Prognostic value of moderate or massive ascites in patients with advanced gastric cancer

doi:10.21203/rs.3.rs-3124054/v1

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Prognostic value of moderate or massive ascites in patients with advanced gastric cancer

https://doi.org/10.21203/rs.3.rs-3124054/v1

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Background

Advanced gastric cancer is one of highly aggressive malignancies. The available literature does not provide the prognostic value of ascites based on its degree because most clinical trials exclude patients who present with massive ascites. Therefore, this study aimed to examine whether the presence or degree of ascites has a prognostic value in patients with advanced gastric cancer in clinical settings.

Methods

Totally, 124 patients with advanced gastric cancer were recruited. The degree of ascites was assessed using computed tomography (CT) and classified as none, small, moderate, or massive. The overall survival (OS) was compared based on the presence or degree of ascites. Furthermore, the Cox proportional hazards analysis was performed to ascertain the predictors of OS.

Results

The cumulative one year, and two year OS rates in patients without ascites were 43.5%, and 20.2%, respectively, whereas those in patients with ascites were 29.1%, and 13.6%, respectively (P = 0.116). The cumulative one year, and two year OS rates in patients without moderate or massive ascites were 39.5%, and 20.9%, respectively, whereas those in patients with moderate or massive ascites were 28.0%, and 4.0%, respectively (P = 0.027). In the multivariate analysis, diffuse-type (hazard ratio [HR], 1.532; 95% confidence interval [CI], 1.002–2.343; P = 0.049), moderate or massive ascites (HR, 2.153; 95% CI, 1.301–3.564; P = 0.003), and chemotherapy (HR, 0.189; 95% CI, 0.101–0.352; P < 0.001) were significant predictive factors of OS.

Conclusion

We determined that moderate or massive ascites influenced OS of patients with advanced gastric cancer.

ascites

advanced gastric cancer

prognosis

Stomach cancer accounts for over 1,000,000 cases annually worldwide. It is the fourth leading cause of cancer and the fifth leading cause of mortality [1]. Recent studies show that the five-year overall survival (OS) of patients undergoing endoscopic resection or laparoscopy-assisted distal gastrectomy for gastric cancer is 89.0–98.2% [2, 3]. However, the long-term outcomes of patients with advanced or unresectable gastric cancer remain poor. Despite of recent advances in chemotherapeutics, the median OS is 13.1–17.45 months in patients with unresectable advanced gastric cancer receiving nivolumab plus chemotherapy [4, 5].

A study from Netherlands reported a median OS of four months in gastric cancer patients with peritoneal metastasis [6]. Intraperitoneal paclitaxel in addition to systemic chemotherapy was developed to improve their outcomes, however, the median OS in patients undergoing intraperitoneal paclitaxel with systemic chemotherapy was not found superior to that of patients who undergoing systemic chemotherapy alone (17.7 vs 15.2 months, p = 0.08) in the PHOENIX-GC trial [7]. In clinical settings, the presence of massive ascites can impair activities of daily living, resulting in poor prognosis. Additionally, many clinical trials exclude gastric cancer patients with massive ascites caused by peritoneal metastasis, suggesting that data from clinical studies may not reflect the clinical course of patients with peritoneal metastasis.

Therefore, our aim was to examine whether the presence or degree of ascites in advanced gastric cancer influenced prognostic value using real-world data.

Patients

We retrospectively recruited 124 advanced gastric cancer patients who were diagnosed or treated at Fukuchiyama City Hospital from April 2009 to March 2020. We assessed patient characteristics, including blood chemical analysis at diagnosis, age, sex, and Eastern Cooperative Oncology Group Performance Status (ECOG-PS). We also assessed clinicopathological characteristics such as macroscopic type, location, histological type, human epidermal growth factor receptor 2 (HER2) status, liver metastasis, bone metastasis, and the presence and degree of ascites. The histological type was classified as intestinal or diffuse type according to the Lauren classification [8]. Blood chemical analysis included the following items; white blood cell count, hemoglobin, platelet count, total protein, albumin, alkaline phosphatase (ALP), lactate dehydrogenase (LDH), C-reactive protein (CRP), carcinoembryonic antigen (CEA), carbohydrate antigen 19 − 9 (CA19-9) and neutrophil-to-lymphocyte ratio (NLR). We also collected the data on the treatment and chemotherapy regimens. This study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Fukuchiyama City Hospital.

