombus (RGAVCT) have a poor prognosis, with a 5-year survival rate ranging from 18.42%-53.57%. These patients need a reasonable postoperative treatment plan to improve their prognosis.
To determine the most effective postoperative chemotherapy regimen for patients with RGAVCT.
We retrospectively collected the clinicopathological data of 530 patients who un
In all, 530 eligible individuals with RGAVCT were enrolled in this study. The median overall survival (OS) of patients with RGAVCT was 24 months, and the survival rates were 80.2%, 62.5%, and 42.3% at 12, 24, and 59 months, respectively. Preoperative complications, tumor size, T stage, and postoperative chemotherapy were identified as independent factors that influenced OS in patients with RGAVCT according to the Cox multivariate analysis model. A Kaplan-Meier analysis revealed that chemotherapy had no effect on OS of patients with stage I or II RGAVCT; however, chemotherapy did have an effect on OS of stage III patients. Stage III patients who were treated with chemotherapy consisting of dual- or triple-agent regimens had better survival than those treated with single-agent regimens, and no significant difference was observed in the survival of patients treated with chemo
For patients with stage III RGAVCT, a dual-agent regimen of postoperative chemotherapy should be recom
Core Tip: In patients with resectable gastric adenocarcinoma accompanied by vascular cancer thrombus (RGAVCT), postoperative chemotherapy has an independent effect on overall survival and may even improve survival. Patients with stage I and II RGAVCT should not receive postoperative chemotherapy, and low-toxicity single-agent therapy is advised even in the presence of high-risk variables. For patients with stage III RGAVCT, a dual-agent regimen of postoperative chemotherapy should be recommended rather than a triple-agent treatment, as the latter is associated with increased risks.
- Citation: Yang ZF, Dong ZX, Dai CJ, Fu LZ, Yu HM, Wang YS. Correlation between postoperative chemotherapy regimen and survival in patients with resectable gastric adenocarcinoma accompanied with vascular cancer thrombus. World J Gastrointest Surg 2024; 16(6): 1618-1628
- URL: https://www.wjgnet.com/1948-9366/full/v16/i6/1618.htm
- DOI: https://dx.doi.org/10.4240/wjgs.v16.i6.1618
According to the 2020 Tumor Report[1], gastric cancer (GC) ranked fourth among all cancers according to the number of new cases, with approximately 1.1 million cases per year. GC ranked third in terms of mortality rate, with approximately 760000 deaths per year. GC is an important life-threatening disease and one of the most common malignant tumors worldwide. China ranks second and third in terms of new cases and deaths related to GC, respectively[2]. Studies by Zhang[3] and the Asian Cancer Research Group[4] marked significant advancements in the molecular typing of GC, thereby leading to enhanced medical treatment strategies. For stage III GC, the 5-year survival rate following surgery is 34.8%-54.6%[5], and radical surgical resection remains the preferred course of treatment. When tumor cells infiltrate the interior of lymphatic or vascular vessels, which are composed of endothelial cells, the condition is referred to as lym
Clinicopathological data were retrospectively collected from 530 patients (107 women and 423 men) who underwent radical surgery for GC at Shanxi Cancer Hospital between January 2017 and January 2022 and who were pathologically diagnosed with stomach adenocarcinoma with a vascular cancer embolus. Patient ages ranged from 28-83 years (median, 63 years). This study was approved by the Clinical Research Ethics Committee of Shanxi Cancer Hospital (approval number: KY2023010). During their first visit to the hospital, all patients provided written informed consent for the co
Inclusion and exclusion criteria: The inclusion criteria were as follows: (1) Radical resection of GC at Shanxi Cancer Hospital; (2) postoperative pathological confirmation of gastric adenocarcinoma or adenocarcinoma of the gastroesophageal junction; (3) postoperative pathological evidence of vascular cancer thrombus; (4) clinical stage I, II, or III disease; and (5) availability of complete clinicopathological data. The exclusion criteria were as follows: (1) Presence of other tumors; (2) nonradical resection, such as surgery with positive margins or palliative surgery; and (3) incomplete or una
Staging and Ki-67 positivity: Pathological and histological staging was performed according to the 2019 version of the World Health Organization Classification of Tumors of the Digestive System. Ki-67 positivity < 30% was considered low expression, while Ki-67 positivity ≥ 30% was considered high expression.
Follow-up: Regular gastroenterology outpatient reviews, hospitalization, and telephone interviews were used for patient survival follow-up. The deadline for follow-up was March 2023. Overall survival (OS) was defined as the time from the date of surgery to the date of death or the end of follow-up.
Clinical information: Patient information, including sex, age at the time of surgery, medical history, family history, preoperative complications, surgical procedures, and postoperative chemotherapy, was collected.
