Self-management positivity and its influencing factors among lung cancer patients: A cross-sectional study.

1. Introduction
Lung cancer is the most commonly diagnosed cancer among both men and women, and it is one of the leading malignant tumors causing death globally due to its relatively late diagnosis, poor treatment outcome, and high prevalence.[1] For instance, there were about 2.2 million new lung cancer cases worldwide in 2020, and approximately 1.8 million new deaths were confirmed in the same year.[2] Its incidence has shown an upward trend in many countries recently. Smoking, air pollution, occupational exposure and genetic suspectibility have been confirmed as the high-risk factors of lung cancer.[3] Although the recent improvements in early diagnosis and new treatment options, such as molecular-targeted therapies and immunotherapies, the 5-year survival rate of lung cancer patients is still very low.[4] Small cell lung cancer (SCLC) accounts for about 15% of lung cancer cases and non-small-cell lung cancer (NSCLC) by far the most common form, representing about 85% of all lung cancer cases.[5] Operation is still the most effective treatment method, and a comprehensive treatment mode mainly based on surgery is suitable for most of patients with NSCLC and partial patients with SCLC.
Lung cancer as a chronic disease can exacerbate anxiety, intensify fear of recurrence, hinder life plans, and increase stigma-related challenges. Treatment itself can give rise to several adverse reactions for lung cancer including haematological abnormalities, hypertension, pneumonia and treatment fatigue which further lead to adverse effects on patients.
Promoting self-management behaviors is necessary for these disease burdens. Recent studies have confirmed that self-management behaviors of patients have beneficial impact on the therapeutic effect of the disease.[6,7] Self-management is described as a person’s ability to manage their disease symptoms including treatment, physical, social and lifestyle changes. Several advantages of self-management have been authenticated, for instances, self-management can contribute to better health, better healthcare, better doctor-patient relationships, as well as reductions in depression, fatigue, pain, and emergency room visits.[8–11] Patient activation has been confirmed as an effective indicator for evaluating self-management of patients. Self-management positivity can be summarized as patient’s cognition and behavior during the course of disease treatment.[7,12] The theory of patient activation was proposed by some experts and scholars in 2010,[13] and the theory illustrated variable degree of patient activation which could be divided into 4 progressive levels.
So far, several studies have explored the correlation between patient activation and different kinds of cancers including breast cancer, nasopharyngeal carcinoma, etc,[9,14] however, few studies have been reported on the self-management positivity in lung cancer patients. In this study, Patient Activation Measure 13 (PAM-13) was used to investigate the activation of patients in whom lung cancer was diagnosed and different treatment methods were performed, and activation-related influence factors were analyzed with the aim of helping patients to improve self-management positivity, to experience better disease management and to improve quality of life.

2. Methods

2.1. Enrolled patients and eligibility of participants
Patients who were diagnosed as lung cancer including both NSCLC and SCLC from August 2023 to June 2024 were recruited by convenience sampling from Cancer Hospital, Chinese Academy of Medical Sciences and Beijing Chao-yang Hospital in this study. Inclusion criteria were as follows: NSCLC or SCLC was pathologically confirmed; at least 18-year old; patients had self-care ability; and patients had normal ability to read and communicate; Exclusion criteria included: patients had serious complications and comorbidities which seriously influenced their life safety, such as massive pleural effusion restricting respiration, obstructive pneumonia, respiratory failure, heart failure, cachexia, etc; patients had serious cognitive impairments or mental disorders; refused to accept any treatment; uncontrolled brain metastases; and bone metastases accompanying severe tumor erodes and cortical bone destruction confirmed by imaging examination which had the risk of pathologic fractures in the performance of exercise training. The study was conducted in accordance with the Helsinki Declaration and had been approved by the Institutional Ethical Committees of the Cancer Hospital, Chinese Academy of Medical Sciences and Beijing Chao-yang Hospital. All participants gave written informed consents for participation.

2.2. Design of questionnaire and collection of data
Lots of relevant literatures both domestically and internationally were read before formulating questionnaire, and factors affecting cancer patient positivity were synthesized, then our survey questionnaire was designed, and it was improved under the guidance of relevant experts. The contents of the questionnaires included patients’ demographic data such as gender, age, body mass index (BMI), educational background, family residence, marital status, work status, etc and information of disease such as tumor type, treatment intention (curative, palliative or supportive-care-only) and diagnosis status (primary or relapse). The PAM-13 was used to judge the patient activation. In addition, health literacy, cancer loneliness and general self-efficacy were assessed by corresponding scales. Researchers explained the purpose of study exactly and obtained the informed consent of the patients, then they distributed the questionnaires to participants, and the participants should provide the answers. Then, we retrieve the completed questionnaires at once.

