Skip to main content
NCBI home page
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2023 Jan 11;31(2):110. doi: 10.1007/s00520-022-07572-8

Financial toxicity following surgical treatment for colorectal cancer: a cross-sectional study

Minghui Mo 1, Peipei Jia 2, Kai Zhu 2, Wenjing Huang 2, Li Han 2, Cuiping Liu 3,✉, Xia Huang 2,✉
PMCID: PMC9838282  PMID: 36629938

Abstract

Purpose

Financial toxicity has become a global public health issue. The purpose of the study is to investigate and analyze the influencing factors of financial toxicity in patients with non-metastatic colorectal cancer.

Methods

A convenient sample of 250 patients with stage I-III colorectal cancer was investigated in the study. They completed a set of questionnaires, including the Comprehensive Score for Financial Toxicity questionnaire, the Perceived Social Support Scale, and the Hospital Anxiety and Depression Scale. Univariate and multivariate linear regression were performed to investigate the influencing factors of financial toxicity.

Results

Over half (52.8%, n = 132) of the colorectal cancer survivors experienced financial toxicity. Multivariate regression analysis showed that the factors associated with financial toxicity were young age, unemployment, low annual household income, chemotherapy, and the lack of sufficient social support (p < 0.05).

Conclusions

Financial toxicity is common among non-metastatic colorectal cancer survivors. Young age, lower annual household income, unemployment, chemotherapy, and insufficient social support were associated with financial toxicity.

Keywords: Financial toxicity, Cross-sectional survey, Determinants, Colorectal cancer, Social support

Introduction

Colorectal cancer is the third most common cause of cancer death worldwide, with more than 1.90 million cases and 935,000 deaths yearly [49]. It is estimated that there will be 592,232 new cases of colorectal cancer in China by 2022, accounting for 12.3% of cancer cases [54]. Over the past few decades, considerable advancements have been achieved in diagnosing and treating colorectal cancer [28]. Moreover, recent progress in next-generation sequencing and high-throughput technologies is beneficial to uncovering the underlying mechanisms of diversified therapeutic regimens in colorectal cancer [33]. All of these have significant improvements in overall survival and clinical effects for patients [2, 48].

Nevertheless, the cost of these technological advances also has caused a growing burden on patients and entire healthcare systems. In the USA, the financial burden caused by colorectal cancer was as high as $14.1 billion, accounting for 5.5% of the total cost of health care [34]. Compared with other cancers, the direct financial burden of colorectal cancer has the highest growth rate in China [7], and the direct medical expenses of colorectal cancer reached 61,829 CNY (approximately $8,698) per case [23]. Financial toxicity has become a globally severe economic problem [1], especially in middle-income countries, including China, because of low government spending on public health, insurance coverage gaps, and high care cost. Medical insurance in China consists of basic medical insurance for urban workers, basic medical insurance for urban residents, and new rural cooperative medical care. At the end of 2018, China’s medical insurance participation rate reached 95%, covering 1.3 billion Chinese citizens [50]. Even though basic medical insurance has achieved universal coverage, uneven medical insurance coverage, unbalanced medical insurance reimbursement ratios, and expensive anticancer drugs still plague most cancer patients [8, 36].

The cost of cancer treatment can be divided into direct and indirect costs. Direct costs include drugs, adjuvant therapy, imaging tests, commuting, and lodging expenses, and indirect costs include time costs for patients and caregivers, and long-term production costs on account of diagnosis and treatment [8, 36]. The 1-year out-of-pocket costs of newly diagnosed colorectal cancer patients were 32,649 CNY (approximately $4,557) [23], the most expensive of the six major cancers in China, even though these were much lower than EUR 16,375–16,450 (approximately $16,777–16,854) for German male patients and $21,427 for Iranian patients [22, 38]. Due to the high cost of cancer care, many cancer survivors are more likely to face substantial self-payments and financial difficulties than those without cancer [56]. Financial hardship was prevalent in cancer survivors, with 25.3% of this group reporting material hardship (e.g., problems paying medical bills) and 34.3% reporting psychological hardship (e.g., worries about medical bills)[56]. In the past 10 years, the term “financial toxicity” has been popularized in cancer research. It is recognized that the financial toxicity related to the treatment and care can be just as significant as the physical toxicities traditionally associated with cancer therapeutics. Financial toxicity refers to cancer treatment’s financial burden and suffering to patients and their families. This toxicity has been shown to affect 48–73% of cancer patients [19]. Some studies have shown that financial toxicity is associated with clinically relevant patient outcomes, including poorer health-related quality of life, decreased survival, increased symptom burden, and decreased treatment compliance [30, 43, 45].

Much attention has been paid to financial toxicity in breast, lung, prostate, bladder, kidney, and blood cancer patients [6, 16–18, 25, 40]. Studies on the financial toxicity of colorectal cancer were mainly conducted in countries with well-established social welfare systems, such as the USA, Ireland, and Germany [21, 35, 45]. Previously identified factors influencing financial toxicity generally included sociodemographic characteristics, clinical data, direct and indirect costs, expectations of possible financial burdens, individual’s economic circumstances, and patient-specific values [25, 45, 47]. Additionally, oncologists were expected to investigate financial toxicity in advanced cancer patients who consistently report physical, mental, and emotional distress [15]. In a study of breast cancer, anxiety and depression were associated with financial toxicity [41]. All of these results provide further insights into the factors influencing financial toxicity. Because there are many differences between China and western countries in terms of medical systems, insurance systems, and patient attitudes, financial toxicity may vary in different influencing factors. With considerable advances in the treatment of non-metastatic colorectal cancer, the 5-year survival rate of stage I-III colorectal cancer patients reached 66.4% [37]. Prolonged postoperative survival of patients may lead to severe financial toxicity. However, few studies on financial toxicity among colorectal cancer patients in China have been conducted. The purpose of this study was to analyze the influencing factors of financial toxicity of non-metastatic colorectal cancer.

Methods

Design and sample

This was a single-institution, cross-sectional pilot study. We enrolled 287 patients with pathologically confirmed stage I-III colorectal cancer in a tertiary academic medical center in North China from January 2022 to June 2022. The patients were included if they (1) were at least 18 years old at the time of their cancer diagnosis, (2) underwent surgical care in this hospital, (3) received at least one type of adjuvant therapy (chemotherapy, radiotherapy) for at least 3 months, (4) had regular reading and writing skills, and (5) were able to complete surveys independently or with assistance. Patients were excluded if they had more than 1 type of cancer and had a history of mental illness or disorder.

