Introduction

Many reports have observed that hospital factors along with various patient and surgeon factors affect the short-term and long-term outcomes of patients undergoing surgery for colorectal cancer [1, 2]. Hospital volume is the best known example of a hospital factor [3, 4]. Patients with stage IV colorectal cancer need support from various medical professionals with diverse backgrounds and skills, including colorectal surgeons, medical oncologists, radiologists, and palliative care physicians. Accordingly, their prognosis is possibly influenced by many factors [5–8]. However, little is known regarding the hospital factors that may affect the prognosis of patients with incurable colorectal cancer. Therefore, in this study, we assessed certain hospital factors that potentially affected the prognosis of patients with stage IV colorectal cancer who underwent palliative primary tumor resection.

Materials and methods

Patients

The Japan Society of Laparoscopic Colorectal Surgery (JSLCS) retrospectively collected data on 968 patients with stage IV colorectal cancer who underwent palliative tumor resection at 41 participating hospitals between January 2006 and December 2007. All surgeons were experienced in laparotomy, and most of them performed over 100 laparoscopic surgeries [9]. From the 968 patients, we excluded 37 patients who had active cancer in other organs, 5 patients with a performance status of 4, 51 patients who underwent emergency operation, and 23 patients who underwent insufficient lymph node dissection (D0 or D1). We included only patients undergoing D2 or D3 lymph node dissection. The scope of lymph node dissection was classified between D0 and D3 according to guidelines from the Japanese Society for Cancer of the Colon and Rectum [10]. D2 lymph node dissection indicates the removal of pericolic and intermediate lymph nodes, and D3 involves removal of pericolic, intermediate, and main lymph nodes around the root of the regional artery. Hepatic and peritoneum metastases were distinguished from distant metastasis according to Japanese classification [10]. Finally, 853 patients who underwent elective palliative tumor resection with sufficient scope of lymph node dissection were included in the analyses.

Hospital factors

This study included 41 hospitals that participated in the JSLCS study. We focused on three hospital factors, namely hospital type (university hospital, cancer center, or community hospital), hospital volume, and number of colorectal surgeons. In Japan, university hospitals and cancer centers play a leading role in cancer care, and we divided the hospitals into the following two groups according to the hospital type: (1) group A, which included university hospitals and cancer centers, and (2) group B, which included community hospitals. Hospital volume was defined as the average annual number of colorectal cancer patients who underwent surgery in each institution.

Statistical analysis

Continuous variables were compared by Student’s t test. Categorical valuables were compared by Fisher’s exact test. Survival analyses were performed with Kaplan-Meier estimates, and they were compared by the log-rank test. Multivariate analysis was performed using the Cox proportional hazards model. Overall survival (OS) was defined as the time between the date of primary tumor resection and the date of death. All p values were two-sided, and p values less than 0.05 were considered statistically significant. All statistical analyses were performed using JMP Statistical Software Version 11 (SAS-Institute Inc., Cary, NC).

Results

The clinicopathological characteristics of the 853 patients are shown in Table 1, and the characteristics of the 41 participating hospitals are described in Table 2. Groups A and B comprised 28 and 13 institutions, respectively, and the numbers of patients treated in each hospital group were 626 and 227, respectively. Hospital volume was classified into two categories of ≥200 and <200 operations/year, with 10 institutions (350 patients) and 31 institutions (503 patients) classified into the respective categories. The number of colorectal surgeons in each institute was divided into two categories of ≥5 and <5, with 20 institutions (396 patients) and 21 institutions (457 patients) classified into the respective categories.

Table 1 Patient background characteristics
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Table 2 Hospital characteristics
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Among patient factors, age, tumor depth, regional lymph node metastasis, hepatic metastasis, peritoneal metastasis, distant metastasis, tumor location, surgical approach, scope of lymph node dissection, preoperative intestinal stenosis, carcinoembryonic antigen (CEA), carbohydrate 19–9 (CA19-9), American Society of Anesthesiologists - Physical Status (ASA-PS) score, and postoperative chemotherapy were significantly associated with OS (Table 3). Among hospital factors, only hospital type was significantly associated with OS, and OS was significantly higher in the group A hospitals than in the group B hospitals (median survival time: 772 vs. 616 days, p = 0.034) (Fig. 1). The other hospital factors—hospital volume and number of colorectal surgeons—were not associated with OS (Table 4). In multivariate analysis, hospital type remained significantly associated with OS even after adjusting for patient factors (Table 5).