2.3. Investigate tools and survey items
All outcomes were obtained from questionnaires completed by patients themselves, except for relevant disease-related information (such as tumor type, treatment intention and diagnosis status), which were extracted from routine medical documentation. The score of PAM-13 was calculated, and correlations between PAM-13 and demographic data of patients and disease-related information were analyzed.

2.4. PAM-13
After receiving permission from Insignia Health, Inc., the American original version of PAM-13 was translated as recommended by the World Health Organization’s procedures for cross-cultural validation and adaptation of self-report measures, and the original scale was translated to Chinese in 2018.[15] It is a measure that assesses patient knowledge, skills and confidence for disease self-management, and it is a non-disease-specific tool which can be used across different patient populations. The PAM-13 is consisted of 13 items on a 5-point Likert scale (0 = not applicable, 1 = strongly disagree, 2 = disagree, 3 = agree, 4 = strongly agree). Item scores are summed up to a raw sum score resulting in theoretical values between 13 and 52, which are then transformed to a standardized metric ranging from 0 to 100, 4 levels of patient activation were divided into according to the total score (Level 1: ≤47, Level 2: 47.1–55.1, Level 3: 55.2–67.0, Level 4: ≥67.1), and the PAM-13 scale can then be categorized into 4 hierarchical stages of activation: cognition (items 1–2), skills (items 3–8), action (items 9–11), and belief (items 12–13).

2.5. Other outcomes measures
Health Literacy Management Scale, Cancer Loneliness Scale and General Self-Efficacy Scale were used for evaluation. Correlations between PAM-13 and these scales were also analyzed.

2.6. Health literacy management scale
Jordan and his colleagues developed Health Literacy Management Scale firstly,[16] and the Health Literacy Management Scale for Chronic Disease Patients was proposed by Sun in 2012. It has been used to evaluate health literacy in Chinese patients who were diagnosed as different kinds of chronic disease for several years. All of 24 items are included in this scale, and the 24 items with a total score of 120 points are divided into 4 dimensions. The higher score represents the better health literacy.

2.7. Cancer loneliness scale
Adams and his colleagues developed this scale in 2017.[17] All of 7 items were included in this scale, and each item is scored on a 5-point Likert scale, the total score ranges from 7 to 35, with higher scores indicating more loneliness.

2.8. General self-efficacy scale
General self-efficacy scale which was first developed in German by Schwarzer and Jerusalem in 1995,[18] and then it was translated for Chinese adults by Wang et al.[19] The 10 items in the General Self-Efficacy Scale are on a four-point ordinal scale scored. Higher scores indicate higher self-efficacy.

3. Statistical analysis
SPSS 26.0 (IBM, Chicago) was used to conduct data analysis. Student t test was used to analyze the influence of “gender,” “pathology of tumor” and “diagnosis status” on PAM-13; ANOVA was used to analyze the impact of “age,” “BMI,” “education,” “family residence,” “marital status,” “monthly household income,” “work status,” “understanding about disease” and “treatment intention” on PAM-13. Pearson correlation analysis was used to analyze the correlation between “health literacy,” “cancer loneliness,” “general self-efficacy” and PAM-13. Relationship between influencing factors and PAM-13 was analyzed by multiple stepwise regression analysis. Influencing factors were obtained through univariate analysis, which were confirmed having clear relevance to PAM-13. Before the multifactorial analysis, collinearity diagnostics were performed on the variables with statistical differences in the univariate analysis. P-value <.05 was considered statistically significant. Missing values were deleted pairwise to calculate correlations. No missing values were imputed.

4. Results

4.1. General information of patients
All of 462 questionnaires were distributed and 443 valid questionnaires were retrieved, and the returned pass rate of questionnaires was 95.9%. Among the 443 patients, 154 cases were male and 289 cases were female. The age of patients ranged from 26 to 77 years old with a median age of 57 years. The BMI ranged from 20 to 34 kg/m2 with a median of 26 kg/m2. The other demographic outcomes including education level, family residence, marital status, work status and monthly household income, etc and disease-related information were shown exactly in "Table 1 and Table S1 (Supplemental Digital Content, https://links.lww.com/MD/R436).

4.2. Outcomes of PAM-13
The score of PAM-13 ranged from 19.79 to 100, and the mean score was 62.95 ± 16.77. The score of each item was listed in Table 2. The distribution of patients in each item was revealed in Figure 1. The score in dimension of “Cognition” was 3.12 ± 0.61, 2.42 ± 1.03 in “Belief,” 2.30 ± 1.15 in “skill,” and 2.23 ± 1.05 in “Action,” all of them were shown in Table 3.

