Factors associated with functional ability in patients with esophageal cancer undergoing chemoradiotherapy: a prospective longitudinal study Running head: Patient functional ability in unresectable EC

doi:10.21203/rs.3.rs-4694635/v1

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Research Article

Factors associated with functional ability in patients with esophageal cancer undergoing chemoradiotherapy: a prospective longitudinal study Running head: Patient functional ability in unresectable EC

https://doi.org/10.21203/rs.3.rs-4694635/v1

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Purpose

During and after treatment, esophageal cancer (EC) patients experience changes in body mass index (BMI), performance status, nutrition status, symptom distress, and physical fitness. This study aims to evaluate temporal changes and their associated factors in BMI, performance status, nutrition status, symptom distress, physical fitness, and functional ability in EC patients during and after treatment.

Methods

This prospective longitudinal study recruited EC patients from a medical center in Northern Taiwan. The 112 EC patients were assessed before treatment (T0), 1 month after starting treatment (T1), 3 months after starting treatment (end of treatment) (T2), and 6 months after starting treatment (T3). Generalized estimating equation analysis was used to determine the factors associated with changes in functional ability over time.

Results

Patient nutrition status was lowest before treatment and then increased by 6 months after treatment. Symptom distress slightly decreased from before treatment to 3 months after treatment, rising at 6 months after treatment but not reaching baseline (T0). Functional ability increased from before treatment to 1 month after treatment and then declined at 3 months after starting treatment, increasing at 6 months to below baseline (T0). Patients who had a BMI less than 25 kg/m², engaged less in physical activity, and were less physically fit were more likely to have worse functional ability.

Conclusion

BMI, level of physical activity, and the degree of physical fitness were the important factors associated with functional ability in EC patients. Healthcare professionals should design patient-tailored prehabilitation programs in advance to strengthen physical fitness.

Esophageal cancer

Longitudinal studies

Nutritional status

Symptom distress

Physical fitness

Physical ability

Esophageal cancer (EC) is the 8th most common cancer worldwide and the 7th most common cancer in men [1]. Approximately 2300 people in Taiwan are diagnosed with EC annually, and most patients are diagnosed at an advanced stage [2]. Currently, the effective treatments for advanced EC are radiotherapy (RT), chemotherapy (CT), and chemoradiation (CCRT) [3]. During treatment and the early post-treatment phase, EC patients often experience varying levels of symptom distress [4] (Wang et al., 2022), physical performance decline [5], and malnutrition [6], resulting in decreased physical abilities [7–10].

Chang et al. [11] found that EC patients had significantly worse fatigue, pain, dyspnea, nausea and vomiting, and insomnia at 1-month post-surgery than did before surgery; additional symptoms that were significantly worse after 1 month included eating problems, reflux, taste problems, coughing, and speech problems. Reflux continued to worsen up to 6 months post-surgery. Nutritional status, weight decline before diagnosis, which continued to drop, and significantly largest weight reduction during the time of diagnosis and 1 month after surgery [12]. Appetite loss was significantly worse before surgery to 1-month post-surgery and had gradually improved at 6-months post-surgery but had not recovered to baseline [11]. Previous studies have shown that fitness and physical functional decline in EC patients [7–10]. After completing treatment, EC survivors have been shown to have a lower fitness level and to spend less time engaged in moderate and vigorous physical activity [7]. The physical fitness level patients who underwent esophagectomy was significantly lower after the procedure than before [10]. EC patients’ physical functioning decreased significantly from pre-surgery to 1-month post-surgery, and 1-month post-surgery recovering to baseline [8]. Patients also reported that their participation in light or moderate-to-vigorous activity declined from before surgery to 6 months post-surgery, remained significantly increased at 6 months, but lower than pre-surgery [8]. Physical function decreased after surgery and up to 1 year after surgery and had not returned to the preoperative baseline at 1 year after surgery [9].

Functional ability, which refers to a patient’s physical, psychological, cognitive, and social ability to perform the activities of daily living, is affected by disease-related factors and changes during the disease course [13]. Cancer patients often experience physical and psychosocial dysfunction, resulting in functional limitations [14]. Worse functional ability is associated with lower physical and mental health [15], poor social function [16], and co-morbidities [17]. Lee et al. found that for colorectal cancer survivors, the mean World Health Organization Disability Assessment Schedule 2.0 (WHODAS 2.0) score was 46.0 (range, 0–100) with declines in participation in society, getting around, performing household activities, conducting self-care, getting along with people, and understanding and communicating [15]. Using the same assessment, Lee et al. [18] found that head-and-neck cancer patients had a mean WHODAS score of 33.95–49.72 (range, 0–100), with declining levels for being a participant in society, conducting household activities, getting around, conducting self-care, and understanding and communicating. In another study, Zhao et al. [19] found that breast cancer survivors had a mean WHODAS score of 29.1 (range, 0–100), with declining levels for performing household activities, participating in society, conducting self-care, getting around, getting along with people, and understanding and communicating.