Assessment of ascites and overall survival

The degree of ascites was assessed using computed tomography at diagnosis and was classified as none, small (within the pelvic cavity), moderate (beyond the pelvic cavity), or massive (extending throughout the abdominal cavity), based on the classification used in previous studies [7, 9, 10]. We divided the patients into those with ascites and those with moderate or massive ascites. The overall survival (OS) rate was evaluated from the date of computed tomography examination to the last follow-up date or date of death.

Uni- and multivariate Cox proportional hazards analyses were conducted to identify predictors of OS in patients with advanced gastric cancer. The candidates were as follows; age, sex, ECOG-PS, macroscopic type, histological type, HER2 status, liver metastasis, bone metastasis, ascites, moderate or massive ascites, ALP, LDH, CEA, CA19-9, NLR, and chemotherapy. We compared the clinical features of patients with moderate or massive ascites and those without moderate or massive ascites.

Statistical analysis

Statistical analysis was performed using the IBM SPSS Statistics 27 (IBM Japan, Tokyo, Japan). Statistical significance was set at P less than 0.05. Continuous variables are presented as medians and ranges, and comparisons were conducted using the Mann-Whitney U test. Categorical variables are expressed as numbers and percentages, and comparisons were performed by use of the chi-square test. The OS rate was evaluated using Kaplan-Meier survival curves and the log rank tests. Cox proportional hazards model analysis was used to estimate hazard ratio (HR) and 95% confidence interval (CI). Significant variables in the univariate analysis were included in the multivariate analysis.

Clinicopathological characteristics of advanced gastric cancer

Table 1 presents the clinicopathological characteristics. The median age was 73, and the proportion of male was 66.9%. The median follow-up period was 232.5 days, and 112 patients (90.3%) died. The ratio of Borrmann type III or IV in the macroscopic type was 51.6%. Regarding histological type, the percentage of the intestinal type was 45.2%, while that of the diffuse type was 53.2%. In this study, 43.5% of the patients had ascites of whom 20.2% had moderate or massive ascites.

Table 1

Clinicopathological characteristics of advanced gastric cancer
Age (years), median (range)	73	(31–97)
Sex, n (%)
Female	41	(33.1)
Male	83	(66.9)
ECOG-PS, n (%)
0 or 1	96	(77.4)
2 or above	27	(21.8)
Unknown	1	(0.8)
Follow-up period (days), median (range)	232.5	(5–2656)
Deaths during follow-up period, n (%)	112	(90.3)
Macroscopic type, n (%)
Borrmann type III or IV	64	(51.6)
Others	60	(48.4)
Location, n (%)
Upper	40	(32.3)
Middle	43	(34.7)
Lower	41	(33.1)
Histological type, n (%)
Intestinal	56	(45.2)
Diffuse	66	(53.2)
Others	2	(1.6)
HER2 status, n (%)
Negative	71	(57.3)
Positive	10	(8.1)
Unknown	43	(34.7)
Liver metastasis, n (%)
Absent	74	(59.7)
Present	50	(40.3)
Bone metastasis, n (%)
Absent	119	(96.0)
Present	5	(4.0)
Ascites, n (%)
Absent	70	(56.5)
Present	54	(43.5)
Moderate or massive ascites, n (%)
Absent	99	(79.8)
Present	25	(20.2)
ECOG-PS Eastern Cooperative Oncology Group Performance Status
HER2 human epidermal growth factor receptor 2

