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Article

Radiotherapy-Related Clinical and Functional Sequelae in Lung Cancer Survivors

by
Alejandro Heredia-Ciuró
1,
Paula Blasco-Valls
2,
Andrés Calvache-Mateo
1,
Geraldine Valenza-Peña
1,
Laura López-López
1,
Araceli Ortiz-Rubio
1,* and
Marie Carmen Valenza
1
1
Department of Physiotherapy, University of Granada, 18071 Granada, Spain
2
Department of Oncological Radiotherapy, San Cecilio University Hospital, 18071 Granada, Spain
*
Author to whom correspondence should be addressed.
Appl. Sci. 2024, 14(13), 5874; https://doi.org/10.3390/app14135874
Submission received: 3 June 2024 / Revised: 1 July 2024 / Accepted: 2 July 2024 / Published: 5 July 2024
(This article belongs to the Special Issue Advances in Diagnostic and Therapeutic Radiology — 2nd Edition)
Browse Figure
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Abstract

:
It is known that lung cancer survivors experience sequelae due to the evolution of the disease and oncological treatment. However, there is no consensus about their sequelae after radiotherapy treatment. The aim of this study was to analyze the clinical–functional profile of lung cancer survivors who receive radiotherapy treatment. This prospective observational study evaluated lung cancer patients who were candidates for radiotherapy treatment in the oncological radiotherapy unit of San Cecilio University Hospital in Granada. Symptoms (i.e., fatigue, cough, and dyspnea), functionality (i.e., physical activity levels and muscle mass), and quality of life were evaluated pre- and post-radiotherapy treatment. Sixty-five participants were included, and sixty-one completed both evaluations. Patients showed a significant increase in symptoms (p < 0.05) and a decline in functionality (p < 0.001) after completing radiotherapy. Quality of life was significantly lower after completing radiotherapy treatment (p < 0.05). Lung cancer survivors showed an increase in symptoms, a decline in physical activity levels, and a decline in perceived quality of life after receiving radiotherapy treatment. These results provide more accurate knowledge about the functional impairment experienced by lung cancer patients and can facilitate the future management of impairment in lung cancer patients, thus improving their quality of life.

1. Introduction

Lung cancer has an incidence of 2,206,771 cases per year and is one of the most prevalent cancers worldwide. This disease has a 15% five-year survival rate, which makes it the deadliest type of cancer [1]. The pathogenesis of lung cancer has been associated with exposure to various risk factors, among which tobacco consumption stands out [2]. It is important to highlight the role of unhealthy lifestyle habits, such as an inadequate diet or a sedentary lifestyle, as predisposing factors for the development of cancer [3].
Lung cancer treatment is composed of lung resection and several possible coadjuvant treatments where radiotherapy is often established as the last line of treatment to control the disease [4]. Radiotherapy is a key treatment for thorax and lung cancer because of its ability to selectively ablate the tumor. For this reason, it is applied before and after other treatments, both in unresectable, extensive tumors and in frail patients for whom surgery is not recommended [5].
Cancer treatments lead to the formation of free radicals, cytokine release, and a local and systemic inflammatory response that conditions the appearance of side effects and sequelae [6]. In this regard, lung cancer patients are associated with a high burden of disease, physical difficulties, and significant symptomatic suffering [7]. Published studies have shown that lung cancer survivors often experience persistent cancer and treatment-related symptoms including cough, chest pain, fatigue, insomnia, nausea, and erythema, among others [8]. The symptoms can become chronic [9], impacting the functionality and quality of life of these patients. Moreover, these chronic conditions lead to an increase in patient morbidity [10].
Physical activity can be a key factor in cancer patient recovery that helps patients cope with anti-cancer treatment and decreases long-term symptoms [11]. However, lung cancer patients have significant limitations in performing physical exercise. Previous studies have shown that before cancer treatment, the physical activity levels of these patients are lower than those of healthy subjects [12]. These levels decrease even more after cancer treatment [13]. These factors result in a cycle of inactivity and functional impairment, which is described in detail in the literature on the management of lung cancer survivors [14]. Functional capacity effectively predicts survival in lung cancer patients [15], especially in cancer survivors treated with radiochemotherapy, who often do not recover the functional capacity they had before treatment [5].
To our knowledge, no previous studies have explored the sequelae experienced by lung cancer patients after receiving radiotherapy treatment [16], even though radiotherapy ablation has a significant number of side effects. An example is cardio-pulmonary toxicity, which is known as one of the side effects of radiotherapy and influences the morbidity and mortality of these patients [17].
Considering the above, this study aimed to analyze the functional and clinical profile of lung cancer survivors after receiving radiotherapy treatment and to evaluate their self-perceived health-related quality of life.

