Summary of findings and interpretation
We observed a socioeconomic trend in the receipt of major resection favouring the most affluent patients for stages II and III cancer but it was not statistically significant (p > 0.05). Patients with older age, left-sided colon, non-adenocarcinoma, a higher number of comorbidities and non-obese groups had higher odds of not undergoing resection when compared with the reference group. Patients with emergency presentation had approximately 40% lower odds of not receiving resection.
We also found that the percentage of patients undergoing urgent surgery was higher in the deprived groups than in the most affluent group; seemingly, the waiting time target of providing treatment within 31 days of diagnosis was achieved more in the deprived groups. The mean time to surgical treatment was approximately 38 days when the patients undergoing urgent surgery were removed. No socioeconomic disparities were observed for the time to treatment when patients were confined to those undergoing elective surgery. Patients with non-adenocarcinoma or having 2+ comorbidities experienced a longer time to treatment than patients with adenocarcinoma or those with no comorbidities.
There were no clear socioeconomic differences in the receipt of major resection. However, cautious interpretation is needed. Among patients with stage I or IV cancer, not undergoing major resection does not necessarily mean inappropriate care. For some patients with stage I cancer, having only an endoscopic resection (e.g. endoscopic mucosal resection or endoscopic submucosal dissection) alone can be a sufficient treatment option intending cure. There was no information on whether the stage I patients had unfavourable histological findings, and data regarding why major resection was not performed were mostly missing. Similarly, for patients with stage IV, there was little information on why major resection was not performed. In stage IV, indication for the major resection of the primary lesion largely depends on clinical factors (e.g. performance status, the severity of obstruction or bleeding symptoms, whether the patient reacted to chemotherapy aiming conversion therapy and the extent of metastasis to other organs) that are not fully captured in the population data. Neither palliative nor curative intent was clear among the patients with stage IV cancer. Misclassification of the outcome could occur because of the aforementioned reasons. At this point, therefore, the results may only be interpreted with certainty for patients with stage II or III cancer, who have the potential to be cured if treated appropriately.
As the cancer locates more distal, the odds of not receiving resection increased. For some reason, right-sided colon cancers were selected for resection. One potential reason is that the patients with more distal cancer may be diagnosed with more obvious symptoms such as obstruction. These patients may have died immediately after the diagnosis, before undergoing resection. Similarly, patients with higher tumour grades (G3/G4) may have died before resection because their tumours were more aggressive than those of lower grades (G1/G2). While patients with 2+ chronic comorbidities had more than three times higher odds of not undergoing resection compared with those without chronic comorbidities, patients with 2+ acute comorbidities had only twice the odds of not receiving resection compared with those without acute comorbidities. Chronic comorbidities, which we confined to ten comorbidities with irreversible damages of vital organs, may have affected the decisions regarding treatment more importantly than the acute comorbidities. Instead, patients with a higher number of chronic comorbidities might be more likely to die before resection. This situation may also imply that current care lacks proper guidelines for the simultaneous management of chronic multimorbidity [18]. Another possible explanation is that patients with a larger number of acute comorbidities rather reflect the receipt of appropriate care. They may have received thorough screenings for other diseases, such as underlying cancer, and were therefore diagnosed and operated for the colon cancer.
Regarding time to treatment, we found no socioeconomic variations in the number of days from diagnosis to resection for all stages when patients were restricted to those with elective surgery. Socioeconomic differences in time to treatment have been investigated in many other studies [19-26]. However, the reported outcome varies by study (e.g. outcomes shown in days, hazard ratios or odds ratios at a certain cut-off-time). The definition of the treatment (e.g. any treatment, major resection only, chemotherapy or radiotherapy) also differs by study. As in line with the previous reviews on time to treatment [27, 28], there is a wide diversity in the definition of ‘delay’.
Our study demonstrated that one of the waiting time targets, providing treatment within 31 days of diagnosis, was achieved in higher proportions among the deprived groups as with a larger proportion of more deprived patients undergoing urgent surgery. Considering that the presence of emergency presentation confounded urgent surgery, achievement in the waiting time target may not necessarily reflect a high quality of cancer care.