Table 2 presents the laboratory findings and treatment pattern of patients with advanced gastric cancer. Regarding tumor markers, the median CEA level was 5.4 ng/mL, whereas the median CA19-9 level was 34.6 ng/mL. For the inflammatory markers, the median NLR was 3.91. Regarding treatment, 40 patients (32.3%) received best supportive care, 84 (67.7%) underwent chemotherapy. As for first-line chemotherapy regimen, 38 (30.6%) patients received cisplatin-based chemotherapy, 30 (24.2%) received oxaliplatin-based chemotherapy, 9 (7.3%) received fluoropyrimidine monotherapy, 5 (4.0%) received taxane-based chemotherapy, while 2 (1.6%) did in other institutions.

Table 2

Laboratory findings and treatment in advanced gastric cancer patients
Laboratory findings, median (range)
White blood cell (/µL)	7025	(3560–47500)
Hemoglobin (g/dL)	10.75	(3.5–17.8)
Platelet (10⁴/µL)	26.6	(11.8–69.6)
Total protein (g/dL)	6.4	(4.6–8.5)
Albumin (g/dL)	3.4	(1.9–4.5)
ALP (IU/L)	267	(116–3186)
LDH (IU/L)	202.5	(122–1266)
CRP (mg/dL)	1.15	(0.01–36.9)
CEA (ng/mL)	5.4	(0.7–7827.1)
CA19-9 (U/mL)	34.6	(2.0–120000)
NLR	3.91	(1.20–36.69)
Treatment, n (%)
Best supportive care	40	(32.3)
First-line chemotherapy	84	(67.7)
Cisplatin-based chemotherapy	38	(30.6)
Oxaliplatin-based chemotherapy	30	(24.2)
Fluoropyrimidine monotherapy	9	(7.3)
Taxane-based chemotherapy	5	(4.0)
Unknown	2	(1.6)
ALP alkaline phosphatase; LDH lactate dehydrogenase
CRP C-reactive protein; CEA carcinoembryonic antigen
CA19-9 carbohydrate antigen 19 − 9; NLR neutrophil to lymphocyte ratio

Clinical outcomes with respect to ascites

Figure 1 shows the OS with respects to ascites. The median OS were 294.0 days (95% CI, 182.0–406.0 days) in patients without ascites, and 136.0 days (95% CI, 17.3–254.7 days) in patients with ascites. The cumulative one year, and two year OS rates in patients without ascites were 43.5%, and 20.2%, respectively, whereas those in patients with ascites were 29.1%, and 13.6%, respectively (P = 0.116; Fig. 1a). The median OS were 289.0 days (95% CI, 204.0–374.0 days) in patients without moderate or massive ascites, and 127.0 days (95% CI, 3.0–251.0 days) in patients with moderate or massive ascites. The cumulative one year, and two year OS rates in patients without moderate or massive ascites were 39.5%, and 20.9%, respectively, whereas those in patients with moderate or massive ascites were 28.0%, and 4.0%, respectively, (P = 0.027; Fig. 1b).

Predictors of overall survival in patients with advanced gastric cancer

Table 3 shows the predictors of OS in patients with advanced gastric cancer. In univariate analysis, age ≥ 80 (HR, 2.243; 95% CI, 1.503–3.347; P < 0.001), ECOG-PS ≥ 2 (HR, 3.277; 95% CI, 2.049–5.238; P < 0.001), diffuse type (HR, 1.551; 95% CI, 1.051–2.289; P = 0.027), moderate or massive ascites (HR, 1.650; 95% CI, 1.053–2.586; P = 0.029), ALP > 321 (HR, 1.569; 95% CI, 1.053–2.336; P = 0.027), LDH > 245 (HR, 1.535; 95% CI, 1.039–2.267; P = 0.031), NLR > 5 (HR, 2.187; 95% CI, 1.479–3.232; P < 0.001), and chemotherapy (HR, 0.145; 95% CI, 0.091–0.231; P < 0.001) were determined to be predictive factors. In multivariate analysis, diffuse type (HR, 1.532; 95% CI, 1.002–2.343; P = 0.049), moderate or massive ascites (HR, 2.153; 95% CI, 1.301–3.564; P = 0.003), and chemotherapy (HR, 0.189; 95% CI, 0.101–0.352; P < 0.001) were significant predictive factors for OS.