2. Materials and Methods

2.1. Design

We performed a prospective observational study in which lung cancer patients who were going to be treated with radiotherapy were recruited from the Radiotherapy Unit of San Cecilio University Hospital (Granada, Spain) between September 2022 and September 2023. This study was conducted in accordance with the Declaration of Helsinki. The Biomedical Research Ethics Committee of Granada (Granada, Spain; 0092-N-20) reviewed and approved this study.

2.2. Participants

Inclusion criteria were lung cancer survivors aged 18–80 years who were candidates for radiotherapy treatment and could give written informed consent. Exclusion criteria included comprehension deficits (according to the Montreal Cognitive Assessment) or impaired cognition [18]; limitations in communicating; a diagnosis of a neurological condition that prevented the evaluation; conditions affecting the musculoskeletal system; or a medical contraindication to physical exercise.
Patients underwent two assessments: before radiotherapy treatment and after completing radiotherapy treatment. Both evaluations were conducted by the same two physiotherapists, each with over two years of experience in assessing lung cancer survivors with different sequelae in rehabilitation programs.

2.3. Outcomes

At admission, we collected patients’ anthropometric data, comorbidities, tumor location, and radiotherapy characteristics from their medical history [19]. Comorbidities were evaluated with the Charlson Index, which has been validated for several disorders [20]. Data collection was performed at the laboratories of the University of Granada.
The main study outcomes included respiratory symptoms (i.e., dyspnea, cough, and fatigue), functionality, and the quality of life of lung cancer survivors.
Dyspnea was evaluated with the Modified Borg Scale, which has been validated in respiratory and cancer patients [21]. Patients rated their respiratory distress on a total scale of 0–10 (0 = no distress and 10 = breathing was very difficult).
Cough was assessed with the Cough Assessment Test (COAT) [22]. This scale is composed of five subscales that measure the severity of cough and cough frequency, limitations on activities of daily life, sleep disturbance, fatigue, and hypersensitivity to some irritants. Each item is scored from 0 to 4, with a total score of 0–20. Higher scores indicate a more severe cough.
Fatigue was measured with the Piper Fatigue Scale-Revised (PFS-R) [23]. This scale includes 22 items that assess self-reported fatigue using numerical rating scales (0–10). It contains 4 subscales that reflect the subjective experience of fatigue: behavioral/severity, affective meaning, sensory, and cognitive/mood. The overall score is obtained by adding up the total scores and dividing the result by the total number of items. Higher scores indicate higher levels of fatigue.
Functional status was evaluated by assessing physical activity levels and muscle strength. The International Physical Activity Questionnaire-Short Form (IPAQ-SF) was used to assess physical activity levels [24]. Time spent performing physical activity is classified as vigorous exercise, moderate activities, or walking. An MET score is calculated based on the performed physical activity according to the classification by Ainswoth et al. [25]. Total METs/hour per week for each physical activity subtype were calculated and then added together to calculate the total METs per week. Sedentary behavior was measured with the recorded sitting time (minutes per day) [26].
Additionally, an evaluation of the perceived barriers to perform physical activity was included. This measure was assessed with the Physical Activity Barriers After Cancer (PABAC) instrument [27]. This tool includes 12 barrier items scored on a 4-point Likert scale (1 = strongly disagree to 4 = strongly agree). The total score was obtained by adding up the items, with possible scores ranging from 12 to 48. Higher scores indicate more barriers to physical activity.
Muscle strength was explored by measuring the cross-sectional area of the rectus femoris [28]. A B-mode ultrasonography with an 8 MHz 5.6 cm linear transducer (ECO 3 Expert Doppler, Chison, Wuxi, China) was used, similarly to the method of De Bruin et al. [29]. The transducer was positioned perpendicular to the long axis of the thigh on its superior aspect, at three-fifths of the distance from the anterior superior iliac spine to the superior patellar border. The evaluation was conducted in a supine position with the extended leg relaxed. Rectus femoris cross-sectional area (RFCSA) was calculated using a planimetric technique, tracing the inner echogenic line of the rectus femoris with a movable cursor on a frozen image. RFCSA was calculated as the average of three consecutive measurements within 10%.
Finally, self-perceived health-related quality of life was evaluated with the EuroQol-5 Dimensions 5 Levels (EQ-5D-5L) (Rotterdam, The Netherlands) [30]. This tool is composed of five items that assess five dimensions (i.e., mobility; self-care; usual activities; pain; anxiety/depression) and a 0–100 visual analog scale (VAS) where patients report their self-perceived status. The Spanish version of this questionnaire has shown good validity and high reliability [30].

