Patient Perspective and Worry regarding Ulcerative Colitis-Associated Cancer: A Questionnaire-Based Surveillance Study Open Access

Ulcerative colitis (UC) is characterized by chronic intestinal inflammation of unknown cause, resulting from an inappropriate intestinal immune response to luminal content in genetically susceptible individuals [1]. The prevalence of UC is increasing worldwide [2]. Colonic mucosal inflammation in UC is associated with repeated relapses and remissions, and many patients experience frequent stools, bloody stools, tenesmus, and urgency of defecation [3]; UC affects physiological, psychological, and social impacts on patients.

UC patients develop colorectal cancer owing to inflammatory carcinogenesis [4]. A previous report revealed that 8.3% of patients developed cancer within 20 years [5], and a more recent report showed that cancer occurrence was estimated to be 4.8% within 10 years [6]. UC-associated neoplasm (UCAN) is often difficult to detect endoscopically because it occurs as a flat lesion in the inflamed mucosa and is sometimes eventually found in a progressive stage. Therefore, regular surveillance colonoscopy is recommended to detect UCAN in an earlier stage.

Because no radical treatment has been established for UC, patients often search for information related to the disease through social networking services (SNS) and the internet on their own, interactions with other patients, and asking healthcare professionals. However, little is known about patient perceptions of cancer development in UC, their awareness of risk factors, and their anxiety about developing cancer.

Cancer worry is an emotional and cognitive response to the threat of cancer [7], and is often a motive for surveillance examinations. The Cancer Worry Scale (CWS) [8] is widely used to assess cancer risk, assessing the intensity of worry about developing cancer and its influence on mood and activities in daily life [9]. The CWS can be used in a wide range of age groups, including people with no history of cancer. Patients with UC may be affected by depressive disorder and other mental health issues [10], chronically plagued by defecation and abdominal symptoms, and may be concerned about an increase in colorectal cancer.

We, therefore, aimed to investigate the state of awareness regarding cancer in patients with UC, as well as their concerns about cancer, awareness of risk factors, and information-gathering methods. We also examined the psychological impact of the CWS in patients with UC and investigated the characteristics those who were prone to worry about cancer development. The results of this study may improve the possibility to educate patients with more accurate and appropriate information and provide scientific explanations as the basis for shared decision-making so that they accept surveillance colonoscopy based on the result of this study.

This quantitative, self-administered questionnaire study was conducted at Akita University Hospital and Omagari Kosei Medical Center, Japan, from December 2023 to April 2024. Patients with UC visiting the hospitals regularly were informed about the study and asked to answer a questionnaire. The questionnaire included the CWS, Short Form-8 (SF-8), Inflammatory Bowel Disease Questionnaire (IBDQ), perspective of developing colorectal cancer in UC, and how to obtain information about the disease. Patients’ medical information and data were collected from their electronic medical records, including age, sex, disease recurrence in the last year, partial Mayo Score (PMS) at the time of enrollment into the study, maximum PMS in the past, and medication. The PMS consists of three categories (bleeding, stool frequency, and physician assessment) rated from 0 to 3, which are summed to give a total score ranging from 0 to 9, [11] with higher scores indicating more clinical severity. Disease recurrence was defined as the state in which PMS increased by 3 points from baseline and treatment was changed.

In addition to three standardized questionnaires, participants were asked about their perception of developing colorectal cancer regarding UC, the risks of UCAN, and how to access information about the disease. The questions were addressed as “How do you find out information about ulcerative colitis?,” “Do you know that ulcerative colitis increases the risk of colorectal cancer?,” “How do you know and find out more about ulcerative colitis causing cancer?,” “How do you find out more about cancer caused by ulcerative colitis?,” and “Do you know the risk factors for developing cancer from ulcerative colitis?”

The CWS assesses the intensity of worry about developing cancer and its effects on mood and activities in daily life. The scale comprises eight-item questions, with each rated on a four-point Likert scale ranging from 1 (“never”) to 4 (“almost always”) [8]. The possible scores range from 8 to 32, with higher scores indicating greater worry. The CWS for gastric cancer was compared to that of colorectal cancer. In this study, a score of 13 or more was considered positive for cancer worry [12].

The SF-8 assesses subjective health on eight items, with higher scores indicating better quality of life (QOL) [13]. The score comprises two summary scores which display the level of physical health “Physical Component Summary (PCS),” and mental health “Mental Component Summary (MCS).” The national standard values for the scores were presented in this study; the average score was 50, with higher values indicating a better QOL. The Japanese SF-8 was licensed by Quality Metric (Durham, USA).