One systematic review identified an equivocal association between time to treatment and survival [27]. We did not examine this association in the present study. However, like a previous report [29], persistent socioeconomic inequalities in survival, alongside our findings of no socioeconomic variation in time to treatment for patients with elective surgery, may suggest that achieving some waiting time targets is not related to better survival. Rather, a noteworthy point in assessing colon cancer care might be the high number of deprived patients experiencing emergency presentation and urgent surgery. It is known that health-seeking behaviours, screening uptake and access barriers to healthcare may influence emergency presentation [28, 30]. Some up-stream factors are not easily modifiable but improving access to healthcare system may reduce the emergency presentation. Evidence suggests that emergency presentation is low in screening participants [31] and that screening uptake is low amongst deprived groups [32]. The situation observed here might be because of the ‘inverse equity law’ [33]. Low screening uptake in the deprived groups may be partly attributable to the high emergency presentation amongst the population and, subsequently, to poorer survival [34, 35]. Another potential barrier in healthcare access could be quality postoperative care. Deprived groups tend to have worse short-term postoperative mortality [36, 37]. However, when provided care was equalised for all SES groups, a socioeconomic gap in survival was not observed [38]. These findings support our hypothesis that the survival gap may be partly explained by access inequalities in cancer care, particularly the postoperative care. Deprived patients may be referred to hospitals with less specialised or less experienced doctors and may therefore suffer from poorer survival. Future studies should focus on identifying the bottleneck of care through decomposing patient pathways to modify access inequalities.
Strength and limitations
The strength of our study is that, through the use of the national cancer registry data linked with clinical information from HES, we provided an overall picture of how patient factors (age, sex and comorbidities) and tumour factors (site, stage, histology and tumour grade) interacts with the performance of healthcare system at the national level. Our analyses also included crucial tumour factors, i.e. not only stage but also histology and tumour grades. One limitation is that the difference by SES for some histological types (mucinous, signet-cell carcinoma versus other adenocarcinomas) was not explored. This was because the majority were recorded without detailed histological information (i.e. recorded as adenocarcinoma), and 12.6% of the total cases were recorded as having neoplasm or carcinoma. Patients with histological types of neoplasm or carcinoma were grouped into patients with adenocarcinoma under the assumption that the majority of the colon cancer cases are likely to have adenocarcinoma. Thus, misclassification may exist.
For the first analysis, other potential outcomes that may reflect the performance of a healthcare system are the percentage of patients who received major resection for curative intent, the number of lymph nodes yielded, postoperative complications or failure-to-rescue rate [25, 39-45]. These measures were not used because the missingness was substantial for those outcomes.
When analysing time to treatment, patients who received urgent surgery were removed. The urgent surgery was defined as an operation performed within seven days of diagnosis. This cut-off in days may be arbitrary, but while the patients receiving resection within three days of diagnosis exceeded 29% of those who received resection, only 2.1% underwent resection four to seven days from the date of diagnosis. Therefore, the cut-off of the number of days with which an urgent surgery is defined is considered to make little change in the results.
Another limitation is that our study did not consider random effects due to a 10% missingness in hospital information. Both receipt of resection and time to treatment may be affected by differences in patient characteristics, which are also likely to vary among hospitals.
Although there was no socioeconomic difference in the time from diagnosis to treatment, the time from recognition of symptoms to diagnosis could be longer in the deprived groups due to differences in health-seeking behaviour. Time to diagnosis, otherwise called the ‘appraisal interval’ and ‘help-seeking interval’ [28], was not incorporated in our analysis. These time lengths may differ by SES and could lead to socioeconomic inequalities in survival.
Implication for cancer policy
We found no socioeconomic differences in the receipt of resection for all patients with colon cancer. However, a more substantial proportion of patients in the deprived groups seemed to have undergone emergency presentation and urgent surgery than the most affluent group. The paradox for observing no socioeconomic variation in receiving resection is that the emergency presentation worked protective against the failure to receive resection. The presence of emergency presentation also worked positively for achieving the waiting time target of treatment within 31 days of diagnosis. Time from diagnosis to treatment was equally distributed among different SES groups only if patients were limited to those with elective surgery. Identification of other potential reasons for survival inequalities is needed, particularly focusing on what happens before and after patients receive resection. Examples include an investigation into access before diagnosis to reduce high emergency presentation and urgent operation, an assessment of the quality of postoperative care by SES, such as an exploration of complication rates or failure-to-rescue rates by SES, and inspection of within and between-hospital variations in these outcomes. Further evaluation of the receipt of treatment, such as differences in the receipt of chemotherapy and radiotherapy by SES, may also be worth investigating.