2.4. Statistical Analysis

G*Power 3.1.9.2 was used to estimate a sample size based on the minimum clinically significant difference of the Modified Borg Scale [31]: 1.00. Based on a confidence level of 95% (α = 0.05) and a power of 80% (β = 0.2), we obtained a sample size of 48 participants. In anticipation of a dropout rate of 20%, the total sample size calculation was increased to 58 participants.
Statistical analysis was performed using IBM SPSS version 20.0 [32]. The Kolmogorov–Smirnov test was used to explore the normality of the data distribution, and Fisher’s F-test was used to check the homogeneity of variances. Parametric tests were used when both conditions were met; otherwise, non-parametric tests were applied. Differences in characteristics between lung cancer patients before and after radiotherapy were evaluated using the dependent sample t-test for numerical variables with a normal distribution. Statistical analysis was conducted at a 95% confidence level, and a p-value < 0.05 was considered statistically significant. Numerical variables were expressed as the mean ± SD or percentage (%).

3. Results

3.1. Distribution of Participants

A total of 75 patients were screened at the beginning of the study. Three participants declined to participate and seven did not meet the inclusion criteria. Finally, 65 were included in the study. All 65 patients signed the informed consent form and were evaluated for their inclusion, but only 61 completed both evaluations. A flow diagram of the participants is presented in Figure 1.

3.2. Characteristics of Participants Included in This Study

The clinical characteristics of the participants are presented in Table 1. The study sample had an average age of 68.09 ± 6.88 years, and 75.40% of the lung cancer patients were males. The mean Body Mass Index (BMI) was 27.34 kg/m2 and the mean number of comorbidities was 6.51 ± 2.18 according to the Charlson Index. Of the lung cancer patients, 83.10% had non-small cell lung cancer, and 70.80% were in an advanced stage. The radiotherapy treatment applied was homogeneous, with a mean of 24.29 ± 8.80 sessions, a total radiation dose of 55.38 ± 9.13 G, and a mean radiated organ volume of 456.58 ± 200.57 cc. A total of 21.50% of patients received a lung resection, and 80% received chemotherapy treatment.

3.3. Clinical and Functional Outcomes of This Study

Differences in symptoms and physical activity performed before and after radiotherapy treatment are shown in Table 2. Regarding symptoms, significant differences were found in dyspnea (p = 0.001), cough (p = 0.002), and fatigue (p < 0.001). Patients showed worse fatigue in the different dimensions after radiotherapy treatment, with significant results in the behavioral (p < 0.001), cognitive (p < 0.001), sensory (p < 0.001), and total score (p < 0.001).
Functional status assessed with the IPAQ showed significant differences for slight (p < 0.001), moderate (p < 0.001), vigorous (p < 0.001), and total physical activity performed. Patients also showed lower physical activity levels after radiotherapy treatment, with a mean of 847.33 ± 727.97 METs (p < 0.001). In addition, a significant increase was observed in the sedentary habits of these patients, with 447.73 min of sitting per day (p = 0.001). They also reported a significant increase in perceived barriers to perform physical activity (p < 0.001). The decrease observed in muscle section area indicated significant muscle weakening (p = 0.002) when the RFCSA before radiotherapy (1.16 ± 0.29) was compared to the RFCSA after radiotherapy (1.00 ± 0.28).

