Frailty, Illness Perception and Lung Functional Exercise Adherence in Lung Cancer Patients After Thoracoscopic Surgery

Introduction

Lung cancer is the world’s highest morbidity and mortality disease.¹ The impact of the novel coronavirus epidemic,² some people have cough, dyspnea and other symptoms, which have caused attention to the examination.³ As People’s health awareness increases, they participated in physical examinations, and more lung cancer patients have been detected through detailed imaging examination.⁴ Early stage lung cancer patients with small symptoms were also widely detected.⁵ Early detection and early treatment are the main treatment methods for cancer patients to improve life expectancy.⁶ Thoracoscopic surgery is a common method for the diagnosis and treatment of lung diseases.⁷ This technique is characterized by short operation time, less trauma, and quick recovery,⁸ but the decline in lung function and not dependent on recovery is worrying.⁹ Although the length of hospitalization is short, the recovery of lung function needs to continue. Patients may not pay attention to postoperative exercise compliance (cough, get out of bed early, deep breathing, balloon blowing, and so on), resulting in increased complications such as atelectasis or discharge which may increase the readmission rate.^10,11 Compliance with lung function exercise plays an important role in postoperative recovery.¹²

Disease perception is the core factor in the common-sense model of self-regulation. It is the cognitive and emotional representation of the patient’s own disease, and these representations influence the patient’s response to the disease.¹³ This model recommends exploring the early stages of the disease and intervening.¹⁴ The model also supports surgical recovery behavior, explaining that patients can implement health management plans by understanding changes in their disease.¹⁵ A review has shown that disease perception was measured before and after intervention to evaluate the intervention effect of the self-regulating common-sense model on behavioral compliance.¹⁶ The effect of disease perception on patient compliance with disease and interventions has been studied in other diseases. Disease perception was associated with medication compliance, glycemic control, and compliance with cardiac rehabilitation programs.^17–19 For lung cancer patients, the relationship between disease perception and exercise compliance still needs to be explored.

Frailty is related to age. Most of the research focuses on the elderly. However, according to the concept of frailty, the body becomes vulnerable to a variety of stressors, including hospitalization, surgery, and cancer and aging.^20–22 The incidence of frailty in lung cancer patients was 45%.²³ After surgery, it can be debilitating due to the loss of ability to carry out daily activities such as wound pain.²⁴ Frailty affects patients’ health outcomes, and frailty affects patients’ functional recovery and quality of life.²⁵ Studies have shown that frailty will affect the post-operative effects of cancer patients.²⁶ In terms of rehabilitation compliance, colorectal cancer postoperative rehabilitation compliance and abdominal surgery rehabilitation compliance are related to frailty.^27,28 In addition, studies have shown that faltering of hemodialysis patients can most affect the compliance.²⁹ However, what is the weak state of lung cancer patients after thoracoscopic surgery, and whether it affects the compliance, we need to explore.

Study Hypothesis

The common-sense of self-regulation model is grounded in illness perception, describing how patients make sense of changes in health threats and develop and assess management plans. In view of this theory, it is important to assess patients’ perceptions and expectations for thoracoscopic postoperative rehabilitation, which will actively promote patients in their own healthcare, and provide adequate support during the transition to home.¹⁵ The conceptual model considers broader mediating factors.¹⁶ Previous studies have explored the relationship between drug belief as mediator and drug compliance, and the relationship between disease perception as mediator and psychological distress.^30,31 The model also provides a basis for us to explore the relationship between frailty, disease perception and lung function exercise compliance in lung cancer patients after thoracoscopic surgery. Based on the literature review and common-sense model, we will explore the mediating role of illness perception in the frailty of lung cancer patients after thoracoscopic surgery and lung function exercise adherence (Figure 1).

Figure 1 The Hypothetical model about explanatory factors used in mediation analysis. Notes: In this hypothetical model: 1. The influence coefficient of influence of frailty X on disease perception M is a; 2. The influence coefficient of disease perception M on lung function exercise adherence Y is b; 3. The influence coefficient of frailty X on lung function exercise adherence Y is c’. Exploring the mediation model will involve two regression equations of the influence coefficient: 1.M = Constant 1+a × X 2.Y = Constant 2 +b × M +c’ × X Therefore, 1. The indirect effect of frailty X on lung function exercise adherence Y through illness perception M is ab; 2. The direct influence of frailty X on lung function exercise adherence Y is c’; 3. The total effect of frailty X on lung function exercise adherence (Y) c=c’+ ab.