Pathological information: The pathology report included information regarding the location and size of the tumor, the degree of tumor differentiation, the Lauren classification, LBVI, neural invasion, the depth of invasion, the total number of cleared lymph nodes, and immunohistochemistry findings.
Research participants and chemotherapy regimens: To ensure the authenticity and reliability of our results, we collected information on patients who received postoperative adjuvant chemotherapy at our hospital.
SPSS (version 25.0; IBM, Armonk, NY) and R 4.3.0 (R Foundation, Vienna, Austria) were used for the statistical analysis. The rank-sum test was used to evaluate the skewed distributions, which are expressed as the mean and standard de
The 530 patients with RGAVCT who met the inclusion criteria ranged in age from 28–83 (median, 63) years (Table 1). A 4:1 male-to-female ratio was noted, with 423 men and 107 women. A total of 9.2% of patients had a family history of tumors, and 86.4% of patients had no preoperative complications. For those patients who did experience preoperative complications, 7.7%, 1.9%, 1.1%, and 2.8% experienced gastrointestinal obstruction, gastrointestinal hemorrhage, other complications (such as perforation, gastric retention, and anemia), and multiple complications, respectively. Open sur
| Characteristic | n (%) | χ2 | P value |
| Age, yr | |||
| < 60 | 211 (39.8) | 5.943 | 0.015 |
| ≥ 60 | 319 (60.2) | ||
| Sex | |||
| Male | 423 (79.8) | 7.533 | 0.006 |
| Female | 107 (20.2) | ||
| Past history | |||
| No | 289 (54.5) | 3.76 | 0.052 |
| Yes | 241 (45.5) | ||
| Family history | |||
| No | 479 (90.4) | 4.711 | 0.030 |
| Yes | 51 (9.6) | ||
| Preoperative complications | |||
| No | 458 (86.4) | 1.982 | 0.037 |
| Digestive tract obstruction | 41 (7.7) | ||
| Alimentary tract hemorrhage | 10 (1.9) | ||
| Others1 | 6 (1.1) | ||
| ≥ 2 complications | 15 (2.8) | ||
| Surgical method | |||
| Open abdominal | 328 (61.9) | 1.853 | 0.396 |
| Laparoscopy | 179 (33.8) | ||
| Joint thoracoabdominal | 23 (4.3) | ||
| Chemotherapy | |||
| No | 136 (25.7) | 63.834 | <0.001 |
| Yes | 394 (74.3) | ||
| Tumor site | |||
| Proximal | 286 (54) | 2.217 | 0.330 |
| Distal | 144 (27.2) | ||
| Body | 100 (18.9) | ||
| Differentiation | |||
| Moderate | 54 (10.2) | 5.742 | 0.057 |
| Moderate-poor | 188 (35.5) | ||
| Poor | 288 (54.3) | ||
| Lauren classification | |||
| Diffused type | 182 (34.3) | 11.859 | 0.008 |
| Intestinal type | 62 (11.7) | ||
| Mixed type | 252 (47.5) | ||
| NA | 34 (6.4) | ||
| Neural invasion | |||
| Absence | 247 (46.6) | 5.899 | 0.015 |
| Presence | 283 (53.4) | ||
| Tumor size, cm | |||
| < 5 | 231 (43.6) | 8.976 | 0.003 |
| ≥ 5 | 299 (56.4) | ||
| HER2 expression | |||
| Negative | 458 (86.4) | 0.495 | 0.482 |
| Positive | 72 (13.6) | ||
| MMR status | |||
| dMMR | 14 (2.6) | 0.229 | 0.633 |
| pMMR | 516 (97.4) | ||
| Ki-67 expression | |||
| Low | 8 (1.5) | 6.019 | 0.014 |
| High | 522 (98.5) | ||
| T stage | |||
| 2 | 44 (8.5) | 25.459 | < 0.001 |
| 3 | 374 (70.6) | ||
| 4a | 93 (17.5) | ||
| 4b | 18 (3.4) | ||
| N stage | |||
| 0 | 37 (7) | 42.8 | < 0.001 |
| 1 | 104 (19.6) | ||
| 2 | 137 (25.8) | ||
| 3a | 158 (29.8) | ||
| 3b | 94 (17.7) | ||
| Stage | |||
| IB | 10 (1.9) | 62.765 | < 0.001 |
| IIA | 43 (8.1) | ||
| IIB | 80 (15.1) | ||
| IIIA | 132 (24.9) | ||
| IIIB | 171 (32.3) | ||
| ШC | 94 (17.7) |
According to the Union for International Cancer Control TNM staging system (8th edition), 10 patients (1.9%) were categorized as stage IB, 43 (8.1%) as stage IIA, 80 (15.1%) as stage IIB, 132 (24.9%) as stage IIIA, 171 (32.3%) as stage IIIB, and 94 (17.7%) as stage IIIC. The RGAVCT tumor sites were mainly distributed in the proximal (54%), distal (27.2%), and gastric bodies (18.9%). Tumors were predominantly poorly differentiated (54.3%), intermediate-poorly differentiated (35.5%), and moderately differentiated (10.2%); none were well differentiated.