Table 3

Predictors of overall survival in patients with advanced gastric cancer
	Univariate analysis			Multivariate analysis
	HR	95% CI	P	HR	95% CI	P
Age, year
80 or above	2.243	1.503–3.347	< 0.001	1.387	0.817–2.353	0.226
Sex
Male	0.775	0.524–1.145	0.200
ECOG-PS
2 or above	3.277	2.049–5.238	< 0.001	1.661	0.987–2.797	0.056
Macroscopic type
Borrmann type III or IV	1.387	0.952–2.022	0.089
Histological type
Diffuse	1.551	1.051–2.289	0.027	1.532	1.002–2.343	0.049
HER2 status
Positive	0.961	0.490–1.885	0.909
Liver metastasis
Present	0.951	0.647–1.396	0.796
Bone metastasis
Present	2.250	0.894–5.663	0.085
Ascites
Present	1.351	0.926–1.969	0.118
Moderate or massive ascites
Present	1.650	1.053–2.586	0.029	2.153	1.301–3.564	0.003
ALP
>321	1.569	1.053–2.336	0.027	1.722	0.984–3.015	0.057
LDH
>245	1.535	1.039–2.267	0.031	1.184	0.716–1.957	0.511
CEA
>5	1.001	0.676–1.483	0.996
CA19-9
>37	1.072	0.722–1.593	0.729
NLR
>5	2.187	1.479–3.232	< 0.001	1.338	0.863–2.074	0.194
Chemotherapy
Present	0.145	0.091–0.231	< 0.001	0.189	0.101–0.352	< 0.001
ECOG-PS Eastern Cooperative Oncology Group Performance Status
HER2 human epidermal growth factor receptor 2; ALP alkaline phosphatase
LDH lactate dehydrogenase; CEA carcinoembryonic antigen
CA19-9 carbohydrate antigen 19 − 9; NLR neutrophil to lymphocyte ratio

Clinical features of patients with moderate or massive ascites and those without moderate or massive ascites

Table 4 shows comparative clinical features between patients with moderate or massive ascites and those without it. Gastric cancer showing Borrmann type III or IV was significantly higher in those with moderate or massive ascites compared with those without moderate or massive ascites (76.0% vs 45.5%, P = 0.012). In contrast, no significant differences were observed regarding age, sex, ECOG-PS, tumor location, histological type, and HER2 status. Regarding laboratory findings, hemoglobin concentration was significantly higher in the patients with moderate or massive ascites than those without moderate or massive ascites (12.3 g/dL vs 10.4 g/dL, P = 0.020). Furthermore, the serum CEA level was significantly lower in patients with moderate or massive ascites than those without moderate or massive ascites (3.4 ng/dL vs 7.3 ng/dL, P = 0.020). As for chemotherapy, the presence or absence of treatment with first- and second-line chemotherapy was not significantly different.

