The fear of cancer recurrence in elderly patients after endoscopic submucosal dissection for early esophageal cancer: a cross-sectional study

Introduction

Esophageal cancer is a common malignant tumor of the digestive system, and has high incidence and mortality rates worldwide (1). In recent years, with the rapid development of endoscopic technology, endoscopic submucosal dissection (ESD) has become the preferred method to treat early esophageal cancer (2). This technique can effectively resect the lesion and maximally preserve the function and integrity of the esophagus, which is of great significance in improving the quality of life of patients (3,4). However, despite the remarkable success of ESD in clinical settings, the risk of cancer recurrence in postoperative patients remains. This risk not only arises from the biological characteristics of the tumor but is also closely related to the psychological state of the patient (5).

The fear of cancer recurrence (FCR) is defined as “fear, worry, or concern relating to the possibility that primary cancer or subsequent malignancy will return or progress to other parts of the body” (6,7). FCR is a common psychological phenomenon among cancer patients, especially those who have undergone surgical treatment. Patients’ worry about FCR may be further aggravated by surgical treatment, affecting their postoperative quality of life, recovery process, and psychological health (8,9). Due to their relatively weaker physical functions, limited psychological tolerance, and insufficient knowledge of cancer and its treatments, elderly patients are more prone to fear and anxiety of disease recurrence (10,11). As mentioned above, elderly patients after ESD for early esophageal cancer are more likely to exhibit high levels of FCR.

Disease perception and coping styles have been reported to be important factors of FCR in cancer patients (12,13). This fear may not only cause patients to be overly concerned with their health, frequently visit doctors for check-ups, and increase the burden of medical treatment, it may also affect their daily lives, such as eating and sleeping, and could even lead to the occurrence of psychological disorders, such as depression and anxiety (14,15).

At present, the data about the FCR in elderly patients after ESD from China are lacking, so an in-depth understanding of FCR and its relevant factors in elderly postoperative ESD patients with premature esophageal cancer is of great significance to the development of effective psychological interventions and improvement of patients’ quality of life.

This study aimed to assess FCR in elderly postoperative ESD patients with premature esophageal cancer and to explore its relevant factors to provide a scientific basis for the development of individualized psychological interventions in clinical practice. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1567/rc).

Methods

Study design and study population

This cross-sectional study was conducted from June 2022 to June 2023 at the Department of Gastroenterology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University in Nanjing, Jiangsu Province.

To be eligible for inclusion in this study, the patients had to meet the following inclusion criteria: (I) have undergone ESD; (II) have postoperative pathology results suggesting esophageal intraepithelial neoplasia, intramucosal carcinoma, or submucosal carcinoma; (III) be aged ≥60 years old; (IV) have a clear state of consciousness, and the ability to communicate and understand effectively; and (V) voluntarily participate in this study and sign the informed consent form. Patients were excluded from the study if they met any of the following exclusion criteria: (I) were unaware of their condition and diagnosis; (II) had other types of malignant tumors or severe organic lesions; and/or (III) had undergone non-curative resection, or additional surgery.

According to Kendall sample size estimation principle (16), a total of 15 variables [10 in the general information questionnaire; two in the Fear of Progression Questionnaire-Short Form (FoP-Q-SF); one in the Brief Illness Perception Questionnaire (BIPQ); three in the Medical Coping Modes Questionnaire (MCMQ)] were designed in this study, and 90 to 180 cases were required considering the 20% sample shedding rate.

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Ethics Committee of Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing, China (Project No. 2022-607-02), and informed consent was taken from all the patients.

Measurements

The study subjects were carefully chosen based on the inclusion and exclusion criteria. After obtaining their permission when they left the hospital, the data of the patients were collected by phone calls and administering in-person or electronic questionnaires during a 1-month follow-up period. A consistent set of guidelines was used to explain the study’s purpose, importance, and the completion instructions to the subjects, who were evaluated once they completed the questionnaires.