3.4. Quality of Life

Table 3 shows the differences in the quality of life of patients before and after radiotherapy treatment. Significant differences were observed in the subscales for mobility (p = 0.007), self-care (p = 0.007), and pain (p < 0.001). No significant differences were found in the subscales for activities, anxiety and depression, or VAS. However, the post-radiotherapy assessment of the VAS subscale showed a lower score of 60.90 ± 19.89 compared to the pre-treatment VAS, which showed a mean score of 67.38 ± 19.14.

4. Discussion

This study aimed to analyze the functional and clinical profile of lung cancer survivors after receiving radiotherapy treatment and to evaluate the quality of life of these patients. The results showed higher functional impairment and worse symptoms and perceived health-related quality of life after completing radiotherapy treatment.
The study sample accurately reflected the broader population of lung cancer patients receiving radiotherapy treatment. We observed similar sociodemographic characteristics [33], a homogeneous etiological profile [34], and a radiotherapeutic approach similar to that received by lung cancer survivors in previous studies [35].
Our results showed an increase in symptoms after completing radiotherapy treatment, with a significant increase in cough, dyspnea, and perceived fatigue compared to pre-radiation symptom levels. Previous studies in other cancer populations have shown similar results to ours. For example, the study by Tombal et al. [36] also showed a high prevalence of radiotherapy-related symptoms in prostate cancer survivors.
The presence of a significantly high level of dyspnea is an important symptom to consider due to its importance as a predictor of long-term survival after anti-cancer treatment [37]. Fatigue is also a cardinal symptom of these patients. In this regard, published studies have shown that perceived fatigue is maintained even 5 years after completing anti-cancer treatment [38].
Our findings on physical activity levels are also in line with the decline presented in the physical activity and exercise capacity of other cancer survivors who have completed radiotherapy treatment [39]. Previous studies in lung cancer populations have reported that more than 70% of these patients do not generally achieve the physical activity recommendations for cancer survivors [40], which has a direct negative effect on their quality of life.
Based on the articles published to date, it is important to note that this decline in physical activity levels could be influenced by a voluntary limitation of physical activity by patients to avoid triggering the symptoms they experience [14]. These symptoms cause great discomfort to patients and interfere with their activities of daily living [7].
This clinical condition is in line with the results obtained on barriers to physical activity, which increase significantly after completing radiotherapy treatment. Moreover, previous studies have obtained similar results to ours in populations with different types of cancer [41].
Patients in this study also showed a significant decline in their self-perceived quality of life after radiotherapy. This decline has been reported in previous studies that assessed the evolution of lung cancer survivors in advanced stages. For example, the study by Presley et al. [42] found disturbances in 37.6% of the sample’s activities of daily living, 26.6% of their mobility, and 5.2% of their self-care. However, the heterogeneity of the population did not allow them to establish a relationship between this decline and factors such as the treatment received.
Other sequelae should be taken into account for the management of these patients after radiotherapy treatment. Previous studies [43] have highlighted neurocognitive functional sequelae after radiotherapy that should be considered. This is particularly disturbing for patients and for the specialists who treat them. Such problems tend to affect one’s problem-solving ability, attention, information-processing speed, and could negatively affect one’s ability to perform physical activity.
Rehabilitation could be a good approach to manage the sequelae and a future line of research. It has been shown to increase exercise capacity, reduce dyspnea and fatigue, and improve quality of life [44]. Specifically, therapeutic exercise programs have been reported as safe approaches to patients with comorbidities such as coronary heart disease, chronic inflammation, and musculoskeletal dysfunction [45]. Exercise has been proposed for treatment and prevention of cancer in many studies of high methodological quality.