The IBDQ is a validated form for QOL specific to IBD patients with 32 items on four domains of well-being, including bowel and systemic symptoms, and emotional and social function [14]. All items comprise seven-point Likert-type scales, and the total score ranged from 32 to 224. Higher scores indicated better QOL. The IBDQ was provided under a license from McMaster University.

The study protocol was approved by the Ethics Committee of Akita University and the participating institutes (2,620). Informed consent was obtained from each individual to participate in the study.

Continuous and categorical variables are expressed as median (standard deviation [SD]), and the number (proportion) was compared using Student’s t test and the chi-square test, respectively. Ordinal scales were expressed as median (interquartile range) and compared using the Mann-Whitney U-test. A pairwise t test was performed to compare the CWS for colorectal cancer and gastric cancer. All statistical analyses were conducted using the EZR software program, and p < 0.05 were considered statistically significant.

A total of 112 patients with UC were recruited, and all patients answered the questionnaires. The patient demographics are presented in Table 1. The median age of the study participants was 49 years (SD, 15.6), and 60.7% were male. The disease duration was 6 years (SD, 8.9), and over half of the disease extension was total colitis. Most patients were in clinical remission at entry into this study, with a median PMS of 0 (SD, 1.2). The maximum PMS score in the past was 6 (SD, 1.8), indicating that most patients experienced moderately active symptoms. Twenty-seven patients (24.1%) experienced active flares in the previous year. Fifty-four patients (48.2%) received advanced therapies, such as biologics or JAK inhibitors. The SF-8 scores of 52.3 (SD, 4.5) with 52.6 (SD, 4.5) of MCS and 53.5 (SD, 4.8) of PCS exceeded the mean. The total IBDQ scores were 170 (SD, 28.5), 54 (SD, 10.0), 28 (SD, 4.9), 65 (SD, 11.9), and 26.5 (SD, 5.6) for the bowel symptoms, systemic symptoms, emotional function, and social function components, respectively.

Seventy-eight patients (72.2%) perceived a risk of developing colorectal cancer. Younger male patients were more likely to know the cancer risk; however, disease severity, duration, and treatment were not associated with this perception. SF-8 and IBDQ scores were not associated with perception. While the CWS for gastric cancer was not associated with the perception, a higher CWS for colorectal cancer was associated with the perception of developing colorectal cancer in UC.

The median CWS was 15 (SD, 3.1) for colorectal cancer, which was significantly higher than that of 12 for gastric cancer (SD, 3.6), which was questioned for comparison with colorectal cancer. Most patients (73.9%) were positive for CWS against colon cancer, whereas less than half (43.2%) were positive for gastric cancer (Fig. 1).

As shown in Figure 2, most participants asked doctors at the hospital (77.6%) or used the internet and SNS (73.8%) to access information about UC. Of the patients who answered that they perceived developing colorectal cancer with UC, 71.4% asked doctors and 79.2% searched the internet and SNS; furthermore, 70% found out more details about developing cancer by asking doctors and 85.7% used the internet and SNS, which indicated that patients frequently utilized the internet and SNS on their own.

Risk factors for colorectal cancer in patients with UC have been reported to include early onset, total colitis type, disease duration, disease severity, family history of colorectal cancer, and comorbidity with primary sclerosing cholangitis [15]. Although half of the number of patients noticed the risk factors for the long duration of the disease, they did not know much about other factors, such as early onset, severity, and family history. Most patients (62.5%) wanted to know the cause of the disease, and approximately 50% of patients liked to ask about the treatment, the adverse events, and the diet.

In the analysis of the factors associated with CWS in Table 2, the IBDQ score, which is specific for QOL in patients with IBD, especially bowel symptoms, systemic symptoms, and emotional function, was associated with positive results for CWS. In the SF-8, a lower MCS was also associated with a positive CWS. Those with UC who perceived the risk of developing colorectal cancer also showed increased CWS. Sex, age, PMS, recent recurrence, and treatment were not associated with the CWS.

We evaluated the extent to which worry about developing cancer in patients with UC affected mood and daily lives, and examined the factors most likely to be associated with anxiety. Concerns about cancer were revealed in UC patients, especially for colorectal cancer, which was more evident than that for gastric cancer. As expected, patients were affected by the psychological burden of cancer in their daily lives. Survey results showed that 71.9% of patients with UC perceived a risk of developing colorectal cancer. UC is a common disease among the working generations who are familiar with accessing information through the internet. This study revealed that most people obtain information about the disease through the internet and SNS, and use the internet more frequently to obtain further information about colorectal cancer in addition to asking medical staff. Therefore, it is necessary to make patients aware of reliable educational sites, so that they can access accurate information. Further evidence and precise information are needed so that patients can better understand UC.