Patients were recruited during their oncology hospital stay. We contacted the oncologists and nurses in charge in advance, and with their assistance, we evaluated the inpatients with colorectal cancer. We explained the purpose and significance of the investigation to patients who met the inclusion and exclusion criteria. Afterward, patients were given sufficient time to consider whether to participate in the study. After obtaining the patients’ consent, we conducted our survey in a comfortable meeting room the hospital. We distributed questionnaires and informed consent forms to patients. They typically completed the questionnaires independently. For patients with difficulties in reading and writing, we read the questions item by item in neutral, non-suggestive language to aid patients in completing the questionnaires. After patients completed the questionnaires, we confirmed that the questionnaires had been completed. If there was any omission, patients were asked to immediately fill out the questionnaires. Among 287 patients we recruited, 29 refused to participate in the study because they were not feeling well, they were inconvenient, their families disagreed, and some did not disclose their reasons.

We estimated the sample size based on the formula =Zα22p(1-p)d2, where N = initial estimated sample size, Z = confidence level (α), p = prevalence, and d = marginal error. The financial toxicity was evaluated in a previous study which was 16% [5]. With a 95% confidence level, a margin of error of 0.05, and an assumed 20% invalid completion rate. We estimated that at least 241 participants should be recruited. The Ethics Committee of the Affiliated Hospital of Qingdao University approved this study (NO. QYFYWZLL25862).

Data collection and measures

Our investigation consists of four questionnaires. Sociodemographic and clinicopathological data were collected using an 11-item questionnaire. Age, sex, residence, household income per year, employment status, marital status, primary insurance status, and education level were collected as sociodemographic factors. We extracted clinical data, including tumor stage at diagnosis, tumor location (colon/rectal), and treatment (chemotherapy, radiotherapy) from the electronic medical registry at the hospital.

Financial toxicity was assessed using the 11-item Comprehensive Score for Financial Toxicity (COST) questionnaire. It scored from 0 to 44, and each item was rated on a 4-point. Low values represented financial toxicity from more significant treatment modalities [12]. The psychometric properties of the scale were tested in insured patients with multiple myeloma, and the COST measure showed reliable internal consistency [24]. The test–retest intraclass correlation coefficient (ICC) was 0.80 [13]. The Cronbach’s α coefficient of the scale in this study was 0.930.

Another scale was the Perceived Social Support Scale (PSSS), with 12 self-reported items measuring three domains of subjective social support level, including family support, friends support, and other support [24]. Each item was rated on a 7-point, and scores of respective domains were standardized into a range of 12 to 84. There was a positive correlation between scores and social support. The Cronbach’s α coefficient of 0.814 indicated that the scale’s internal consistency was good among the Chinese colorectal cancer patients.

The patient’s anxiety and depression were measured by the Hospital Anxiety and Depression Scale (HADS). The scale consists of 14 items, seven for the anxiety subscale and seven for the depression subscale [42]. Each item was scored on a 4-point response scale from 0 to 3. The total score range for the subscales is 0 to 21. The recommended score for suspected cases is 8 to 10, and the recommended score for confirmed cases is ≥ 11. In the study, the Cronbach’s α for the HADS total score was 0.709, and the Cronbach’s α for the anxiety and depression subscales was 0.908 and 0.814, indicating good to excellent internal consistency of the scale.

Statistical analysis

Continuous data were expressed as means with the standard deviation, and categorical data were expressed as percentages and frequencies. The normal distribution of COST scores was assessed with the Shapiro–Wilk normality test. As appropriate, we compared sociodemographic and clinical characteristics using the student’s t-test, chi-square test, and ANOVA, as appropriate. Patients were initially divided into two groups based on the media COST score (score 21) to determine the relationship between COST score and sociodemographic, psychosocial, and treatment factors of objects.

We then constructed a multiple regression model to determine the correlation between each element of the original continuous data scale and the COST score. When choosing a model, we first analyzed one variable from the univariate linear regression analysis and then selected variables with P < 0.05 to construct a multivariate regression model. The expansion factor for each variance is used to check the collinearity of the selected variables. Hosmer-Ramesh’s test determined the excellent fit of the final model. All statistical tests were two-tailed, and P values less than 0.05 were considered statistically significant. Statistical analyses were performed in SPSS 26.0.

Results

Distribution of demographic and clinical variables

We recruited 287 patients in oncology wards; 258 patients returned the questionnaires, with a response rate of 89.9%. We excluded eight patients whose electronic medical record was incomplete. Then there were 250 subjects in our final analysis sample.

The baseline patient characteristics of the total cohort and COST scores are presented in Table 1. The median age of the sample was 62.0 years. 62.4% of the participants were male. Approximately 43.6% of respondents were retired, and most (92.8%) patients were married. In addition, 66.0% of the patients participated in Urban Employees Basic Medical Insurance (UEBMI). Patients’ average annual household income ranged from 20,000 to 49,999 (CNY). More than half (54.8%) of the patients were in stage III colorectal cancer, and most received chemotherapy (82.8%) and radiotherapy (69.6%). 35 (14.0%) patients reported advanced social support. The median COST score was 21. Compared with the patients who scored above 21, the patients who scored below the median were younger, female, less likely to be retired, had a higher household income, possessed UEBMI, and was more likely to have higher education. The patients who scored below the median also had a lower pathological stage, received radiation and chemotherapy, and were more reasonable to be free of depression and anxiety. Finally, having a moderate level of social support was more common among groups with lower COST scores. In this study, over half (52.8%) of colorectal cancer survivors experienced financial toxicity.

Table 1.

Patients characteristics by COST score (N = 250)