4.1. Limitations

Our study had a limitation regarding the follow-up of the study: patients were lost during radiotherapy treatment. However, previous studies have shown similar sample sizes to our study [46]. Additionally, to improve the quality of our results, it would be useful to perform a follow-up assessment after completing radiotherapy treatment, analyzing the evolution of these variables over time. However, previous studies have had the same study design as ours for evaluating sequelae after anti-cancer treatment [47].
The study design may have led to possible bias. Comparisons with a control group of lung cancer patients who did not receive radiotherapy or received alternative treatments would strengthen the relationships between these results. However, a one-group study was able to detect smaller differences, making them more sensitive to the effects of the independent variable [48].

4.2. Future Research

Future studies are needed to follow up on the sequelae found in lung cancer patients. This would allow us to obtain more accurate knowledge about the chronic functional impairment experienced by lung cancer patients. Learning more about what kind of physical activity is affected in the long term would be useful for designing future interventions.
Future studies should also include molecular experiments to briefly explain and support these results. The ability to understand the sequelae of lung cancer patients based on a set of biomarkers that predict toxicity risk would enable the adjustment of radiotherapy and serve as a valuable tool for precision medicine and personalized radiotherapy treatment [49].

5. Conclusions

In conclusion, lung cancer survivors showed increased symptoms and a decline in functionality after receiving radiotherapy treatment, with a decline in self-perceived quality of life. These results provide clinicians with more accurate knowledge about the functional impairment experienced by lung cancer patients and facilitate the management of impairment in these patients, reducing sequelae after cancer treatment and thus improving their overall health status.

Author Contributions

Conceptualization, M.C.V. and A.H.-C.; methodology, A.O.-R. and L.L.-L.; software, M.C.V.; formal analysis, M.C.V. and A.C.-M.; investigation, P.B.-V. and G.V.-P.; resources, L.L.-L. and P.B.-V.; data curation, A.O.-R. and A.C.-M.; writing—original draft preparation, A.H.-C.; writing—review and editing, M.C.V.; visualization, A.O.-R.; supervision, M.C.V.; project administration, A.H.-C. and P.B.-V. All authors have read and agreed to the published version of the manuscript.

Funding

This study received an award from the Professional Association of Physiotherapists of Andalusia, Spain (Ilustre Colegio Profesional de Fisioterapeutas de Andalucía) (Award for the Promotion of Oncological Physiotherapy).

Institutional Review Board Statement

This study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Granada (Granada, Spain) (0092-N-20; 15 January 2020).

Informed Consent Statement

Written informed consent was obtained from the patient(s) to publish this paper.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to privacy.

Acknowledgments

The authors thank the Professional Association of Physiotherapists of Andalusia for supporting this study and facilitating the publication and dissemination of these results.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of the data; in the writing of the manuscript; or in the decision to publish the results.