Table 4

Clinical features of patients with moderate or massive ascites and those without moderate or massive ascites
	Patients without moderate or massive ascites		Patients with moderate or massive ascites		P
Age (yeas), median (range)	73	(31–97)	72	(31–90)	0.527
Sex, n (%)
Female	32	(32.3)	9	(36.0)	0.911
Male	67	(67.3)	16	(64.0)
ECOG-PS, n (%)
0 or 1	78	(79.6)	18	(72.0)	0.584
2 or above	20	(20.4)	7	(28.0)
Macroscopic type, n (%)
Borrmann type III or IV	45	(45.5)	19	(76.0)	0.012
Others	54	(54.5)	6	(24.0)
Location, n (%)
Upper	29	(29.3)	11	(44.0)	0.336
Middle	35	(35.4)	8	(32.0)
Lower	35	(35.4)	6	(24.0)
Histological type, n (%)
Intestinal	49	(50.0)	7	(29.2)	0.108
Diffuse	49	(50.0)	17	(70.8)
HER2 status
Negative	58	(87.9)	13	(86.7)	1.000
Positive	8	(12.1)	2	(13.3)
Laboratory findings
White blood cell	6840	(3560–47500)	7770	(4140–14750)	0.130
Hemoglobin	10.4	(3.5–17.8)	12.3	(5.4–17.2)	0.020
Platelet	26.0	(11.8–69.6)	27.3	(12.4–67.0)	0.711
Total protein	6.4	(4.6–8.5)	6.5	(5.2–7.9)	0.165
Albumin	3.4	(1.9–4.5)	3.2	(1.9–4.5)	0.456
ALP	280	(118–3186)	253	(116–3124)	0.581
LDH	202	(122–1266)	203	(156–831)	0.560
CRP	0.69	(0.01–18.51)	2.63	(0.01–36.90)	0.073
CEA	7.3	(0.7–7827.1)	3.4	(0.7–6816.0)	0.019
CA19-9	36.85	(2.0–120000)	24.5	(2.1–51486.7)	0.908
NLR	3.6	(1.2–36.7)	6.0	(1.2–29.4)	0.054
First-line chemotherapy
Absent	31	(31.3)	9	(36.0)	0.835
Present	68	(68.7)	16	(64.0)
Second-line chemotherapy
Absent	18	(26.5)	5	(31.3)	0.523
Present	45	(66.2)	11	(68.8)
Unknown	5	(7.4)	0	(0.0)
ECOG-PS Eastern Cooperative Oncology Group performance status
HER2 human epidermal growth factor receptor 2; ALP alkaline phosphatase
LDH lactate dehydrogenase; CRP C-reactive protein; CEA carcinoembryonic antigen
CA19-9 carbohydrate antigen 19 − 9; NLR neutrophil to lymphocyte ratio

In this study, we assessed clinicopathological factors, including the degree of ascites, to determine predictive factors in patients with advanced gastric cancer. The OS of patients with moderate or massive ascites was significantly lower than that of patients without moderate or massive ascites. Furthermore, multivariate analysis revealed that diffuse type, moderate or massive ascites, and chemotherapy were pivotal prognostic factors for OS. Collectively, we observed that moderate or massive ascites could influence OS in patients with advanced gastric cancer in a clinical setting.

Previous studies have shown that the presence of ascites or peritoneal metastases are pivotal prognostic factors in patients with advanced gastric cancer who are undergoing chemotherapy [11–13]. A prognostic index consisting of the ECOG-PS, number of metastatic sites, prior gastrectomy, and serum ALP level has been established and validated in advanced gastric cancer using phase III study data [14, 15]. In clinical settings, patients with advanced gastric cancer who occasionally present with massive ascites cannot receive systemic chemotherapy because of impaired activities of daily living or inadequate oral intake. Absence of chemotherapy, in addition to malignant ascites itself, may worsen the outcomes of such patients. Accordingly, our aim was to evaluate the prognostic factors of advanced gastric cancer, including patients who did not receive chemotherapy.

