Epidemiology and prognostic analysis of patients with pancreatic signet ring cell carcinoma: a population-based study | BMC Gastroenterology

Demographic and clinicopathologic characteristics

In this study, a total of 585 eligible patients with PSRCC were identified. The clinical features of the patients are presented in Table 1. The median age was 67 years. The male-to-female ratio in this study was 1.25:1, with 325 (55.6%) male patients and 260 (44.4%) female patients. White patients account for 82.7% of the population. Of 585 patients, 383 (65.5%) patients had a record of available tumour size. Among the known records, 43.6% of the tumours were > 4 cm and 56.4% were ≤ 4 cm. The most common grade of differentiation was III/IV, accounting for 87.9%, while grade I/II accounted for 12.1%.

Table 1 The clinical features of the patients with pancreatic signet ring cell carcinoma (PSRCC)

At diagnosis, 70% of patients had distant metastatic disease. Chemotherapy, which accounts for 45% of PSRCC treatment, is the initial treatment option for patients. One hundred (17.2%) patients underwent surgery, while 80 (13.7%) patients received radiation therapy. When presented in summary stages, details of treatment are presented in Table 2. Of 170 patients with localised/regional disease, 78 (45.9%) underwent primary surgery, 87 (51.2%) received chemotherapy and 54 (31.8%) received radiotherapy.

Table 2 The clinical features of the patients with pancreatic signet ring cell carcinoma (PSRCC) according to stratification by summary stage

Age-adjusted incidence

Table 3 summarises the age-adjusted incidence rates for common clinical features. The overall annual incidence of PSRCC within the SEER-18 database was 0.349 (95% CI, 0.321–0.379) per million population between 2000 and 2018. The age-adjusted incidence rates are higher in men than in women, higher in Black patients than in other races and tumours in the head of the pancreas are more common between 2000 and 2009. As presented in Fig. 1, the annual adjusted incidence rate decreased with time, from 0.48 per million in 2000 to 0.16 per million in 2018. Over the past few decades, there has been a significant decline in the incidence of PSRCC. The incidence of PSRCC increased significantly with age, especially in patients aged 55 and above, and gradually reduced after 70 years of age, peaked between the ages 75 and 79 years (2.12 per million) and gradually declined thereafter (Fig. 2). Similar results were observed when the incidence was grouped by sex (Fig. 3a). The changes in incidence rates by age across ethnic groups are presented in Fig. 3b. The incidence peaked earlier in Black patients than in White patients, with the first peak occurring between the ages of 65 and 69 for Black patients in a bimodal distribution and between the ages 75 and 79 for White patients. The incidence rate of Black patients was higher than that of other races (0.369 per million).

Table 3 The age-adjusted incidence of pancreatic signet ring cell carcinoma (PSRCC) in Surveillance, Epidemiology and End Results (SEER) 2000–2018
Fig. 1

The age-adjusted incidence of pancreatic signet ring cell carcinoma (PSRCC) from 2000 to 2018

Fig. 2
figure 2

The age-adjusted incidence rate of pancreatic signet ring cell carcinoma (PSRCC) in different age groups

Fig. 3
figure 3

The age-stratified incidence rates for different races and genders

Survival analysis

Subsequently, the age-adjusted survival rate was calculated using SEER*Stat software version 8.3.9 and is presented in Table 4. The 1-, 2- and 5-year observed survival rates were 20.1, 8.3 and 3.4%, respectively.

Table 4 Observed, expected and relative survival rates of pancreatic signet ring cell carcinoma (PSRCC) patients from 2000 to 2018

The log-rank test revealed that there may be a relationship between OS and the variables age at diagnosis (Fig. 4a), year of diagnosis (Fig. 4b), marital status (Fig. 4c), primary site (Fig. 4d), differentiation grade (Fig. 4e), summary stage (Fig. 4f), regional nodes status (Fig. 4g), tumour size (Fig. 4h), surgery (Fig. 4i), chemotherapy (Fig. 4j) and radiation (Fig. 4k). The stage has a great impact on the course of treatment. Therefore, the effectiveness of treatment in different summary stages was compared. The Kaplan–Meier survival curve stratified according to the therapy and summary stage are displayed in Fig. 5. Patients who underwent primary tumour surgery, chemotherapy and radiation had substantially improved OS (Fig. 5, P < 0.05).