General information questionnaire

The questionnaire was self-designed according to the purpose of the study and the literature review. The questionnaire comprised two parts, one directed at collecting demographic-sociological data (e.g., age, gender, place of residence, and education) and the other directed at collecting disease-related data (e.g., number of foci, pathological stage, and lesion length).

FoP-Q-SF

FoP-Q-SF was developed by Mehnert et al. based on the Fear of Progression Questionnaire (17). Wu et al. translated and revised the questionnaire into Chinese in 2015, and reported a Cronbach’s alpha coefficient for the FoP-Q-SF of 0.883 (18). The FoP-Q-SF comprises two dimensions (i.e., physical health, and social and family dimensions) with 12 entries. A 5-point Likert scale was used, with the total possible score ranging from 12–60 points, with higher scores indicating higher levels of fear, and a score of ≥34 indicating a level beyond normal fear (19).

BIPQ

BIPQ was developed by Broadbent et al. based on the Illness Perception Questionnaire and the Revised Illness Perception Questionnaire to assess patients’ level of illness perception (20). This study used the Chinese version developed by Mei et al. (21). This BIPQ comprises eight entries and one open-ended question (in which the patient analyses the leading causes of their illness). The first eight entries were scored on a 0–10 scale; the 9th entry was not analyzed for the purpose of this study. The total possible score of the questionnaire ranged from 0–80, with higher scores indicating that patients perceived the threat of the disease to be more severe and had a more negative view of the disease. The Cronbach’s alpha coefficient for the questionnaire was 0.77 (21).

MCMQ

MCMQ was developed by Feifel to assess the coping strategies adopted by patients in dealing with disease-related problems (22). Shen et al. revised it to establish a 20-item Chinese version that had three dimensions (i.e., confrontation, avoidance, and resignation) with each entry scored on a four-point Likert scale, in which eight entries (1, 4, 9, 10, 12, 13, 18, and 19) had to be reversed. The Cronbach’s α coefficients for the three dimensions were 0.69, 0.60, and 0.76, respectively, indicating good reliability and validity (23).

Statistical analysis

The data were analyzed using SPSS 27.0 (IBM, Armonk, NK, USA). General information is described as the frequency and percentage. The current status of the FCR is described as the mean, standard deviation, frequency, and rate. The data underwent a variance chi-square test, and the quantitative data conforming to a normal distribution were subjected to an independent sample t-test and a one-way analysis of variance to analyze the factors influencing the FCR. A Pearson correlation analysis was used to explore the correlation between the FCR and patients’ perceptions of the disease and coping methods. Additionally, a multiple stepwise regression analysis was conducted to analyze the main factors influencing the FCR. All tests were bilateral, and P<0.05 was considered statistically significant.

Results

FCR, disease perception scores, and medical coping style scores in elderly patients with early esophageal cancer after ESD

In total, 162 patients diagnosed with early esophageal cancer and treated with ESD participated in the study, of whom, 107 were male and 55 were female. The patients had a mean age of 69.96±5.19 years. The total FoP-Q-SF score of the elderly early esophageal cancer patients after ESD was 34.38±4.10, of which the physical health dimension score was 19.96±2.78, and the social and family dimension score was 14.40±2.23. The total FoP-Q-SF score of the elderly early esophageal cancer patients after ESD exceeded the average level (≥34) in 98 cases (60.5%). The total BIPQ score was 42.34±3.96. The MCMQ scores were 21.81±3.29 for the confrontation dimension, 15.02±1.72 for the avoidance dimension, and 10.88±3.84 for the resignation dimension.

Univariate analysis of the factors influencing the FCR in older patients with early esophageal cancer after ESD

Univariate analysis showed that different qualifications, number of lesions, pathological stages, lesion length, depth of infiltration and esophageal stenosis were significantly correlated with FCR in older patients with early esophageal cancer after ESD (P<0.05) (Table 1).