Based on these previous observations, we suppose that body mass index (BMI), performance status, nutrition status, symptom distress, physical fitness, and functional ability fluctuate during and after treatment. Although several studies have surveyed these problems, most were in chronic diseases [17], colorectal cancer [15], head and neck cancer [18], breast cancer [19], and postsurgical EC patients [8–12]. Few studies have explored changes in these parameters in EC patients before and after treatment. This study aims to evaluate the trajectories of and factors influencing BMI, performance status, nutrition status, symptom distress, physical fitness, and functional ability in patients with esophageal cancer during and after treatment.

Design and sample

This prospective, longitudinal study investigated the trajectories of BMI, performance status, nutrition status, symptom distress, physical fitness, and functional ability and the factors associated with functional ability. The participants were selected by consecutive sampling from the outpatient radiation departments of a medical center in northern Taiwan from August 2019 to July 2021. The inclusion criteria were as follows: (1) age 18 years or more; (2) first esophageal cancer diagnosis; (3) treatment plan included surgery, RT, CT, or CCRT; and (4) fluency to speak and write in Taiwan.

Ethical considerations

All study procedures were in accordance with the ethical principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Chang Gung Memorial Hospital (Ethics Certificate Number: 201801842B0). Participants gave written informed consent before the survey.

Data collection

Participants were assessed at 4 time points: before treatment (T0), 1 month after beginning treatment (T1), at 3 months after beginning treatment (the end of treatment) (T2), and 6 months after beginning treatment (T3). At T0, we collected the patients’ demographic and disease-related characteristics. At each time point, BMI, performance status, nutrition status, symptom distress, physical fitness, and functional ability were assessed.

Patients were treated with RT, CT, or CCRT following the National Comprehensive Cancer Network (NCCN) Guideline [3]. The protocol included a dose of 180–200 cGy RT per fraction per day, administered 5 days per week, for a total dose of approximately 4140 to 5040 cGy over 5 to 6 weeks. Patients received chemotherapy or concomitant chemotherapy with the Cisplatin/5-FU or Carboplatin/Paclitaxel regimens.

Assessments

1. Demographic and disease characteristics form

We collected patients’ demographic and disease characteristics including age, sex, occupation (unemployed vs. employed), marital status (living alone vs. living with a partner), educational level (elementary, junior high, senior high, college, and above), religion (none, Buddhism, Taoism, Christianity/Catholicism), smoking status, and alcohol-drinking status. Disease-related characteristics included tumor site, cancer stage, medical treatment, and BMI.

2. Karnofsky Performance Status (KPS)

Physical performance was assessed using the Karnofsky Performance Status (KPS) scale. The KPS is a single item with scores ranging from 100% (fully normal function) to 0% (death) [20]. This scale has been widely used to assess the physical performance of cancer patients [21, 22].

3. Mini Nutritional Assessment (MNA) short form

The MNA-SF was used to assess nutritional status. The MNA-SF is composed of 6 categories of questions: anthropometric measurements (BMI and weight loss), global assessment (motility), dietary questions (food intake), and health assessment (acute diseases and neurological problems). Scores of 12 points or higher indicate normal nutritional status, and scores of 11 points or below indicate possible malnutrition [23]. The MNA-SF has been widely used to assess the nutritional status of cancer patients in previous studies [24, 25]. The inter-observer reliability coefficient for MNA-SF was 0.97.

4. Functional Assessment of Cancer Therapy-Esophageal (FACT-E)

Symptom distress regarding EC and its treatment was measured using the Functional Assessment of Cancer Therapy-Esophageal (FACT-E), developed by Darling et al. [26]. This 17-item assessment is scored on a Likert-type scale, ranging from 0 to 4, with higher scores indicating less symptom distress [26]. The Chinese FACT-E showed satisfactory psychometric characteristics in previous studies [9, 27]. The Cronbach’s α for the FACT-E in this study was 0.92.