Patients with UC are mentally affected, such as by depression due to chronic symptoms and anxiety about recurrence even in the clinical remission stage, or being vulnerable under brain-gut interaction [16]. Anxiety about developing cancer is known to be higher in people with a history of cancer [17] or those at a hereditary higher risk, such as in familial adenomatous polyposis [8]. However, cancer worry does not necessarily increase among individuals with a family history of cancer [18]. Thus, the psychological impact of cancer development may differ depending on the patient’s background and disease.

Patients with UC have low QOL due to chronic physical symptoms and the psychological burden of repeated relapses [19]. The IBDQ, which is commonly used as a QOL score validated for IBD patients with disease-specific items, can evaluate bowel and systemic symptoms and emotional and social function [14]. The median IBDQ score in this study of 170.5 indicated that approximately half of the cohort was in IBDQ remission, as a score of 170 or above is considered remission in most clinical trials. Bowel and systemic symptoms, emotional function, and total IBDQ scores were associated with CWS. CWS-positive individuals tended to have lower social function sub-scores, but the difference was not significant. IBD-specific questions on QOL suggested that worsening physical and emotional symptoms impose a particular daily psychological burden with CWS. On the other hand, in this study, PMS was not associated with CWS, which was thought to be because most of the subjects were in remission (PMS median, 0). In addition, CWS may not be less associated with objective severity rather than subjective scores such as IBDQ, but this remains to be investigated in the future.

The SF-8 is a simple health-related QOL instrument that provides a national standard-based assessment score adjusted for sex and age, which comprises sub-scores for general physical and mental health. SF-8 scores in the participants in this study were above average, indicating that patients were not always affected by their general QOL in clinical remission. On the other hand, SF-8 was correlated with the CWS in UC and with mental activity. Mental health itself was associated with cancer worry regardless of the cause, which is consistent with the positive results for the CWS due to worsening emotional symptoms in the IBDQ.

Patients with UC, especially those with risk factors for developing cancer, such as young onset, pancolitis phenotype, long-term disease, severe disease, family history of colorectal cancer, and concomitant primary sclerosing cholangitis, are recommended to undergo regular surveillance colonoscopy [15, 20]. However, when performing invasive endoscopic examinations, it is necessary to provide patients with evidence to gain understanding. Patients with UC in clinical remission are numerically the major and important subjects for surveillance endoscopy. Even in symptomatic remission, some patients show active inflammation endoscopically, which may cause inflammatory carcinogenesis [21]. Based on the results of the IBDQ in this study which included ten items for their subjective bowel symptoms, if bowel symptoms affected their QOL, CWS was high and could be a motivation for receiving endoscopy; however, it is also necessary to explain the evidence sufficiently to get patients in remission to accept the need for invasive endoscopy. Furthermore, the lower CWS in patients who did not perceive the risk of cancer suggests the need to disseminate the evidence of the risk of developing cancer and the current data to patients who are unaware of cancer, which is important to improve surveillance endoscopy. In this study, we did not include risk factors for general colorectal cancer such as smoking, drinking, obesity, meals to investigate cancer worry for UC-associated neoplasm. To assess total personal CWS, it should be also considered to have comparison with non-UC individuals in future.

Patients with UC are affected by cancer concerns. More scientific evidence, reliable information that patients can access, and accurate information conveyed by the medical staff are required to practice UC medicine.

The study protocol was approved by the Ethics Committee of Akita University and the participating institutes (2,620). Informed consent was obtained from each individual to attend the study. Written consent forms were obtained from all patients.

The authors have no conflicts of interest to declare.

This study was not supported by any sponsor or funder.

Conceptualization and methodology: Yosuke Shimodaira and Katsunori Iijima. Data acquisition: Yosuke Shimodaira, Sho Fukuda, Tatsuki Yoshida, Kenta Watanabe, Tamotsu Matsuhashi, and Kengo Onochi. Formal analysis and investigation: Yosuke Shimodaira, and Kenta Watanabe. Writing – original draft preparation: Yosuke Shimodaira. Writing – review and editing: all authors.

The data that support the findings of this study are not publicly available due to their containing information that could compromise the privacy of research participants but are available from the corresponding author upon reasonable request.