The results of the Pearson correlation analysis showed that the total FoP-Q-SF scores of the elderly early esophageal cancer patients after ESD were positively correlated with the BIPQ scores (r=0.424, P<0.001), negatively correlated with the confrontation dimension scores (r=−0.369, P<0.001), positively correlated with the avoidance dimension score (r=0.317, P<0.001), and positively correlated with the resignation dimension scores (r=0.523, P<0.001).

Multifactorial analysis of the factors influencing the FCR in elderly patients after ESD for early esophageal cancer

The total FoP-Q-SF score after ESD for early esophageal cancer in the elderly patients served as the dependent variable. The statistically significant variables in the univariate and Pearson correlation analyses served as the independent variables in the multivariate stepwise regression analyses (αin =0.05, αout =0.10). The coding of the independent variables is presented in Table 2. Four factors (i.e., education level, esophageal stenosis, the total perception of disease score, and the resignation dimensions score) were entered into the regression equation (Table 3).

Discussion

The results of this study showed that the FCR score in elderly patients with early esophageal cancer after ESD was 34.38±4.10. Of the patients, 98 (60.5%) had a score ≥34 for the psychological dysfunction of fear of disease progression, which was slightly higher than the score reported by Zhang et al. (24) for 300 patients with early esophageal cancer after surgery of 29.81±3.76, but lower than the scores for other categories in tumor patients (25). This may be because surgical resection is considered the first choice of treatment for esophageal cancer and can achieve good efficacy, which can primarily alleviate the psychological burden of FCR or fear of disease progression in esophageal cancer patients. However, the recurrence rate of early esophageal cancer within five years of ESD is 12.3%, so patients have different degrees of FCR after surgery (26). Conversely, the 5-year survival rate of esophageal ESD is 90%, with a good prognosis, which could affect patients’ FCR to a certain extent (27).

The results of the study showed that literacy level was an factor influencing the FCR in elderly patients with early esophageal cancer after ESD. The higher literacy level, the lower the level of FCR. It may be that the more educated the patients, the wider their access to information about the disease, the more comprehensive their knowledge about the disease, and the lower their FCR. In addition, elderly early esophageal cancer patients need long-term follow-up and regular reviews after ESD, but frequent checkups and diagnostic behaviors further aggravate the psychological stress reaction of patients. Patients with higher education levels can adapt to the disease condition more quickly, adopt positive coping styles, better regulate their negative emotions, and show improved compliance (28). Therefore, healthcare professionals should focus on patients with low education, such as the use of graphic and graphic brochures, shooting easy-to-understand popular science videos and other forms of education, to strengthen patients’ understanding of early esophageal cancer and ESD-related knowledge, so that they can better cope with the disease, and then reduce FCR.

The results of this study showed that esophageal stenosis is a factor influencing the FCR in elderly patients with early esophageal cancer after ESD. During the ESD of esophageal lesions by esophageal endoscopy, the incidence of esophageal stenosis can be as high as 88% if the lesion is more significant than 3/4 of the circumference of the esophagus (29). Esophageal stenosis often occurs about two to four weeks after surgery (30). In addition to the symptoms of dysphagia, it is usually accompanied by esophageal reflux, aspiration pneumonia, and retrosternal pain that seriously affect patients’ quality of life (31). Currently, post-ESD esophageal stenosis are often dilated with esophageal balloons or probe strips to improve patients’ dysphagia. However, patients usually need to make multiple trips to and from the hospital for dilatation, and there is still a possibility of recurrent stenosis (32). Some patients have severe stenosis at the time of presentation due to limited awareness, which also increases the frequency and period of treatment, and increases the risk of complications such as perforation and bleeding. The occurrence of esophageal stenosis aggravates the physical and mental pain of patients, which not only increases the costs of treatment but also increases patients’ worry about the effectiveness of surgery and their prognosis and further deepens the FCR. These results suggest that healthcare professionals should focus on patients who are prone to esophageal stenosis, carry out individualized monitoring and follow up for patients at high-risk of esophageal stenosis, and can promptly detect patients’ subjective symptoms, esophageal functional status, psychological reactions, and other comprehensive health statuses by constructing the PROMIS (Patient-reported Outcomes Measurement Information System) data collection platform. To achieve real-time collection, timely treatment and early warning, and give patients targeted health guidance, such as corresponding dysphagia symptoms, to remind patients to seek medical treatment in time, and track.