We propose the following hypothesis:

H1: Frailty has a positive effect on disease perception;

That’s why we wanted to do this study: (1) The clinical status of patients undergoing thoracoscopic surgery for lung cancer is few studies. (2) To explore the influencing factors of postoperative pulmonary function exercise compliance and whether disease perception is beneficial to the self-management of postoperative rehabilitation behavior. (3) Based on the self-regulation common-sense model, we need to explore whether the patients’ disease cognition and emotion are affected by the debilitating state, and whether it will affect the rehabilitation exercise behavior.

Materials and Methods

Sample and Setting

A cross-sectional survey of patients undergoing cardiac and thoracic surgery in the affiliated Hospital of Jiangnan University in Wuxi, China, from October 2022 to April 2023. Patients who meet the following criteria are eligible for registration: (a) Everyone must be over the age of 18; (b) Thoracoscopic surgery was first performed to remove the tumor; (c) The imaging diagnosis was pulmonary nodules or intraoperative pathological puncture showed lung cancer; (d)Survey those who have no mental retardation, are good at speaking and understanding, and are willing to cooperate. These patients will be excluded: (a) The patient had metastatic tumor disease; (b) non-Lung cancer patients confirmed by postoperative pathology and diagnosis in accordance with the 2021 WHO Classification of Lung Tumors.³²

The Ethics Committee of the Jiangnan University approved the present research, the Reference Number is JNU20221201IRB37.

Data Collection

All registered participants adopted the convenient sampling method. The investigators engaged in this study have been trained to score the correct content and scale, and to present the purpose and content of the scale to qualified patients in a consistent form. All patients signed a written consent form before taking part in the trial. In the form of individual interviews, distribute questionnaires, collect information, and collect and review in the field. In the process of collecting data, the patient will fill in the data, and then we will talk to the patient to better achieve the patients’ authentic information. The recovered questionnaire was checked twice to ensure the correctness of all data entries. The time of assessment was after thoracoscopic surgery.

Study Variables and Instruments

Demographic and clinical questionnaires collected data including patient name, hospitalization number, age, sex, culture, BMI (body mass index), hypertension, diabetes, double nodules, time from diagnosis to surgery, cancer, location of surgery, lymphatic clearance, postoperative fever, postoperative stool, pain, sleep, preoperative time, postoperative time, the first day of drainage, total postoperative drainage, time to drain tube placement. Location of surgery, hypertension, diabetes, double nodules, location of surgery, lymphatic clearance were obtained through patient records and physician reports. Preoperative time, postoperative time, the first day of drainage, total postoperative drainage, time to drain tube placement were collated by looking at electronic medical records.

BMI was divided into three groups based on normal weight (18.5 ≤ BMI < 25 kg/m²): <18.5, 18.5≤BMI <25, >25.³³ Time from diagnosis to surgery refers to how long after a diagnosis of lung disease is found to be treated, and it’s divided into three periods, one month, one month to a year, and over a year. Classification of lung cancer is based on postoperative pathological results.³² Postoperative fever and postoperative stool were asked whether the patient had the situation within three days after surgery. The pain was scored using the NRS pain scale.³⁴ The patient was given an analgesic pump for 1 day after surgery, if the patient was not allergic to the drug. Patients who report pain may use pain medication or painkillers. Regardless of whether the patient takes medication, the patient’s feeling about pain is the standard. Sleep was assessed by whether patients reported good or bad sleep in the days after surgery, and by whether they used sleeping pills.