Characteristic Entire cohort (N = 250) COST ≤ 21(n = 132) COST > 21 (n = 118) P value
Median age (range), years 62.0 (52.75~68) 57.0 (48.0~65.8) 65.0 (58.8~70.0)  < 0.001
Age group  < 0.001
 < 50 40 (16.0%) 36 (27.3%) 4 (3.4%)
50–64 107 (42.8%) 58 (43.9%) 49 (41.5%)
65–74 87 (34.8%) 35 (26.5%) 52 (44.1%)
 ≥ 75 16 (6.4%) 3 (2.3%) 13 (11.0%)
Sex 0.003
Male 156 (62.4%) 71 (45.5%) 85 (54.5%)
Female 94 (37.6%) 61 (64.9%) 33 (35.1%)
Residence  < 0.001
Rural 108 (43.2) 80 (74.1%) 52 (36.6%)
Urban 142 (56.8) 28 (25.9%) 90 (63.4%)
Marital status 0.374
Married 232 (92.8%) 120 (57.1%) 112 (48.3%)
Unmarried/divorced/widowed 18 (7.2%) 12 (67.4%) 6 (35.3%)
Employment status  < 0.001
Employed (full-time, part-time) 57 (22.8%) 36 (63.2%) 21 (36.8%)
Retired 109 (43.6%) 24 (22.0%) 85 (78.0%)
Unemployed 84 (33.6%) 72 (85.7%) 12 (14.3%)
Education level 0.003
Illiteracy 11 (4.4%) 8 (72.7%) 3 (27.3%)
Primary school 36 (14.4%) 27 (75.0%) 9 (25.0%)
Junior or Senior high school 136 (54.4%) 71 (52.2%) 65 (47.8%)
University and above 67 (26.8%) 26 (38.8%) 41 (61.2%)
Household income per year (CNY)  < 0.001
 < 20,000 68 (27.2%) 58 (85.3%) 10 (14.7%)
20,000–49,999 75 (30.0%) 40 (53.3%) 35 (46.7%)
50,000–99,999 72 (28.8%) 24 (33.3%) 48 (66.7%)
 ≥ 100,000 35 (14.0%) 10 (28.6%) 25 (71.4%)
Primary insurance status  < 0.001
UEBMI 165 (66.0%) 64 (38.8%) 101 (61.2%)
URBMI 9 (3.6%) 7 (77.8%) 2 (22.2%)
NRCMS 72 (28.8%) 58 (80.6%) 14 (19.4%)
None 4 (1.6%) 3 (76.0%) 1 (25.0%)
Site 0.542
Rectum 139 (55.6%) 71 (51.1%) 68 (48.9%)
Colon 111 (44.4%) 61 (55.0%) 50 (45.0%)
Stage  < 0.001
I 15 (6.0%) 1 (6.7%) 14 (93.3%)
II 98 (39.2%) 51 (52.0%) 47 (48.0%)
III 137 (54.8%) 80 (58.4%) 57 (41.6%)
Chemotherapy  < 0.001
Yes 207 (82.8%) 119 (57.5%) 88 (42.5%)
No 43 (17.2%) 13 (30.2%) 30 (69.8%)
Radiotherapy 0.025
Yes 174 (69.6%) 100 (57.5%) 74 (42.5%)
No 76 (30.4%) 32 (42.1%) 44 (57.9%)
Anxiety  < 0.001
None 124 (49.6%) 47 (35.6%) 77 (65.3%)
Might exist 72 (28.8%) 50 (37.9%) 22 (18.6%)
Certainly exist 54 (21.6%) 35 (26.5%) 19 (16.1%)
Depression  < 0.001
None 166 (66.4%) 72 (54.5%) 94 (79.7%)
Might exist 55 (22.0%) 40 (30.3%) 15 (12.7%)
Certainly exist 29 (11.6%) 20 (15.2%) 9 (7.6%)
Social support level  < 0.001
Low level of social support 27 (10.8%) 22 (16.7%) 5 (4.2%)
Moderate level of social support 188 (75.2%) 105 (79.5%) 83 (70.3%)
High level of social support 35 (14.0%) 5 (3.8%) 30 (25.4%)
Open in a new tab

Abbreviations: CNY, Chinese yuan; NRCMS, New Rural Cooperative Medical Scheme; UEBMI, Urban Employees Basic Medical Insurance; URBMI, Urban Residents Basic Medical Insurance

Results of ANOVA

Table 2 shows associations between financial toxicity and the demographic variables. The variables with significant differences in financial toxicity were age, employment status, education level, household income, cancer staging, chemotherapy, radiotherapy, anxiety, depression, and social support level (P < 0.05).

Table 2.

Distribution of COST score by patient characteristics

Patient characteristic n COST score, mean ± SD (median) P value
Age group  < 0.001
 < 50 40 14.3 ± 6.9 (13.0)
50–64 107 19.5 ± 9.5 (19.0)
65–74 87 22.2 ± 10.1 (25.0)
 ≥ 75 16 26.9 ± 6.3 (26.0)
Sex 0.052
Male 156 21.8 ± 9.4 (24.0)
Female 94 17.2 ± 9.4 (16.0)
Residence 0.404
Rural 108 15.0 ± 8.2 (14.0)
Urban 142 24.0 ± 8.9 (26.0)
Marital status 0.772
Married 232 20.4 ± 9.8 (21.0)
Unmarried/divorced/widowed 18 17.1 ± 7.4 (16.0)
Employment status  < 0.001
Employed (full-time, part-time) 57 19.5 ± 7.9 (19.0)
Retired 109 27.2 ± 6.4 (19.0)
Unemployed 84 11.3 ± 6.3 (28.0)
Education level 0.859
None 11 12.6 ± 8.2 (10.0)
Primary school 36 13.2 ± 8.5 (9.0)
Junior or Senior high school 136 20.7 ± 9.3 (21.0)
University and above 67 23.8 ± 8.9 (26.0)
Household income per year (CNY)  < 0.001
 < 20,000 68 12.3 ± 8.7 (10.0)
20,000–49,999 75 19.6 ± 8.8 (21.0)
50,000–99,999 72 24.8 ± 8.7 (26.0)
 ≥ 100,000 35 26.7 ± 7.4 (28.0)
Primary insurance status 0.471
UEBMI 165 23.8 ± 8.6 (25.0)
URBMI 9 13.3 ± 7.8 (11.0)
NRCMS 72 12.9 ± 7.4 (10.0)
None 4 13.3 ± 7.8 (11.0)
Site 0.561
Rectum 139 19.6 ± 9.8 (21.0)
Colon 111 20.7 ± 9.6(19.0)
Stage 0.032
I 15 25.1 ± 5.5 (25.0)
II 98 20.1 ± 9.3 (21.0)
III 137 19.6 ± 10.1 (19.0)
Chemotherapy 0.089
Yes 206 19.6 ± 9.9 (19.0)
No 44 22.6 ± 8.3 (24.0)
Radiotherapy 0.563
Yes 172 19.5 ± 9.9 (19.0)
No 78 21.5 ± 9.1 (23.0)
Anxiety 0.533
None 124 22.5 ± 9.5 (25.0)
Might exist 72 17.2 ± 9.1 (16.0)
Certainly exist 54 18.6 ± 9.1 (19.0)
Depression 0.406
None 166 21.7 ± 9.6 (24.0)
Might exist 55 15.7 ± 8.7 (13.0)
Certainly exist 29 19.5 ± 9.8 (19.0)
Social support level 0.056
Low level of social support 27 13.9 ± 7.9 (10.0)
Moderate level of social support 188 19.7 ± 9.7 (19.0)
High level of social support 35 26.9 ± 6.0 (27.0)
Open in a new tab