The Lauren classification was predominantly mixed (47.5%) or diffused (34.3%), while the intestinal type was less frequent (11.7%). Neural invasion was observed in 53.4% of the patients. Tumors > 5 cm were found in 56.4% of the patients. Immunohistochemistry indicated Her-2 positivity (3+ or 2+ fluorescent in situ hybridization positivity) in ap
The median OS (mOS) of patients with RGAVCT was 24 months, with survival rates of 80.2%, 62.5%, 54.8%, and 42.3% at 12, 24, 37, and 59 months, respectively. The postoperative chemotherapy group had an mOS of 25 months, and the survival rates were 86.8%, 71.3%, 64.2%, and 52.8% at 12, 24, 37, and 53 months, respectively. The mOS was 15 months in the group that did not receive chemotherapy, and the survival rates were 61%, 38.1%, 28.5%, and 19% at 12, 24, 34, and 59 months, respectively. Patients with stage I and II cancer had an mOS of 27 months, with survival rates of 89.5%, 80%, 74.6%, and 52.2% at 12, 24, 34, and 59 months, respectively (Figure 1A). The mOS of patients with stage III cancer was 23 months, with survival rates of 77.8%, 57.8%, 49.5%, and 40.1% at 12, 24, 37, and 53 months, respectively. The best survival rate was observed in patients with stage IIIA cancer, followed by those with stage IIIB cancer, while the worst survival rate was observed in patients with stage IIIC cancer (Figure 1B).
The univariate analysis by Mantel-Cox regression revealed significant differences (P < 0.05) in age, sex, family history, preoperative complications, postoperative chemotherapy, Lauren classification, neural invasion status, tumor size, Ki-67 expression, T and N stage, and clinical stage, and these factors were significantly correlated with the OS of patients with RGAVCT. A multivariate Cox analysis of the significant influencing factors revealed that preoperative complications (P = 0.035), postoperative chemotherapy [P < 0.001; hazard ratio (HR) = 0.35; 95% confidence interval (CI) = 0.26-0.46], tumor size (P = 0.035; HR = 1.36; 95%CI = 1.02-1.80), and T stage (P = 0.005) were independent factors that affected OS (Figure 2).
Of the 394 patients with RGAVCT who were administered postoperative adjuvant chemotherapy, 323 received che
The univariate analysis revealed no significant difference between postoperative chemotherapy and survival in pa
The Cox multivariate analysis revealed that preoperative complications (P = 0.021), neural invasion (P = 0.02; HR = 2.47; 95%CI = 1.16-5.28), and Ki-67 expression (P = 0.007; HR = 0.05; 95%CI = 0.01-0.44) were independent factors found to influence the survival of patients with stage I and II RGAVCT (Table 2). However, postoperative chemotherapy did not affect the OS of high-risk patients with stage I and II RGAVCT (P = 0.653).
| Characteristic | N | Univariate analysis | Multivariate analysis | ||
| χ2 | P value | HR (95%CI) | P value | ||
| Preoperative complications | |||||
| No | 115 | 27.724 | < 0.001 | 1 | 0.021 |
| Digestive tract obstruction | 4 | 2.15 (0.50-9.32) | 0.304 | ||
| Alimentary tract hemorrhage | 1 | 2.90 (0.38-22.41) | 0.307 | ||
| Others1 | 3 | 7.07 (1.91-26.15) | 0.003 | ||
| Neural invasion | |||||
| Absence | 73 | 10.014 | 0.002 | 1 | |
| Presence | 50 | 2.47 (1.16-5.28) | 0.02 | ||
| Ki-67 expression | |||||
| Low | 1 | 5.58 | 0.018 | 1 | |
| High | 122 | 0.05 (0.01-0.44) | 0.007 | ||
The Kaplan-Meier analysis revealed that postoperative chemotherapy affected the OS of patients with stage III RGAVCT (P < 0.001) (Figure 3A). Furthermore, compared with patients treated with a single-agent regimen, individuals who were treated with chemotherapy consisting of dual- or triple-agent regimens had higher survival rates (P = 0.047 and P = 0.034) (Figure 3B and C), and no significant difference was observed between the survival of patients treated with dual-agent regimens and that of those treated with triple-agent regimens (P = 0.646) (Figure 3D).