Table 3 Patient factors associated with overall survival
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Fig. 1
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Overall survival of patients stratified by hospital type

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Table 4 Hospital factors associated with overall survival
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Table 5 Factors associated with overall survival
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Short-term outcomes after primary tumor resection were compared between the group A and B hospitals; these results are shown in Table 6. There were no significant differences between the two groups in terms of resumption of oral intake, length of postoperative hospital stay, conversion from laparoscopic to open surgery, intraoperative complications, or postoperative complications (National Cancer Institute Common Terminology Criteria for Adverse Events v3.0 ≥ grade 2).

Table 6 Short-term outcomes
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Discussion

Outcomes of patients with colorectal cancer are believed to be influenced by hospital factors as well as tumor, patient, and surgeon factors [1, 2]. Many reports have described an effect of hospital volume on both short-term and long-term outcomes in patients with colorectal cancer [3, 4]. Recently, hospital type has been focused on as an influential factor in various disease groups, such as pediatric disease, urologic cancer, breast cancer, and hepatocellular carcinoma [11–14]. With respect to colorectal cancer, Elferink et al. [15] reported that different hospital types showed significant differences in treatment and long-term outcomes. The treatment of incurable stage IV colorectal cancer shows greater diversity than that of other, curable stages because these patients are treated with multimodality therapy, including medical oncology, radiology, and symptomatic palliative care [6]. Therefore, the survival of patients with stage IV colorectal cancer is expected to be highly influenced by hospital factors. However, little is known regarding the impact of hospital type on the prognosis of patients with stage IV colorectal cancer. In this study, we examined several hospital-related factors, and only hospital type was significantly associated with prognosis, while hospital volume and number of colorectal surgeons were not.

Regarding the reason for better OS in the group A hospitals than in the group B hospitals, we consider that the main difference is the number and variety of cancer specialists apart from surgeons. In Japan, university hospitals and cancer centers (group A hospitals) have many specialists from various fields who are actively involved in cancer care, as compared with community hospitals (group B), which have fewer cancer specialists. Specialized cancer care has been reported to improve outcomes in various cancers, including colorectal cancer, breast cancer, and ovarian cancer [16]. In particular, systemic chemotherapy has been reported to improve survival in patients with incurable colorectal cancer [17, 18], but there are considerable variations in the administration of chemotherapy across hospitals [19]. Japan has faced a chronic shortage of medical oncologists, similar to many other countries [20, 21]. In the present study period (2006–2007), more intensive and toxic chemotherapy, such as FOLFOX and FOLFORI, were introduced into clinical practice in Japan, leading to a greater need for medical oncologists specialized in colorectal cancer chemotherapy. In this study, postoperative chemotherapy significantly improved OS (p < 0.001), but there was no significant difference between group A and B hospitals in the proportion of patients who received postoperative chemotherapy (84.0 vs. 80.6 %, p = 0.174). Therefore, the management of chemotherapy by the oncologists might affect patients’ prognosis. An inhomogeneous distribution of such specialists across hospitals might contribute to the prognostic differences between group A and B hospitals.

Supportive care is also an essential factor in cancer care. Such care is reported to improve the patients’ condition and can help in continuing cancer therapy [7, 8]. Although it is difficult to assess the quality of supportive care, it has been reported that there might be large disparities between hospitals [22]. Higher quality supportive care in group A hospitals might improve the postoperative prognosis of patients with stage IV colorectal cancer who undergo palliative primary tumor resection.

On the other hand, we did not observe any differences between the hospital types in short-term outcomes, including postoperative complication rates and length of hospital stay, which are well-known indicators of the quality of curative colorectal surgery. A possible explanation for this finding is that our study only included hospitals with experienced specialists in colorectal surgery, and so the quality of surgery did not differ by hospital type. Further, in the management of patients with incurable colorectal cancer, the impact of the primary cancer surgery on patient survival might be relatively small compared with the impact of multimodality treatment [23, 24].

This study has some limitations, including its retrospective nature and a possible selection bias, although we made adjustments to minimize the effects of both surgeon factors and patient diversity. Therefore, it may be difficult to generalize our findings. Another limitation is that we lacked information on the patients’ comorbidities and details of postoperative therapies. These factors might influence patient outcomes, but we made best effort to minimize the effect of disease other than colorectal cancer by excluding the patients with insufficient lymph node dissection, which was often performed in patients with severe comorbidities. Despite these limitations, we believe that the results of this study help in resolving medical inequality across hospitals.

In conclusion, hospital type was identified as a significant prognostic factor for OS in patients with stage IV colorectal cancer undergoing palliative primary tumor resection.