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Applsci 14 05874 g001
Figure 1. Flow diagram of participants included in study.
Figure 1. Flow diagram of participants included in study.
Applsci 14 05874 g001
Table 1. The characteristics of the patients included in this study.
Table 1. The characteristics of the patients included in this study.
VariableValues (n = 65)
  Sex (n male/n female)(49/16)
  Age (y)68.09 ± 6.88
  BMI (kg/m2)27.34 ± 4.35
  Charlson Index6.51 ± 2.18
  Smoke habitSmoker/Ex-smoker57 (87.7%)
Non-smoker8 (12.3%)
Lung cancer
  TypeSCLC11 (16.9%)
NSCLC54 (83.1%)
  StageI11 (16.9%)
II8 (12.3%)
III46 (70.8%)
Radiotherapy treatment
  TypeVMAT + IGRT38 (58.5%)
SBRT + IGRT15 (23.1%)
External12 (18.5%)
  Number of sessions24.29 ± 8.80
  Total radiation dose (G)55.38 ± 9.13
  Irradiated organ volume (cc)456.58 ± 200.57
Adjuvant treatment
  Surgery14 (21.5%)
  Chemotherapy52 (80%)
  Immunotherapy9 (13.8%)
Data expressed as n (%) or mean ± SD. Abbreviations: y, years; BMI, Body Mass Index; NSCLC, non-small cell lung cancer; SCLC, small cell lung cancer; VMAT, volumetric intensity-modulated arc therapy; IGRT, image-guided radiation therapy; SBRT, stereotactic body radiation therapy; G, gray.
Table 2. Symptoms, physical activity, and muscle mass of patients included in study before and after radiotherapy treatment.
Table 2. Symptoms, physical activity, and muscle mass of patients included in study before and after radiotherapy treatment.
Before Radiotherapy
(n = 65)		After Radiotherapy
(n = 61)		p-Value
Symptoms
 Dyspnea 2.87 ± 2.134.21 ± 2.040.001 *
 Cough 3.25 ± 4.165.62 ± 4.110.002 *
 Fatigue
  Behavioral1.92 ± 1.293.26 ± 1.630.000 **
  Affective5.13 ± 3.015.02 ± 2.140.810
  Cognitive1.88 ± 1.675.65 ± 2.010.000 **
  Sensory3.32 ± 2.004.81 ± 1.080.000 **
  Total2.89 ± 1.084.68 ± 0.820.000 **
 Physical activity
 Walking918.56 ± 327.59563.76 ± 551.710.000 **
 Moderate1077.70 ± 348.94204.64 ± 375.560.000 **
 Vigorous1095.58 ± 491.6978.94 ± 76.470.000 **
 Total3091.84 ± 737.61847.33 ± 727.970.000 **
 Minutes of sitting time357.42 ± 145.68447.73 ± 152.510.001 *
 Barriers to perform P.A.18.48 ± 5.6725.43 ± 4.690.000 **
Muscle mass
 RFCSA1.16 ± 0.291.00 ± 0.280.002 *
Data expressed as mean ± SD; * p < 0.05; ** p < 0.001. Abbreviations: P.A., physical activity; RFCSA, rectus femoris cross-sectional area.
Table 3. Quality of life of lung cancer patients included in study before and after radiotherapy treatment.
Table 3. Quality of life of lung cancer patients included in study before and after radiotherapy treatment.
Before Radiotherapy
(n = 65)		After Radiotherapy
(n = 61)		p-Value
Mobility subscore1.62 ± 0.932.08 ± 0.900.007 *
Self-care subscore1.31 ± 0.531.69 ± 0.940.007 *
Activities of daily life subscore1.82 ± 1.131.95 ± 0.830.466
Pain subscore1.61 ± 1.052.3 ± 0.820.000 **
Anxiety–depression subscore1.67 ± 0.871.82 ± 0.920.365
VAS subscore (0–100)67.38 ± 19.1460.90 ± 19.890.069
Data expressed as mean ± SD; * p < 0.05; ** p < 0.001. Abbreviations: VAS, visual analog scale.
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Heredia-Ciuró, A.; Blasco-Valls, P.; Calvache-Mateo, A.; Valenza-Peña, G.; López-López, L.; Ortiz-Rubio, A.; Valenza, M.C. Radiotherapy-Related Clinical and Functional Sequelae in Lung Cancer Survivors. Appl. Sci. 2024, 14, 5874. https://doi.org/10.3390/app14135874

AMA Style

Heredia-Ciuró A, Blasco-Valls P, Calvache-Mateo A, Valenza-Peña G, López-López L, Ortiz-Rubio A, Valenza MC. Radiotherapy-Related Clinical and Functional Sequelae in Lung Cancer Survivors. Applied Sciences. 2024; 14(13):5874. https://doi.org/10.3390/app14135874

Chicago/Turabian Style

Heredia-Ciuró, Alejandro, Paula Blasco-Valls, Andrés Calvache-Mateo, Geraldine Valenza-Peña, Laura López-López, Araceli Ortiz-Rubio, and Marie Carmen Valenza. 2024. "Radiotherapy-Related Clinical and Functional Sequelae in Lung Cancer Survivors" Applied Sciences 14, no. 13: 5874. https://doi.org/10.3390/app14135874

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