For all categorical variables, chi-square test was performed

P value = level of statistical significance; Significant (p < 0.05)

Results of univariate and multivariate linear regression

The relationship between patient characteristics and COST outcomes was further elucidated by linear regression. Simple linear regression and multiple regression models were constructed, as shown in Table 3. In the univariate analysis, old age, female, higher income, living in the urban, education level of university and above, retirement at home, not receiving chemotherapy, and a high level of social support were all protective against financial toxicity (P < 0.05). However, unemployed, primary school education, participation in New Rural Cooperative Medical Scheme (NRCMS), and mild anxiety and depression were associated with increased levels of financial toxicity (P < 0.05). Marital status, cancer disease site, cancer stage, and radiation therapy were not significantly related to financial toxicity (P > 0.05). In the multivariate analysis (Table 3), young age, unemployed, low annual household income, chemotherapy, and the lack of sufficient social support remained determinants for financial toxicity (P < 0.05). However, sex, type of medical insurance, place of residence, education level, anxiety, and depression status were no longer significantly associated with financial toxicity (P > 0.05).

Table 3.

Univariate and multivariate linear regression

Patient characteristic Univariate analysis Multivariable analysis
Coefficient (95% CI) P value Coefficient (95% CI) P value
Age group
 < 50(reference)
50–64  − 1.0 (− 3.4 to 1.5) 0.431 2.9 (0.3 to 5.5) 0.023
65–74 3.2 (0.7 to 5.7) 0.012 6.4 (3.4 to 9.4)  < 0.001
 ≥ 75 7.2 (2.4 to 12.1) 0.004 8.8 (4.5 to 13.0)  < 0.001
Sex
Male(reference)
Female  − 4.6 (− 7.1 to − 2.2)  < 0.001  − 1.6 (− 3.3 to 0.2) 0.053
Residence
Rural(reference)
Urban 9.0 (6.8 to 11.1)  < 0.001  − 1.1 (− 3.3 to 1.2) 0.353
Employment status
Employed (full − time, part − time) (reference)
Retired 12.6 (1.2 to 14.5) 0.001 5.5 (− 1.8 to 8.1) 0.075
Unemployed  − 13.3 (− 15.2 to − 11.3) 0.001  − 2.4 (− 5.3 to − 1.1)  < 0.001
Education level
Illiteracy(reference)
Primary school  − 8.0 (− 11.3 to − 4.8)  < 0.001  − 1.5 (− 5.1 to 3.2) 0.659
Junior and Senior high school 1.3 (− 1.1 to 3.8) 0.274  − 0.9 (− 4.9 to 3.2) 0.667
University and above 5.0 (2.3 to 7.7)  < 0.001  − 0.1 (4.6 to 4.5) 0.974
Household income per year (CNY)
 < 20,000(reference)
20,000–49,999  − 0.7 (− 3.3 to 2.0) 0.623 3.7 (1.0 to 6.4) 0.007
50,000–99,999 6.6 (4.0 to 9.1)  < 0.001 7.0 (3.7 to 10.3)  < 0.001
 ≥ 100,000 7.7 (4.3 to 11.0)  < 0.001 11.5 (7.4 to 15.5)  < 0.001
Primary insurance status
UEBMI (reference)
URBMI  − 7.0 (− 13.4 to − 0.6) 0.032  − 0.2 (− 4.6 to 4.2) 0.927
NRCMS  − 10.2 (− 12.5 to − 7.8)  < 0.001  − 1.4 (− 4.1 to 1.3) 0.320
None  − 7.0 (− 16.5 to 2.6) 0.154  − 3.8 (− 10.0 to 2.6) 2.554
Chemotherapy
Yes(reference)
No 3.1 (− 1.0 to 6.2) 0.057 3.6 (1.5 to 5.6) 0.001
Anxiety
None(reference)
Might exist  − 4.1 (− 6.7 to − 1.5) 0.002  − 1.1 (− 3.0 to 0.8) 0.265
Certainly exist  − 2.0 (− 4.9 to 1.0) 0.186  − 0.1 (− 2.9 to 2.7) 0.940
Depression
None(reference)
Might exist  − 5.6 (− 8.4 to − 2.8)  < 0.001  − 1.4 (− 3.6 to 0.8) 0.198
Certainly exist  − 0.7 (− 4.5 to 3.1) 0.715  − 0.4 (− 3.6 to 2.8) 0.821
Social support level
Low level of social support (reference)
Moderate level of social support  − 1.5 (− 4.3 to 1.3) 0.285 1.1 (− 1.4 to 3.6) 0.379
High level of social support 7.9 (4.6 to 11.3)  < 0.001 3.8 (0.5 to 7.1) 0.024
Open in a new tab

Abbreviations: CI, confidence interval

P value = level of statistical significance; Significant (p < 0.05)

Discussion

In the cross-sectional study, we investigated the financial toxicity of postoperative non-metastatic colorectal cancer patients in a tertiary hospital in eastern China and analyzed the associated influencing factors. The Comprehensive Score for Financial Toxicity (COST) was used to measure the financial toxicity of colorectal cancer patients. We found that 52.8% of colorectal cancer survivors suffered from financial toxicity. Our findings suggested that the patients most likely to have financial toxicity were young, had low annual household income, were unemployed, received chemotherapy, and lacked sufficient social support.

Our study demonstrated that elderly patients (> 65 years old) were protected against financial toxicity compared with patients aged 18–65. This result was consistent with prior research on cancer survivors [4, 55]. In the USA, cancer-related financial hardship was more common among survivors aged 18–65 than among older survivors (53.6% vs. 42.0%) [20]. A study found that because younger survivors were more likely to have fewer comorbidities, they may be able to tolerate aggressive therapeutic schemes. Therefore, treatment costs may be higher in younger survivors than in the elderly [31]. For instance, the 1-year net cost for stage III colorectal patients aged 18–64 was $61,600, while the 1-year net cost for patients 65 and older was$56,600 [4]. Previous studies suggested that younger patients had lower savings and the absence of a stable welfare guarantee. Furthermore, cancer treatment and disability caused lower working hours [27]. As the economic backbone of the entire family, young cancer patients in China may bear the most extraordinary economic pressure in society. They usually take the responsibilities of caring for their aging parents, raising children, and paying for daily living expenses. After the cancer diagnosis, there is less time to accumulate assets, resulting in lower income. One study showed that most unemployed and disabled colorectal cancer patients were young (mean age, 51.3 years) and could not undertake work after being diagnosed with colorectal cancer [45]. Due to the global COVID-19 pandemic, the financial toxicity of young cancer patients was further compounded by the fact that 21% of cancer patients reported a change in employment status. More than half of the patients expressed concerns about their future financial situation, so the above reasons aggravated the financial toxicity of young patients (Y. S. [9, 10]. Additionally, people over 65 generally have fulfilled the responsibilities and obligations of supporting their parents and raising their children in China. They are entitled to retirement pensions and are more likely to have considerable retirement savings. Savings and superannuation are unique financial cushions to ease cash flow during periods of low income and high spending due to cancer treatment. Hence, the financial toxicity in this study appeared to be milder in the elderly.