4.3. Univariate analysis results between PAM-13 and general information of patients
As shown in Table 1, the mean score of PAM-13 in patients aged 60 to 70 years was 65.91 ± 16.13, and 51.65 ± 18.64 in patients aged more than 70 years old (P < .001); and the mean score was 51.20 ± 16.92 in patients losing a spouse, 63.92 ± 16.52 in married and 62.57 ± 14.31in unmarried (P < .001); patients with <5000, 5000 to 10,000, >10,000 of monthly household income had the score of 56.80 ± 16.17, 63.22 ± 16.10, and 67.91 ± 16.30 (P < .001); patients who was on duty, retired and unemployed had the mean score of 61.83 ± 16.76, 64.57 ± 16.63, and 57.37 ± 16.55 (P = .025); patients who understood about disease none, vaguely and exactly had the score of 52.50 ± 17.13, 61.88 ± 15.21, and 71.01 ± 15.85 (P < .001); patients receiving curative, palliative and Supportive-care-only treatment had the score of 65.31 ± 15.64, 57.55 ± 18.13, and 52.82 ± 17.73 (P < .001); patients with primary diagnosis and relapse disease had the score of 63.74 ± 16.08 and 56.44 ± 20.67 (P = .004).

4.4. Correlation analysis between PAM-13 and health literacy, cancer loneliness and general self-efficacy
The scores of health literacy, cancer loneliness and self-efficacy were shown in Table 4, and the mean scores were 85.05 ± 19.91, 16.48 ± 6.23, and 23.35 ± 5.77, respectively.

4.5. Multivariate analysis of PAM-13
As shown in Table 5, marital status, monthly household income, work status, treatment intention, health literacy, cancer loneliness and general self-efficacy were independent risk factors of PAM-13.