We determined that age ≥ 80, ECOG-PS ≥ 2, diffuse type, moderate or massive ascites, elevated ALP, elevated LDH, elevated NLR, and no chemotherapy were poor prognostic factors in the univariate analysis. Patient characteristics, such as age and ECOG-PS score, have been identified as the significant prognostic factors in previous studies [11–16]. We determined the diffuse type as a poor prognostic factor, similarly to a previous study [17]. Prognostic scoring models have revealed that peritoneal metastasis and malignant ascites in advanced gastric cancer are pivotal parameters for predicting OS [11–13, 16]. In contrast, another study showed that peritoneal metastasis is not associated with OS [14]. The study was performed using the clinical trial data, in which patients with ascites beyond the pelvic cavity were excluded [18]. This may explain why peritoneal metastasis could not influence OS in the study. However, we encountered patients with abdominal distention due to ascites in the clinical setting. Indeed, 20.2% of patients presented with moderate or massive ascites in this study. Our results imply that that moderate or massive ascites could be a more effective prognostic factor than ascites alone. Serum ALP level has been reported to be a predictive factor of OS in previous studies [11–15, 17], and serum LDH level was also a prognostic factor in some studies [16, 17]. The NLR, an inflammatory biomarker, has been recognized as a prognostic factor for solid tumors, including gastric cancer [17, 19, 20]. Collectively, our data suggest that ALP, LDH, and the NLR may be useful in predicting OS in patients with advanced gastric cancer, as previously reported.

Diffuse type, moderate or excessive ascites, and chemotherapy were the pivotal prognostic factors in multivariate analysis. These findings imply that moderate or massive ascites at diagnosis could influence the OS in patients with advanced gastric cancer. In this study, the ECOG-PS or the ratio of patients undergoing first- and second-line chemotherapy did not differ between patients with moderate or massive ascites and those without moderate or massive ascites. In contrast, the NLR and CRP levels tended to be higher in patients with moderate or massive ascites, suggesting carcinomatous peritonitis. Collectively, the poor OS in patients with moderate or massive ascites may be due to systemic inflammation caused by carcinomatous peritonitis. In addition, we determined that the proportion of the macroscopic type showing Borrmann type III or IV was higher in patients with moderate or massive ascites. A previous study revealed that the macroscopic type III or IV was a pivotal factor in detecting peritoneal metastases in gastric cancer [21]. These findings imply that the macroscopic type was associated with the formation of peritoneal metastases.

This study had some limitations. First, this was conducted at a single center with a retrospective design; thus, a multicenter prospective study is needed to ascertain our findings. Second, all cases with ascites were not be proven to have peritoneal metastases on histological examination. Indeed, peritoneal metastases were not confirmed by histological examinations in five of 25 cases showing with moderate or excessive ascites, although peritoneal metastases were clinically diagnosed. Third, only Japanese patients with advanced gastric cancer were registered. Therefore, these results should be validated in other populations.

Using real-world data, our study determined that moderate or massive ascites at diagnosis could influence OS in advanced gastric cancer.

Acknowledgements The authors thank all members of the Department of Gastroenterology and Hepatology, Fukuchiyama City Hospital, and all members of the Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine.

Author contributions All authors contributed to the study conception and design. Data collection and analysis were performed by Naoto Iwai, Tomoya Ohara, Takashi Okuda, Kohei Oka, Hiroaki Sakai, Mariko Kajiwara-Kubtota, Toshifumi Tsuji, and Junichi Sakagami. All analyses were supervised by Keizo Kagawa, Toshifumi Doi, Ken Inoue, Osamu Dohi, Naohisa Yoshida, Kazuhiko Uchiyama, Takeshi Ishikawa, Tomohisa Takagi, Hideyuki Konishi, and Yoshito Itoh. The first draft of the manuscript was written by Naoto Iwai and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Funding This work was supported by a Grant-in-Aid for Early-Career Scientists from the Japanese Society for the Promotion of Science KAKENHI (grant no. 22K16051) to Naoto Iwai.

Conflicts of interest All authors declare no competing interests.

Ethics approval This study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Fukuchiyama City Hospital.

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Prognostic value of moderate or massive ascites in patients with advanced gastric cancer

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Abstract

Background

Methods

Results

Conclusion

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Introduction

Patients and Methods

Patients

Assessment of ascites and overall survival

Statistical analysis

Results

Clinicopathological characteristics of advanced gastric cancer

Clinical outcomes with respect to ascites

Predictors of overall survival in patients with advanced gastric cancer

Discussion

Declarations

References

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