This study showed that unemployment and lower household income were significantly associated with the financial toxicity of patients. A study found that 45% of colorectal cancer patients with stage III lost their jobs because of the treatment; simultaneously, they worked to lessen the financial burden [51]. Young adults with advanced disease had a 56% higher risk of losing paid work within 4 years of diagnosis than the general population, and the decline in household income because of unemployment was closely relevant to a decrease in quality of life and economic stress [58]. One study on the employment of cancer survivors showed that the average time cost of traveling to and from treatment for working-age patients was $4,809 per month. Moreover, those who lost their jobs or had to retire early because of cancer may experience a drop in their incomes [32]. The physical stress and potential psychological burden of long-term medication and treatment may also prevent them from jobs, compromising work capacity and productivity to some extent in the long run [3]. In the same way, the family caregiver had to spend considerable time and energy, resulting in reduced personal income [53]. All the above causes brought lower household income and more severe financial burdens.

Chemotherapy was associated with increased financial toxicity in our study. In a survey of 409 participants, 57% of cancer patients received chemotherapy, and 67% of patients in this population experienced financial toxicity [57]. Adjuvant chemotherapy is currently the most common and effective treatment modality for colorectal cancer individuals after surgery. Approximately half of the American patients received chemotherapy regimens [52], and respondents receiving chemotherapy reported significant financial burdens [26, 44]. In China, 72.5% of stage II–III colorectal cancer patients received adjuvant therapy (G. [9, 10]. Unfortunately, patients receiving chemotherapy also had advanced staging or severe comorbidities, which resulted in higher reported financial toxicity [16, 17]. At present, adjuvant chemotherapy for colorectal cancer usually lasts 3–6 months with various chemotherapy regimens. Although China government continues to expand the proportion of medical insurance reimbursement for anticancer drugs, patients are still in financial difficulties due to high treatment costs.

In our study, lack of high levels of social support was another factor associated with financial toxicity in the colorectal cancer population. The finding of our study is consistent with the previous result [29]. Nearly one-third of patients with colorectal cancer had decreased levels of social support after diagnosis and treatment [39], and only 14% of participants in this study had high levels of social support. Because of the fear of burdening others, patients avoid communication and contact with informal caregivers, exacerbating their loneliness [11]. A sound social support system could relieve negative emotions such as anxiety and depression. Non-professional caregivers can provide practical material support to patients reducing the overall economic burden. At the same time, it is recommended to increase the communication between oncologists and patients and nurses and patients. Discussion of medical costs is an integral part of high-quality life. Through cost communication, individuals can understand their economic status to seek extensive support from all walks of life.

It is indisputable that the Chinese government has been committed to providing support for patients. China has established a comprehensive medical insurance system through the deepening reform of the health system since 2009 and the Healthy China 2030 Plan [14]. To narrow the diversities in per capita premiums and capital sources, the government set up the outpatient serious disease system to increase the reimbursement rate and reimbursement ceiling for medical expenses. In addition, an urban and rural critical illness insurance system was also established to break the cycle of poverty by preventing the low-income group from being pushed into poverty due to high medical costs [36, 50]. To reduce the economic burden of cancer patients, China continues to expand the coverage of targeted drugs included in medical insurance. Four new colorectal cancer targeted drugs, including cetuximab and bevacizumab, were approved in 2021. However, patients still face enormous financial pressure because of the uneven distribution of health resources and increasing medical costs. In the future, multiple and multifaceted supportive measures should be implemented for colorectal cancer patients.

Limitations

There are several limitations regarding the generalizability of our study. Firstly, it was a single-centered study design, and we recruited a relatively small number of study subjects. Our research was conducted in a large tertiary hospital in a coastal city. The socio-economic level of the region is significantly higher than the average level. Further studies with multi-center, larger-sample, and universal coverage of areas with economic representation are needed to validate our findings. Secondly, the cross-sectional study design restricts any causal inference. Long-term financial toxicity is not assessed in patients with colorectal cancer after the end of treatment. Future prospective longitudinal studies are needed to investigate the financial toxicity profile of cancer survivors during their cancer experiences. However, we believe this finding contributes to the ongoing debate on factors associated with financial toxicity in cancer patients. This study’s results supply insights for further exploration of determinants for financial toxicity in colorectal cancer patients.

Conclusions

In our study, financial toxicity affects at least half of survivors with stage I–III colorectal cancer. Young age, lower annual household income, unemployment, chemotherapy, and insufficient social support were associated with financial toxicity. We will conduct large-scale prospective surveys to assess the financial toxicity of colorectal cancer patients and design targeted interventions to solve the patients’ financial toxicity. It is essential to strengthen the clinical discussion of costs by popularizing cost-related health literacy among cancer survivors and oncologists.

Acknowledgements

We thank the participants of the present study for their time and dedication. We wish to show gratitude to the medical staff of the Department of Oncology of the Affiliated Hospital of Qingdao University. We also thank to Natural Science Foundation of Shandong Province (NO. ZR2020MG057).

Author contribution

Literature analysis, data analysis, writing the original manuscript: Minghui Mo. Study planning, conduct of study, and manuscript editing: Peipei Jia. Literature analysis, data collection: Kai Zhu. Data collection, data analysis: Wenjing Huang. Study design, planning: Li Han. Manuscript review, supervision: Cuiping Liu. Study design, supervision: Xia Huang. All authors of this paper read and approved the final version submitted.

Funding

This current work was supported by the Natural Science Foundation of Shandong Province (NO. ZR2020MG057).

Data availability

The datasets generated during and analyzed during the current study are available from the corresponding author on reasonable request.

Declarations

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki. The Ethics Committee of the Affiliated Hospital of Qingdao University approved this study (NO. QYFYWZLL25862).

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Consent for publication

The authors affirm that human research participants provided informed consent for the publication of the images in Table(s) 1, 2, and 3.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Minghui Mo, Email: 969021415@qq.com.

Cuiping Liu, Email: lcping0926@126.com.

Xia Huang, Email: huangxia7107@qdu.edu.cn.