Frailty

Frailty was assessed by the Groningen frailty indicator (GFI). The GFI consists of 15 questions regarding the following domains of life: physical domain, cognitive domain, social domain, and psychological domain, generating a score ranging from 0 to 15. Frailty was defined as a GFI score ≥4. The Cronbach’s α scale was 0.712 in lung cancer patients.³⁵

Illness Perception (BIPQ)

The Chinese version of BIPQ was utilized to quantify illness perception. This scale consists of 8 items divided into three parts and 1 item analyzes the cause of the disease. (1) Items 1–5 (Consequences, Timeline, Personal control, Treatment control, Identity) make up dimension 1 for representation; (2)a second section for emotion consisting of item 6 and item 8 (Concern, Emotional response); (3)item 7 (Illness coherence) represents the knowledge of illness. The BIPQ assesses the cognitive dimensions (represented by items 1, 2, 3, 4, and 5), emotional dimensions (items 6 and 8), and comprehensibility (item 7) of illness perceptions in an objective manner. The Cronbach’s α scale was 0.931 in lung cancer patients.

Each item has 10 scores, with 3 items being reverse-scored (items 3, 4, 7). We have inverted the data of these entries in the statistics, so the total score of this scale is 80 scores. Higher illness perception scores correspond to negative views regarding how a patient’s illness impacts their health.³⁶

Exercise Adherence

The Exercise Compliance Questionnaire is a 15-item questionnaire using a numeric scale (0–4, ranging from strong disagreement to strong agreement), with higher scores indicating greater adherence to exercise. The Cronbach’s α scale was 0.86 in lung cancer patients.³⁷

Statistical Analysis

In multifactor analysis, the sample size is usually calculated as 5–10 times of the influencing factors of the study variable lung functional exercise adherence, and 20% of the invalid sample size is considered.³⁸ According to Kendall’s principles, the estimated sample size is 138–276 cases. We need to meet the structural equation model’s minimum sample size of 200 cases by Boomsma A’s research,³⁹ so we will collect more than 200 patients. All valid questionnaires were written by responders and reflected the reality of communicating with patients. Descriptive statistics for all variables were calculated using Statistical Package for the Social Sciences (SPSS) version 25.0 and PROCESS version.

Descriptive analyses (frequencies, percentage, mean, and standard deviation) were used to characterize participants’ baseline information, which were compared between low illness perception and high illness perception patients by the chi-square (χ²) test or independent-samples t-test as appropriate. When the two sets of squares are different, the Mann–Whitney test is used. We analyzed the influencing factors of lung function exercise compliance. First, we used t-test, Mann–Whitney test, variance test, and Pearson’s correlation, then conducted linear regression analysis of variables and collinearity analysis to see if the value was < 5. Durbin-Waston diagnosed the independence of the error term.⁴⁰ Pearson’s correlation was adopted to test the coefficient correlation (r) among frailty, illness perception, exercise adherence. To further determine whether and to what illness perception mediated the association between frailty and exercise adherence, then a simple mediation model was conducted. Afterwards, the bootstrapping method with 5000 resamples was applied to test the mediating effect of frailty using the PROCESS macro in SPSS. We assessed the bias-corrected bootstrap confidence intervals (CI) of indirect effects, which were considered significant if the upper and lower bounds of the 95% CI did not straddle zero.

Results

Participant Demographics and Clinical Characteristics

A total of 242 eligible patients after thoracoscopic surgery were recruited to participate in the survey study, then eventually 218 patients were enrolled (Figure 2). Twenty-four patients were excluded because they did not have lung cancer. As shown in Table 1, the mean age of the participants was 60.27±0.881 years, 125 (57.3%) patients of whom were female. We classified low disease perception and high disease perception by a median score of 33.5. Furthermore, Lymphatic clearance (χ²=7.390, p=0.007), Postoperative stool (χ²=4.788, p=0.029), Pain (z=−2.648, p=0.008), frailty (z=−5.343, p<0.001), exercise adherence (z=−3.280, 0=0.001) showed a statistically significant association with high illness perception.

Figure 2 The enrollment of study samples.

Table 1 Baseline Characteristics of the Study

The mean lung functional exercise adherence of the participants was 36.93±12.053 scores. Age (r=−0.171, p=0.012), Cancer (t=10.482, p=0.033), Postoperative fever (t=4.305, p<0.001), Pain (r=−0.177, p=0.009), sleep (t=−3.24, p<0.001), postoperative time (r=−297, 0=0.001), the first day of drainage (r=−0.148, p=0.029), total postoperative drainage (r=−0.283, p<0.001), time to drain tube placement (r=−0.308, p<0.001), frailty(r=0.439, p<0.001), illness perception (r=−0.327, p<0.001) showed a statistically significant association with exercise adherence.