Fig. 4
figure 4

Kaplan–Meier survival curves with statistically significant clinical features in patients with pancreatic signet ring cell carcinoma (PSRCC). age at diagnosis (a), year of diagnosis (b), marital status (c), primary site (d), differentiation grade (e), summary stage (f), regional nodes status (g), tumour size (h), surgery (i), chemotherapy (j), radiation (k)

Fig. 5
figure 5

Kaplan–Meier survival curves for patients with pancreatic signet ring cell carcinoma (PSRCC) based on the summary stage. a, c, e: based on localised/regional stage, a: surgery, c: chemotherapy, e: radiation (b, d, f): based on distant stage, b: surgery, d: chemotherapy, f: radiation

Specifically, compared with the reference group in univariate Cox analysis (Table 5), patients with older age (HR, 1.27; 95% CI, 1.07–1.50; P = 0.005), unmarried (HR, 1.31; 95% CI, 1.10–1.56; P = 0.002), grade III/IV disease (HR, 1.84; 95% CI, 1.25–2.72; P = 0.002), tumours not at the head of the pancreas (Body: HR, 1.47; 95% CI, 1.10–1.97; P = 0.009, Tail: HR, 1.29; 95% CI, 1.00–1.66; P = 0.048, Other: HR, 1.39; 95% CI, 1.01–1.93; P = 0.045) and larger tumour size (HR, 1.37; 95% CI, 1.11–1.69; P = 0.003) were associated with poor prognosis (HR > 1, P < 0.05) whereas patients with earlier stage (summary stage: localised/regional, HR, 0.44; 95% CI, 0.36–0.53; P < 0.001; regional nodes status: negative, HR, 0.71; 95% CI, 0.48–1.06; P = 0.097, no nodes examined, HR, 2.53; 95% CI, 1.98–3.24; P < 0.001) or treated with radiotherapy (HR, 0.45; 95% CI, 0.35–0.58; P < 0.001), chemotherapy (HR, 0.41; 95% CI, 0.35–0.49; P < 0.001) and surgery (HR, 0.31; 95% CI, 0.24–0.40; P < 0.001) were associated with favourable prognosis (HR < 1, P < 0.05). When these factors were incorporated in multivariate Cox regression, it was indicated that the summary stage, regional nodes status, surgery and chemotherapy were independent factors for patients with PSRCC.

Table 5 Univariate and multivariate regression analysis of overall survival (OS) in patients with pancreatic signet ring cell carcinoma (PSRCC)

Multiple imputation (MI) and sensitivity analysis

MI procedures were applied to account for missing data of some key variables in our study, and the results are presented in supplementary Table 1. Receiving surgery (HR, 0.40; 95% CI, 0.26–0.61; P < 0.001), chemotherapy (HR, 0.36; 95% CI, 0.30–0.44; P < 0.001, and an early stage at diagnosis (summary stage: localised/regional, HR, 0.62; 95% CI, 0.49–0.79; P < 0.001; regional nodes status: negative, HR, 0.65; 95% CI, 0.42–0.99; P = 0.046) remained associated with a better prognosis in multivariate Cox regression following MI. The most recent year of diagnosis (HR, 0.741; 95% CI, 0.619–0.886; P < 0.001) was also associated with a better prognosis, while unmarried patients (HR, 1.322; 95% CI, 1.092–1.601; P = 0.005) and older years (HR, 0.74; 95% CI, 0.62–0.89; P = 0.048) were associated with a worse prognosis.

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