References

  • 1.Abrams HR, Durbin S, Huang CX, Johnson SF, Nayak RK, Zahner GJ, Peppercorn J. Financial toxicity in cancer care: origins, impact, and solutions. Transl Behav Med. 2021;11(11):2043–2054. doi: 10.1093/tbm/ibab091. [DOI] [PubMed] [Google Scholar]
  • 2.Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66(4):683–691. doi: 10.1136/gutjnl-2015-310912. [DOI] [PubMed] [Google Scholar]
  • 3.Banegas MP, Guy GP, de Moor JS, Ekwueme DU, Virgo KS, Kent EE, Nutt S, Zheng Z, Rechis R, Yabroff KR. For working-age cancer survivors, medical debt and bankruptcy create financial hardships. Health Affairs (Project Hope) 2016;35(1):54–61. doi: 10.1377/hlthaff.2015.0830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Banegas MP, Yabroff KR, O’Keeffe-Rosetti MC, Ritzwoller DP, Fishman PA, Salloum RG, Lafata JE, Hornbrook MC. Medical care costs associated with cancer in integrated delivery systems. J Natl Compr Cancer Network: JNCCN. 2018;16(4):402–410. doi: 10.6004/jnccn.2017.7065. [DOI] [PubMed] [Google Scholar]
  • 5.Bestvina CM, Zullig LL, Rushing C, Chino F, Samsa GP, Altomare I, Tulsky J, Ubel P, Schrag D, Nicolla J, Abernethy AP, Peppercorn J, Zafar SY. Patient-oncologist cost communication, financial distress, and medication adherence. J Oncol Pract. 2014;10(3):162–167. doi: 10.1200/JOP.2014.001406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Bhanvadia SK, Psutka SP, Burg ML, de Wit R, Dhillon HM, Gyawali B, Morgans AK, Goldstein DA, Smith AB, Sun M, Penson DF. Financial toxicity among patients with prostate, bladder, and kidney cancer: a systematic review and call to action. Eur Urol Oncol. 2021;4(3):396–404. doi: 10.1016/j.euo.2021.02.007. [DOI] [PubMed] [Google Scholar]
  • 7.Cai Y, Xue M, Chen W, Hu M, Miao Z, Lan L, Zheng R, Meng Q. Expenditure of hospital care on cancer in China, from 2011 to 2015. Chin J Cancer Res=Chung-Kuo Yen Cheng Yen Chiu. 2017;29(3):253–262. doi: 10.21147/j.issn.1000-9604.2017.03.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Carrera PM, Kantarjian HM, Blinder VS. The financial burden and distress of patients with cancer: understanding and stepping-up action on the financial toxicity of cancer treatment. CA: A Cancer J Clin. 2018;68(2):153–165. doi: 10.3322/caac.21443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Chen G, Peng J, Xiao Q, Wu H-X, Wu X, Wang F, Li L, Ding P, Zhao Q, Li Y, Wang D, Shao Y, Bao H, Pan Z, Ding K-F, Cai S, Wang F, Xu R-H. Postoperative circulating tumor DNA as markers of recurrence risk in stages II to III colorectal cancer. J Hematol Oncol. 2021;14:80. doi: 10.1186/s13045-021-01089-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Chen YS, Zhou ZN, Glynn SM, Frey MK, Balogun OD, Kanis M, Holcomb K, Gorelick C, Thomas C, Christos PJ, Chapman-Davis E. Financial toxicity, mental health, and gynecologic cancer treatment: the effect of the COVID-19 pandemic among low-income women in New York City. Cancer. 2021;127(14):2399–2408. doi: 10.1002/cncr.33537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Cotrim H, Pereira G. Impact of colorectal cancer on patient and family: implications for care. Eur J Oncol Nurs: Off J Eur Oncol Nurs Soc. 2008;12(3):217–226. doi: 10.1016/j.ejon.2007.11.005. [DOI] [PubMed] [Google Scholar]
  • 12.de Souza JA, Yap BJ, Hlubocky FJ, Wroblewski K, Ratain MJ, Cella D, Daugherty CK. The development of a financial toxicity patient-reported outcome in cancer: the COST measure. Cancer. 2014;120(20):3245–3253. doi: 10.1002/cncr.28814. [DOI] [PubMed] [Google Scholar]
  • 13.de Souza JA, Yap BJ, Wroblewski K, Blinder V, Araújo FS, Hlubocky FJ, Nicholas LH, O’Connor JM, Brockstein B, Ratain MJ, Daugherty CK, Cella D. Measuring financial toxicity as a clinically relevant patient-reported outcome: the validation of the COmprehensive Score for financial Toxicity (COST) Cancer. 2017;123(3):476–484. doi: 10.1002/cncr.30369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Debie A, Khatri RB, Assefa Y. Successes and challenges of health systems governance towards universal health coverage and global health security: a narrative review and synthesis of the literature. Health Res Policy Syst. 2022;20:50. doi: 10.1186/s12961-022-00858-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Delgado-Guay M, Ferrer J, Rieber AG, Rhondali W, Tayjasanant S, Ochoa J, Cantu H, Chisholm G, Williams J, Frisbee-Hume S, Bruera E. Financial distress and its associations with physical and emotional symptoms and quality of life among advanced cancer patients. Oncologist. 2015;20(9):1092–1098. doi: 10.1634/theoncologist.2015-0026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Esselen KM, Gompers A, Hacker MR, Bouberhan S, Shea M, Summerlin SS, Rucker LR, Huh WK, Pisu M, Liang MI. Evaluating meaningful levels of financial toxicity in gynecologic cancers. Int J Gynecol Cancer: Off J Int Gynecol Cancer Soc. 2021;31(6):801–806. doi: 10.1136/ijgc-2021-002475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Esselen KM, Stack-Dunnbier H, Gompers A, Hacker MR. Crowdsourcing to measure financial toxicity in gynecologic oncology. Gynecol Oncol. 2021;161(2):595–600. doi: 10.1016/j.ygyno.2021.01.040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Friedes C, Hazell SZ, Fu W, Hu C, Voong RK, Lee B, Feliciano JL, Nicholas LH, McNutt TR, Han P, Narang AK, Hales RK. Longitudinal trends of financial toxicity in patients with lung cancer: a prospective cohort study. JCO Oncol Pract. 2021;17(8):e1094–e1109. doi: 10.1200/OP.20.00721. [DOI] [PubMed] [Google Scholar]
  • 19.Gordon LG, Merollini KMD, Lowe A, Chan RJ. A systematic review of financial toxicity among cancer survivors: we can’t pay the co-pay. The Patient. 2017;10(3):295–309. doi: 10.1007/s40271-016-0204-x. [DOI] [PubMed] [Google Scholar]