Descriptive Statistics for Illness Perception

According to the total BIPQ score for 34.784±12.084 in Table 2, patients expressed a relatively high degree of concern regarding their illness. The lowest mean score of illness perception is treatment control.

Table 2 Descriptive Statistics for Illness Perception

Linear Regression Model for Frailty and Illness Perception on Exercise Adherence

From the difference analysis and correlation analysis of exercise compliance, it is concluded that in addition to the target independent variables of frailty and disease perception, there are other independent variables interference, so we conducted a linear regression analysis (Table 3). According to the results of Model 3, the model has a good fit, and the adjusted R square is 0.232, which means that the influence degree of the independent variables involved in this regression analysis on the dependent variables reaches 23.2%, indicating that this regression model can better explore the influencing factors of lung cancer patients’ postoperative functional exercise compliance. The linear regression model was significant (F=5.674, p < 0.001), indicating that at least one of the 11 independent variables could significantly affect the dependent variable lung function exercise compliance. Further, combined with the test of the regression coefficient of the independent variables, it can be concluded that postoperative fever significantly negatively affects the pulmonary function exercise compliance, with an influence coefficient of −5.188 (t=−2.686, p=0.008), indicating that fever may lead to poor exercise compliance. Frailty can significantly negatively affect compliance, and the influence coefficient is −1.084 (t=−3.239, p=0.001), that is, the higher the degree of frailty, the worse the exercise compliance. Disease perception can significantly negatively affect compliance, and the influence coefficient is −0.167 (t=−2.366, p=0.019), that is, the higher the disease perception, the more negative emotions, the worse the exercise compliance. In addition, pathological classification of cancer, postoperative time, the first day of drainage and total drainage volume, drainage tube placement time, sleep and pain status may not be influencing factors for compliance. According to the results analyzed in our investigation, these independent variables have no significant relationship with exercise compliance (p > 0.05).

Table 3 Linear Regression Model for Frailty and Illness Perception on Exercise Adherence

Correlates of Illness Perception, Frailty, Exercise Adherence

To further examine the correlation, a Pearson’s correlation coefficient was performed in Table 4. Frailty was positively correlated with illness perception (r=0.439, p<0.01). Illness perception (r=−0.327, p<0.01) was negatively correlated to exercise adherence. Frailty (r=−0.398, p<0.01) was also negatively connected to exercise adherence.

Table 4 Correlates of Illness Perception, Frailty, Exercise Adherence

Mediation Analysis of Illness Perception on the Relationship Between Frailty and Exercise Adherence

As shown in Figure 3, the results of a simple mediation model testing, using Model 4, indicated that frailty inversely predicted exercise adherence (β=−1.061, p<0.01) and positively predicted illness perception (β = 1.896, p<0.01). After that, our results also revealed a significant indirect effect of illness perception on exercise adherence (β= −0.338, p<0.01). Bootstrap results for the mediation analysis that the confidence interval does not include zero, suggesting that illness perception only played a partial mediating role in the association between frailty and exercise adherence. The indirect effect accounted for 24.14% of the total effect (Table 5).

Table 5 Bootstrap Results for the Mediation Analysis

Figure 3 The established structural equation model for frailty and illness perception on exercise adherence. Notes: **p<0.01. The structural model is checked with Model number 4 and number of bootstrap samples are 5000. Covariates: age, pain, cancer, postoperative fever, sleep, postoperative time, the first day of drainage, total postoperative drainage, time to drain tube placement.

Discussion

In this study, the clinical status, frailty, disease perception, and postoperative lung functional exercise compliance of patients with thoracic lung cancer were investigated.