The aim of this study was to determine the most effective postoperative chemotherapy regimen for patients with RG
GC is a life-threatening disease and is one of the primary causes of cancer-related death worldwide. The introduction of novel anticancer medications, neoadjuvant radiation, adjuvant chemotherapy, and late-stage palliative care are among the numerous advancements in the systemic treatment of GC. These measures have significantly increased the survival rates of patients with GC. However, high postoperative recurrence and metastasis rates adversely affect the survival of patients with GC. The postoperative clinicopathological features of GC are also the primary prognostic factors associated with this disease. In a study by Chen et al[8], the depth of tumor infiltration, extent of lymph node metastasis, extent of distant metastasis, and pathological score were used to predict the prognosis and OS of patients with GC. The impact of vascular cancer embolism on the prognosis of malignant tumors has received considerable attention because of detailed research on tumor prognostic variables and the concept of micrometastasis[9,10]. Vascular cancer emboli are tumor cells that form aggregates with fibrin clots, coexist with erythrocytes, infiltrate the endothelial cell space arrangement of the surrounding tissue in the absence of erythrocytes, or invade the smooth muscle cell space arrangement[11,12].
Torre et al[13] reported a 2:1 male-to-female ratio in the global incidence of GC in 2012, while Sung et al[1] reported that the global incidence of GC in 2020 was approximately 7.2% for men and 4.4% for women. These studies show that the number of men with GC is greater than that of women. The male-to-female ratio of patients with RGAVCT in this study was 4:1, which was much higher than the global male-to-female ratio of GC patients. Consequently, vascular cancer em
Regarding the baseline characteristics of patients with RGAVCT, our study revealed that the type of surgery (open, laparoscopic, or combined thoracoabdominal) had no effect on OS. Moreover, we found that surgeons involved in clinical assessments selected the appropriate surgical approach based on the specific conditions of the patients. In more than half (53.4%) of the patients with RGAVCT and concomitant neural invasion, we found that vascular cancer embolus and neural invasion were likely to occur simultaneously. Among the patients with RGAVCT who were analyzed, 10 had stage IB RGAVCT, 123 had stage II RGAVCT, and 397 had stage III RGAVCT, which accounted for 74.9% of all patients. This indicates that vascular cancer embolisms occurred more often in patients with advanced GC. The median survival time (mOS = 23 months) and survival rates at 12 months (77.8%), 24 months (57.8%), 34 months (49.5%), and 53 months (40.1%) of patients with stage III RGAVCT were significantly lower than those of patients with stages I and II RGAVCT (mOS = 27 months; 12 months, 89.5%; 59 months, 52.2%).
The risk factors for GC include many immutable variables, such as age[14], sex, and race/ethnicity. Additionally, some modifiable risk factors, such as Helicobacter pylori infection[15], smoking[16], and high nitrate and nitrite diets, have also been identified. Several known hereditary cancer syndromes are associated with GC, including hereditary diffuse GC (CDH1) syndrome, the most strongly associated syndrome, which occurs in approximately 80% of patients[17]. The mul
In this study, the mOS was 25 months in the chemotherapy group, which was greater than that in the nonchemotherapy group (15 months), which indicates that chemotherapy could prolong the survival of patients with RGAVCT. Several studies[19-21] have suggested that postoperative chemotherapy can improve the prognosis of patients with GC. However, postoperative chemotherapy is the only intervening factor among the independent factors that affect the OS of patients with RGAVCT, and a rational postoperative chemotherapy regimen can further improve the prognosis of these patients. A clinical consensus[22] has been established that postoperative adjuvant therapy should be recommended for patients who undergo D2 radical surgery and who do not receive preoperative treatment for postoperative pathological stage II and III progressive GC. In this study, 530 patients were evaluated based on clinical stage, and we found that postoperative chemotherapy did not affect the OS of patients with stage I and II RGAVCT. We further investigated whe
We explored the effect of postoperative chemotherapy on the OS of patients with stage III RGAVCT (P < 0.001) and discovered a substantial difference in survival between patients who received postoperative chemotherapy and those who did not. The recent JACCRO GC-07 study[23], which investigated chemotherapy regimens and clinical outcomes, showed that the continuation of an oral S-1 monotherapy regimen (DS sequential S-1) after six cycles of postoperative docetaxel combined with S-1 improved the survival of patients with stage III GC compared with S-1 alone (3-year re
Postoperative chemotherapy has an independent effect on OS in patients with RGAVCT and can increase survival. However, chemotherapy administered after surgery had little effect on the OS of patients with stage I and II RGAVCT. Moreover, triple-agent treatment is associated with more adverse events than other forms of treatment. Therefore, we recommend that patients with stage II RGAVCT receive dual-agent chemotherapy. The clinical implications and future scope are clear.
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