  • 20.Han X, Zhao J, Zheng Z, de Moor JS, Virgo KS, Yabroff KR. Medical financial hardship intensity and financial sacrifice associated with cancer in the United States. Cancer Epidemiol, Biomark Prev:Publ Am Assoc Cancer Res, Cosponsored Am Soc Prev Oncol. 2020;29(2):308–317. doi: 10.1158/1055-9965.EPI-19-0460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Hanly P, Maguire R, Ceilleachair AO, Sharp L. Financial hardship associated with colorectal cancer survivorship: the role of asset depletion and debt accumulation. Psychooncology. 2018;27(9):2165–2171. doi: 10.1002/pon.4786. [DOI] [PubMed] [Google Scholar]
  • 22.Heisser T, Simon A, Hapfelmeier J, Hoffmeister M, Brenner H. Treatment costs of colorectal cancer by sex and age: population-based study on health insurance data from Germany. Cancers. 2022;14(15):3836. doi: 10.3390/cancers14153836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Huang H-Y, Shi J-F, Guo L-W, Bai Y-N, Liao X-Z, Liu G-X, Mao A-Y, Ren J-S, Sun X-J, Zhu X-Y, Wang L, Song B-B, Du L-B, Zhu L, Gong J-Y, Zhou Q, Liu Y-Q, Cao R, Mai L, … Dai M (2017) Expenditure and financial burden for the diagnosis and treatment of colorectal cancer in China: a hospital-based, multicenter, cross-sectional survey. Chin J Cancer 36(1):41. 10.1186/s40880-017-0209-4 [DOI] [PMC free article] [PubMed]
  • 24.Huntington SF, Weiss BM, Vogl DT, Cohen AD, Garfall AL, Mangan PA, Doshi JA, Stadtmauer EA. Financial toxicity in insured patients with multiple myeloma: a cross-sectional pilot study. The Lancet Haematol. 2015;2(10):e408–416. doi: 10.1016/S2352-3026(15)00151-9. [DOI] [PubMed] [Google Scholar]
  • 25.Imber BS, Varghese M, Ehdaie B, Gorovets D. Financial toxicity associated with treatment of localized prostate cancer. Nat Rev Urol. 2020;17(1):28–40. doi: 10.1038/s41585-019-0258-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Jagsi R, Hawley ST, Abrahamse P, Li Y, Janz NK, Griggs JJ, Bradley C, Graff JJ, Hamilton A, Katz SJ. Impact of adjuvant chemotherapy on long-term employment of survivors of early-stage breast cancer. Cancer. 2014;120(12):1854–1862. doi: 10.1002/cncr.28607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Jing J, Feng R, Zhang X, Li M, Gao J. Financial toxicity and its associated patient and cancer factors among women with breast cancer: a single-center analysis of low-middle income region in China. Breast Cancer Res Treat. 2020;181(2):435–443. doi: 10.1007/s10549-020-05632-3. [DOI] [PubMed] [Google Scholar]
  • 28.Johdi NA, Sukor NF. Colorectal cancer immunotherapy: options and strategies. Front Immunol. 2020;11:1624. doi: 10.3389/fimmu.2020.01624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Langenberg SMCH, Poort H, Wymenga ANM, de Groot JW, Muller EW, van der Graaf WTA, Prins JB, van Herpen CML. Informal caregiver well-being during and after patients’ treatment with adjuvant chemotherapy for colon cancer: a prospective, exploratory study. Support Care Cancer. 2021;29(5):2481–2491. doi: 10.1007/s00520-020-05738-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Lathan CS, Cronin A, Tucker-Seeley R, Zafar SY, Ayanian JZ, Schrag D. Association of financial strain with symptom burden and quality of life for patients with lung or colorectal cancer. J Clin Oncol: Off J Am Soc Clin Oncol. 2016;34(15):1732–1740. doi: 10.1200/JCO.2015.63.2232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Lieu CH, Renfro LA, de Gramont A, Meyers JP, Maughan TS, Seymour MT, Saltz L, Goldberg RM, Sargent DJ, Eckhardt SG, Eng C. Association of age with survival in patients with metastatic colorectal cancer: analysis from the ARCAD clinical trials program. J Clin Oncol. 2014;32(27):2975–2982. doi: 10.1200/JCO.2013.54.9329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Lu L, Gavin A, Drummond FJ, Sharp L. Cumulative financial stress as a potential risk factor for cancer-related fatigue among prostate cancer survivors. J Cancer Surviv. 2021;15(1):1–13. doi: 10.1007/s11764-020-00906-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Luo X-J, Zhao Q, Liu J, Zheng J-B, Qiu M-Z, Ju H-Q, Xu R-H. Novel genetic and epigenetic biomarkers of prognostic and predictive significance in stage II/III colorectal cancer. Mol Ther: J Am Soc Gene Ther. 2021;29(2):587–596. doi: 10.1016/j.ymthe.2020.12.017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Mariotto AB, Yabroff KR, Shao Y, Feuer EJ, Brown ML. Projections of the cost of cancer care in the United States: 2010–2020. J Natl Cancer Inst. 2011;103(2):117–128. doi: 10.1093/jnci/djq495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Mehlis K, Witte J, Surmann B, Kudlich M, Apostolidis L, Walther J, Jäger D, Greiner W, Winkler EC. The patient-level effect of the cost of cancer care—financial burden in German cancer patients. BMC Cancer. 2020;20(1):529. doi: 10.1186/s12885-020-07028-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Meng Q, Mills A, Wang L, Han Q. What can we learn from China’s health system reform? The BMJ. 2019;365:l2349. doi: 10.1136/bmj.l2349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Micu BV, Vesa ŞC, Pop TR, Micu CM. Evaluation of prognostic factors for 5 year-survival after surgery for colorectal cancer. Ann Ital Chir. 2020;91:41–48. [PubMed] [Google Scholar]