5. Discussion
The concept of patient activation encompasses a broad range of elements that enable patients to become effective and informed managers of their health.[20] Patient activation, also known as self-management positivity, can reflect patients’ beliefs about disease management. Some studies have confirmed that patient activation is conducive to promote healthy behaviors and obtain satisfactory therapeutic effect.[21,22] PAM-13, as an effective and useful tool verified by some experts and scholars, has been used extensively for evaluating patient activation since it was formulated in 2005. Several study results have demonstrated that higher PAM-13 score is associated with better health outcomes, better adherence to therapy and fewer healthcare utilization and costs.[14,23,24]
Higher PAM score values are indicative of higher patient activity levels. As we know, a total of 4 activation levels are divided according to the score: Level 1, patients do not recognize the importance of self-management; Level 2, patients recognize the importance but lack sufficient knowledge and belief in self-management; Level 3, patients can participate in self-management but lack sufficient knowledge and skills to maintain these behaviors; and Level 4, patients have relevant knowledge and skills for self-management but require external support in the face of life pressures. So far, PAM-13 has been used for evaluation in several disease areas, for example, metabolic syndrome,[25] hypertension,[26,27] diabetes,[28,29] mental disorders,[30,31] cardiac conditions,[32,33] and also it has been used in some kinds of malignant tumors, for instance, PAM-13 was used for evaluation in patients with head and neck cancer in a study designed by Gao Z,[15] and PAM-13 was also used to investigate patient activation in breast cancer patients in another study designed by Vrancken Peeters NJMC.[34] Nevertheless, the activation in patients with lung cancer has been seldom reported, and few studies have been conducted on the usage of PAM-13 in lung cancer patients. In a study designed by Inka Roesel,[9] the PAM-13 was used to evaluate the structural validity and psychometric properties of the PAM-13 in an oncological patient cohort, and the overall mean PAM-13 score was 69.68 with a range of 17.9 to 100; another study showed that the PAM13 score of patients with head and neck cancer was 63.48 ± 14.7 at level 3. In our study, the mean score of PAM-13 in lung cancer patients was 62.95 ± 16.77, which was belonged to the level 3. These results revealed that the score in patients with lung cancer was similar to that in some other kinds of cancer. We don’t know the patient activation exactly in other countries and regions due to rarely reports about activation in lung cancer patients. In a Chinese study designed Ma N,[35] the patient activation in young and middle-aged patients with lung cancer was analyzed and the score of PAM-13 was 66.77. Another study reported by Wim G Groen,[36] an interactive digital portal was used to support patients with NSCLC in their study, and slightly lower PAM-13 scores were found, patient activation decreased from 64.8 in the pretest to 59.4 in the post-test. We also found that the “cognition” dimension had the highest score and “action” dimension had the lowest score in our study, which represented that patients had few self-management skills and behaviors. Our findings suggested that medical staff should popularize relevant medical knowledge and perform medical education in lung cancer patients, and finally let them know “how to do.”
Several factors may have influence on patient activation. Patients aged more than 70 years had the lowest score in this study. Elderly patients have more obstacles to understand the importance of self-management, and even if they know the significance, they have more difficulties to practice self-management and to maintain a healthy lifestyle.[37] In addition to this, older patients had lower activation could be influenced by comorbidities, treatment fatigue, or digital health literacy barriers. Marital status was another influence factor confirmed in our study. Widowing is accompanied by strong feelings of loss and loneliness,[38] and even losing the positivity of life is found in a certain proportion of the population. Losing their spouse has a series of negative impact on patients, which would dampen their enthusiasm.[28] Our results confirmed that patients with the more household income had the higher activation and the similar result was found in some other studies. Medical resources maybe have positive correlation with household income. Patients who are on duty or retired have stable income compared to patients unemployed, and the economic base determines the superstructure,[39] so patients who were on duty had the higher PAM-13 score. Palliative and supportive-care-only implies the terminal stage of illness, the same to relapse of disease, which may result in the increased mental stress and psychological pressure, and cause serious negative impacts on patients, such as being on tenterhooks and losing confidence in life.
As some studies showed that inadequate health literacy was associated with decreased patient engagement, worse self-management and poor health outcomes could be induced by lower level of health literacy.[40–42] Inadequate health literacy is associated with cancer self-management behaviors: less uptake of cancer screening behaviors, less uptake of pre-scribed chemotherapy, a greater likelihood of post-operative complications, higher information needs, and less information seeking behaviors.[43,44] Our results verified the correlation between health literacy and patient activation, and confirmed that health literacy was an independent influence factor of patient activation.
Research on loneliness in cancer patients has been conducted for many years. Several studies confirmed that high levels of loneliness can cause great distress, and cancer patients with high level of loneliness inevitably have more severe depressive symptoms, which may have adverse influence on activation, and eventually weaken the enthusiasm of self-management.[45–47]
General self-efficacy has a positive impact on patient activation, which has been confirmed by several studies.[48–50] Patients with the higher self-efficacy usually have lower levels of distress. In addition, patients with higher self-efficacy are more likely to acquire disease-related knowledge and seek help from the doctors and their family members, which is greatly useful for them to maintain the self-management behaviors.[51] Several previous studies had confirmed that self-efficacy was associated with better quality of life and less depression.[49] The fear, denial and the role of treatment-related adverse effects in hindering daily activities can initially result in decreased self-efficacy.[52] Our study also confirmed that lung cancer patients with higher self-efficacy had more activation in self-management.
The limitations of this study: some possible influence factors are not included, for example, the tumor stage, the selection of treatment methods is based on the tumor stage and the severity of harm to the human body is also significantly influenced by tumor stage; treatment modalities as covariates, the treatment methods (chemotherapy, radiotherapy, surgery, etc) may have serious impact on daily activities of patients, surgery-related pain, gastrointestinal reactions induced by chemotherapy, radiation pneumonia or pulmonary fibrosis, all of which may have side effects on patient activation, other influence factors including psychological pressure of patients, socio-economic factors also need to be analyzed; meanwhile medical staffs, caregivers and even family members may play an important role during the process of cancer treatment, whether their attitudes and enthusiasm have influence on patient self-management positivity or not should be analyzed simultaneously. Finally, heavy reliance on questionnaires is the great weakness of this study, because the authenticity and validity of the questionnaire can be influenced by several factors, for instance, the social desirability bias.
In conclusion, most lung cancer patients were at PAM level 3, reflecting adequate awareness but insufficient skills, and that targeted interventions (e.g., educational programs, psychosocial support) are needed. In this study, several factors including age, marital status, monthly household income, work status, level of understanding about disease, treatment intention, diagnosis status, health literacy management, cancer loneliness, general self-efficacy had impact on self-management positivity. It is worth noting that these findings are based on a Chinese cohort and may not be generalizable to other cultural or healthcare contexts.

Acknowledgments
The authors thank Xue-fei Yao, Jia Li and Zhuo Li for presenting idea, their helps are the key for completion of this manuscript.

Author contributions
Conceptualization: Xingmao Zhang, Yao Tong, Wei Zheng.
Data curation: Yao Tong.
Formal analysis: Yao Tong.
Investigation: Yao Tong, Meng-die Hu, Wei Zheng.
Methodology: Xingmao Zhang, Meng-die Hu.
Project administration: Meng-die Hu.
Resources: Meng-die Hu, Zhi-rong Zhang.
Software: Na Zhang, Zhi-rong Zhang.
Supervision: Xingmao Zhang, Na Zhang, Wei Zheng.
Validation: Na Zhang, Zhi-rong Zhang.
Visualization: Zhi-rong Zhang.
Writing – original draft: Yao Tong.

Supplementary Material