The fear of recurrence model states that the fear of recurrence includes both cognitive and emotional responses, and that negative perceptions of the disease, the fear of recurrence, and anxiety and depression brought about by the experience of cancer will increase the FCR level of patients (33). The results of this study showed that the more severe the patient’s perception of the disease, the higher the FCR level, which is consistent with the cancer recurrence fear model. Disease perception is the process by which patients use their previous knowledge and disease experience to analyze and interpret the current symptoms (or disease) (34). It may be that elderly patients with early esophageal cancer do not have enough knowledge of their disease condition and the complications that occur during treatment. Additionally, the increased sensitivity to and attention to physical symptoms contribute to patients’ concern about disease progression and recurrence, aggravating their level of FCR. A study has shown that cognitive-behavioral interventions can help cancer patients improve their disease perceptions, promote medical compliance, and reduce their FCR levels (35). Thus, healthcare professionals should use cognitive reconstruction and identify triggers to help patients establish positive disease perceptions, improve their disease self-management ability, reduce their psychological burden, and lower their FCR levels. On the basis of routine health education, patient groups, and online exchange meetings could be used to help to promote patients’ understanding and awareness of the disease, monitor patients’ follow-up visits and reviews. In relation to psychological care, patients could be guided to enhance their self-efficacy and could be provided with coping strategies to improve their negative perception of the disease and reduce their fear of disease progression.

Coping styles refer to the ability of individuals to maintain relatively stable behaviors or perceptions in the face of emergencies. Three coping styles have been identified: confrontation, avoidance, and resignation (36). The subjects in this study were elderly, their ability to access disease-related knowledge on the Internet and in books is difficult, and thus they only can consult medical staff during hospitalization and at regular follow-ups, which may cause them to experience feelings of pessimism and despair. Thus, elderly patients with early esophageal cancer have more negative coping styles than young patients. In addition, the post-sternal pain and esophageal stenosis brought about by treatment make elderly patients, who have a weak ability to recover, not only experience more physical pain but to also suffer from great psychological torture. Thus, elderly patients with early esophageal cancer are more inclined to adopt a resignation coping method. In the short term, adopting the resignation coping style can help reduce the occurrence of negative emotions. However, if used for an extended period, it may lead to a loss of confidence in patients, reduce subjective initiative, aggravate the accumulation of destructive emotions, and further aggravate the FCR. The frequency of multiple and metachronous esophageal cancers after ESD ranges from 12.5% to 35.8%, highlighting the importance of surveillance (37). Therefore, healthcare professionals help patients carry out self-effective management, timely reminders, and the supervision and tracking of the implementation of patients’ regular esophageal review work, as well as responding to the disease positively.

Conclusions

This study showed that 60.5% of the elderly early esophageal cancer patients had FCR, and the level of FCR was higher in patients with a low level of education, esophageal stenosis, a high total disease perception score, and a high submission dimension score. Medical personnel should develop a plan and intervene to address the factors affecting the FCR in elderly patients with early esophageal cancer to reduce their levels of FCR. This study was conducted with a small sample size of early esophageal cancer patients admitted to a tertiary care hospital and was a cross-sectional study. In the future, large-sample size studies will be conducted to further investigate changes in the FCR among elderly patients with early esophageal cancer at different stages of the disease.

Acknowledgments

Funding: This study was supported by the Nanjing Drum Tower Hospital Nursing Research Key Projects (No. 2023-H444), and the Nanjing Drum Tower Hospital Nursing Research Project (No. 2023-A266).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1567/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1567/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1567/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-24-1567/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). This study was approved by the Ethics Committee of Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing, China (Project No. 2022-607-02), and informed consent was taken from all the patients.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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