  • 38.Nejati M, Razavi M, Harirchi I, Zanganeh M, Salari G, Tabatabaee SM. Resource use and costs associated to the initial phase of treatment for patients with colorectal cancer receiving post-surgery chemotherapy: a cost analysis from a healthcare perspective. Iran J Public Health. 2021;50(9):1887–1896. doi: 10.18502/ijph.v50i9.7062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Nguyen NH, Khera R, Ohno-Machado L, Sandborn WJ, Singh S. Prevalence and effects of food insecurity and social support on financial toxicity in and healthcare use by patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol: Off Clin Pract J Am Gastroenterol Assoc. 2021;19(7):1377–1386.e5. doi: 10.1016/j.cgh.2020.05.056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Ouchveridze E, Banerjee R, Desai A, Aziz M, Lee-Smith W, Mian H, Berger K, McClune B, Sborov D, Qazilbash M, Kumar S, Mohyuddin GR. Financial toxicity in hematological malignancies: a systematic review. Blood Cancer J. 2022;12(4):74. doi: 10.1038/s41408-022-00671-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Perry LM, Hoerger M, Seibert K, Gerhart JI, O’Mahony S, Duberstein PR. Financial strain and physical and emotional quality of life in breast cancer. J Pain Symptom Manage. 2019;58(3):454–459. doi: 10.1016/j.jpainsymman.2019.05.011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Pignatiello GA, Townsend AL, Hickman RL. An examination of the hospital anxiety and depression scale’s structural validity among family members of the critically Ill. Am J Crit Care : Off Publ, Am Assoc Crit-Care Nurs. 2021;30(3):212–220. doi: 10.4037/ajcc2021214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Ramsey SD, Bansal A, Fedorenko CR, Blough DK, Overstreet KA, Shankaran V, Newcomb P. Financial Insolvency as a risk factor for early mortality among patients with cancer. J Clin Oncol: Off J Am Soc Clin Oncol. 2016;34(9):980–986. doi: 10.1200/JCO.2015.64.6620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Regenbogen SE, Veenstra CM, Hawley ST, Banerjee M, Ward KC, Kato I, Morris AM. The personal financial burden of complications after colorectal cancer surgery. Cancer. 2014;120(19):3074–3081. doi: 10.1002/cncr.28812. [DOI] [PubMed] [Google Scholar]
  • 45.Shankaran V, Jolly S, Blough D, Ramsey SD. Risk factors for financial hardship in patients receiving adjuvant chemotherapy for colon cancer: a population-based exploratory analysis. J Clin Oncol: Off J Am Soc Clin Oncol. 2012;30(14):1608–1614. doi: 10.1200/JCO.2011.37.9511. [DOI] [PubMed] [Google Scholar]
  • 46.Shankaran V, Unger JM, Darke AK, Suga JM, Wade JL, III, Kourlas PJ, Chandana SR, O’Rourke MA, Satti S, Liggett D, Hershman DL, Ramsey SD (2022) S1417CD: a prospective multicenter cooperative group-led study of financial hardship in metastatic colorectal cancer patients. JNCI: J Natl Cancer Inst djab210. 10/gphnsg [DOI] [PMC free article] [PubMed]
  • 47.Sharp L, O’Leary E, O’Ceilleachair A, Skally M, Hanly P. Financial impact of colorectal cancer and its consequences: associations between cancer-related financial stress and strain and health-related quality of life. Dis Colon Rectum. 2018;61(1):27–35. doi: 10.1097/DCR.0000000000000923. [DOI] [PubMed] [Google Scholar]
  • 48.Siegel RL, Miller KD, Goding Sauer A, Fedewa SA, Butterly LF, Anderson JC, Cercek A, Smith RA, Jemal A. Colorectal cancer statistics, 2020. CA: Cancer J Clin. 2020;70(3):145–164. doi: 10.3322/caac.21601. [DOI] [PubMed] [Google Scholar]
  • 49.Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: Cancer J Clin. 2021;71(3):209–249. doi: 10.3322/caac.21660. [DOI] [PubMed] [Google Scholar]
  • 50.Tao W, Zeng Z, Dang H, Lu B, Chuong L, Yue D, Wen J, Zhao R, Li W, Kominski GF. Towards universal health coverage: lessons from 10 years of healthcare reform in China. BMJ Glob Health. 2020;5(3):e002086. doi: 10.1136/bmjgh-2019-002086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Veenstra CM, Regenbogen SE, Hawley ST, Abrahamse P, Banerjee M, Morris AM. Association of paid sick leave with job retention and financial burden among working patients with colorectal cancer. JAMA. 2015;314(24):2688–2690. doi: 10.1001/jama.2015.12383. [DOI] [PubMed] [Google Scholar]
  • 52.Veenstra CM, Regenbogen SE, Hawley ST, Griggs JJ, Banerjee M, Kato I, Ward KC, Morris AM. A composite measure of personal financial burden among patients with stage III colorectal cancer. Med Care. 2014;52(11):957–962. doi: 10.1097/MLR.0000000000000241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Warner EL, Millar MM, Orleans B, Edwards SL, Carter ME, Vaca Lopez PL, Sweeney C, Kirchhoff AC. Cancer survivors’ financial hardship and their caregivers’ employment: results from a statewide survey. J Cancer Surviv. 2022 doi: 10.1007/s11764-022-01203-1. [DOI] [PubMed] [Google Scholar]
  • 54.Xia C, Dong X, Li H, Cao M, Sun D, He S, Yang F, Yan X, Zhang S, Li N, Chen W. Cancer statistics in China and United States, 2022: profiles, trends, and determinants. Chin Med J. 2022;135(5):584–590. doi: 10.1097/CM9.0000000000002108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Yabroff KR, Dowling EC, Guy GP, Banegas MP, Davidoff A, Han X, Virgo KS, McNeel TS, Chawla N, Blanch-Hartigan D, Kent EE, Li C, Rodriguez JL, de Moor JS, Zheng Z, Jemal A, Ekwueme DU. Financial hardship associated with cancer in the United States: findings from a population-based sample of adult cancer survivors. J Clin Oncol: Off J Am Soc Clin Oncol. 2016;34(3):259–267. doi: 10.1200/JCO.2015.62.0468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Yabroff KR, Zhao J, Zheng Z, Rai A, Han X. Medical financial hardship among cancer survivors in the United States: what do we know? What do we need to know? Cancer Epidemiol, Biomark Prev: Publ Am Assoc Cancer Res, Cosponsored Am Soc Prev Oncol. 2018;27(12):1389–1397. doi: 10.1158/1055-9965.EPI-18-0617. [DOI] [PubMed] [Google Scholar]
  • 57.Yu H, Li H, Zuo T, Cao L, Bi X, Xing H, Cai L, Sun J, Liu Y. Financial toxicity and psychological distress in adults with cancer: a treatment-based analysis. Asia Pac J Oncol Nurs. 2022;9(9):100069. doi: 10.1016/j.apjon.2022.04.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Yuan C-M, Wang C-C, Wu W-T, Ho C-L, Chen W-L. Risk factors for return to work in colorectal cancer survivors. Cancer Med. 2021;10(12):3938–3951. doi: 10.1002/cam4.3952. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets generated during and analyzed during the current study are available from the corresponding author on reasonable request.

Articles from Supportive Care in Cancer are provided here courtesy of Nature Publishing Group

RESOURCES