Most of the lung cancer patients we investigated who chose thoracoscopic surgery were middle-aged and elderly, and the average age were 60.2±0.881. For patients who can undergo surgery, some of them are asymptomatic patients before surgery, so postoperative symptoms and lifestyle changes may change patients’ thoughts on the disease and treatment and cause psychological burden.^41,42 As our results show, there is a difference in the negative and positive perception of the disease in terms of physical frailty, chest tube placement, fever for three days after surgery, and no bowel movement. The average perceived disease score in our study of people with lung cancer was 34.78±0.818. A comparison of previous studies showed that stage 1 and stage 2 breast cancer had a disease perception score of 32 to 35 after surgery.⁴³ Therefore, our survey was of reference significance. In addition, item 9 of disease perception is an open answer to the cause of disease. Echoing the high-risk factors seen in lung cancer screening,^44,45 69 person-time showed smoking, environmental fumes, dust. In the past two and a half years since the COVID-19 outbreak and vaccination, 45 cases believed that these have been blamed for lung deterioration. The reasons mentioned by other patients also need attention, bad living habits, drinking, staying up late, little exercise, irritable or stuffy mood, body constitution is not good. As the patient said, “there are no symptoms, and I don’t smoke” and “The doctor said that the image is not good and needs treatment, so i had a choose for surgery”. According to our survey, most patients want to know about disease in detail.

The high or low disease perception score affected patients’ perceptions of the disease. The higher the score, the negative disease perception affected patients’ psychological burden, which was associated with adverse outcomes, worse quality of life, and poor self-management behavior.^46,47 We found that the higher the negative score of disease perception, the worse the compliance. In our study, although surgery is considered of great help to the disease (perhaps patients strongly agree with the idea of early diagnosis and early treatment), patients still worry about the disease.⁴² Patients’ awareness of the disease and emotions also have an impact on compliance, such as pulmonary rehabilitation.⁴⁸ This is the same as the self-regulation common sense model, in which patients who are aware of the health threat of physical differences and cancer after surgery develop emotional responses and cognition to the threat, so that it affects behavior.^49,50 In our study, the frailty measurement after lung cancer surgery was 43%, and the previous study showed that lung cancer patients were 45%.²³ Therefore, we believe that the research results are valuable for reference. Frailty is not exclusive of the elderly, frailty and age related, but young middle-aged frailty is not rare.⁵¹ The effect of surgery on patients can make patients who are still weak or patients who are not weak become weak patients,²¹ therefore, the assessment of frailty after surgery can better understand a patient’s state after experiencing many stressors. Previous studies have measured frailty in patients undergoing vascular surgery.³⁵ And studies have shown that the debilitating evaluation of patients with surgery and cancer is beneficial to explore the quality of life, survival rate and recovery effect of patients.⁵² Our results show that frailty is negatively correlated with compliance, this indicates that the health status of the patients after surgery needs our attention.

We found that illness perception mediated the relationship between the frailty and lung functional exercise adherence of lung cancer after thoracoscopic surgery. The path analysis results showed that the indirect effect accounted for 20.91% of the total effect. Postoperative clinical symptoms and signs will cause patients to feel more frailty, thus affecting patients’ perception of the disease. In addition, the common-sense model of self-regulation points out that negative cognition and emotion about the disease will choose negative behavior, that is not conducive to the recovery of the disease. Disease perception needs to adapt to different populations and scenarios, so we explored the situation of lung cancer after thoracoscopic surgery. Postoperative chest tube retention, fever, stool, other relevant patient care also need our attention. It’s consistent with our research that some of the symptoms after surgery can affect our perception of the disease and also affect our recovery.^53,54 Reacquaint themselves with their bodies after treatment for operable lung cancer, and encourage the patient to rebuild his or her identity recognition, thus resume their daily lives.⁵⁵ As for the measurement of lung functional exercise compliance, our previous research evidence found that there was no uniform regulation of the number, content and time of exercise measures.^56,57 This made it difficult for us to investigate, and we used a scale that had been validated in domestic lung cancer patients,³⁷ After that, we hope to have relevant studies to quantify postoperative exercise and objective tools to measure.

The weakness of this study is that our design is cross-sectional, so longitudinal surveys or more variables over different time periods are needed to predict lung functional exercise compliance. We study a small sample of people, based on more comprehensive and extensive exploration of the self-regulation common sense model, we hope to have a larger sample size after that. We want to a multicenter survey, because it will make the research more universal and reliable.

Conclusion

In this study, a model of disease perception was used to explain the effects of patient clinical information, patient psychosomatic social cognition, frailty, and disease perception on exercise compliance in lung cancer patients after thoracoscopic surgery. The findings suggest that disease perception can be used as one aspect of improving postoperative compliance, and that clinical fever, physical recovery, caregivers, and psychology should also be considered as important components of intervention programs when formulating interventions.