5. International Fitness Scale (IFIS)

Physical fitness was measured using the International Fitness Scale (IFIS) [28]. This 5-item scale assesses 5 elements of physical fitness related to health: general physical fitness, cardiorespiratory endurance, muscle strength, speed-agility, and flexibility. Each item is scored from 1 (very poor) to 5 (very good). The total score ranges from 5 to 25, with a higher score indicating better physical fitness [29]. The IFIS was translated into Chinese, and a previous study showed that it had satisfactory psychometric characteristics [30]. For the present study, the Cronbach’s alpha was 0.92.

6. World Health Organization Disability Assessment Schedule 2.0 (WHODAS 2.0)

Functional ability was measured using the World Health Organization Disability Assessment Schedule 2.0 (WHODAS 2.0), developed by Ustun et al. [31]. The 12-item questionnaire covers 6 domains: understanding and communication, self-care, mobility, interpersonal relations, work and household roles, and community and civic roles. Responses are scored on a scale of 0 (none) to 4 (extreme/cannot do), with higher scores indicating less functional ability [32]. Previous studies have shown satisfactory psychometric properties for the Chinese WHODAS 2.0 [33, 34]. The Cronbach’s α for the WHODAS 2.0 in this study was 0.92.

Statistical analysis

Data were analyzed using SPSS 26.0 (IBM Corp., Armonk, NY, USA). Demographic and clinical characteristics were analyzed using descriptive statistics. Trajectories of BMI, performance status, nutrition status, symptom distress, physical fitness, functional ability across four time points were determined by repeated-measures analysis of variance. Generalized estimating equation (GEE) is a regression method used to examine longitudinal data over time with efficiency and no bias [35, 36]. GEE analysis was used to determine the variables associated with trajectories of functional ability (dependent variable). The selected independent variables included age, cancer stage (early vs. advanced), BMI (< 25 kg/m² vs. ≥25 kg/m²), nutrition status, symptom distress, and physical fitness.

Patient characteristics

Of the 120 eligible patients approached, 112 completed 4 assessments, a response rate of 93.3%. The average age of the participants was 56.79 years (standard deviation [SD], 8.06). The majority of participants were male (95.5%), and most were unemployed (68.8%), living with a partner (71.4%), had senior high school education (42.0%), and held Buddhist/Taoist religious beliefs (71.4%). During cancer diagnosis and the post-surgery period, most patients were non-smokers (n = 91; 81.3%) and did not drink alcohol (n = 105; 93.8%). The majority of patients were diagnosed at an advanced stage of cancer, with 46.4% at stage IV, and received CCRT (86.6%). The mean performance status score was 89.29 (SD, 2.59). According to BMI classification [37], 21.4% (n = 24) of patients were overweight, 71.4% (n = 80) were of normal weight, and 7.1% (n = 8) were underweight.

Table 1

Demographic and clinical characteristics (N = 112)
Variable	Number (%)	Mean (SD)
Age		56.79(8.06)
<65	89(79.5)
≥65	23(20.5)
Sex
Female	5(4.5)
Male	107(95.5)
Occupation
Unemployed	77(68.8)
Employed	35(31.3)
Marital status
Living alone	32(28.6)
Living with a partner	80(71.4)
Educational level
Elementary	21(18.8)
Junior high	29(25.9)
Senior high	47(42.0)
College and above	15(13.4)
Religion
None	25(22.3)
Buddhism/Taoism	80(71.4)
Christianity	7(6.3)
Smoking
Nil/ex-smoker	91(81.3)
Current smoker	21(18.8)
Drinking
Nil/ex-smoker	105(93.8)
Current smoker	7(6.3)
Sub-site
Upper	28(25.0)
Middle	51(45.5)
Lower	33(29.5)
Cancer stage
IA, IB	3(2.7)
IIA, IIB	9(8.0)
IIIA, IIIB, IIIC	48(42.9)
IV	52(46.4)
Type of treatment
Surgery + CCRT	12(10.7)
RT or CCRT	100(89.3)
Performance status (level)		89.29(2.59)
80	8(7.1)
90	104(92.9)
BMI
Underweight (< 18.5 kg/m²)	8(7.1)
Normal (18.5 kg/m² to 24.9 kg/m²)	80(71.4)
Overweight (25.0 kg/m² to 30.0 kg/m²)	24(21.4)
Abbreviations: RT, radiotherapy; CT, chemotherapy; CCRT, combined chemotherapy and radiotherapy; BMI, Body Mass Index
SD = standard deviation.

Temporal changes in body mass index, performance status, nutrition status, symptom distress, physical fitness, and functional ability

BMI slightly decreased from T0 to T3 and was lowest at T3, with statistically significant differences. Performance status (KPS score) slightly decreased from T0 to T1 and then slightly increased at T3, and differences did not reach statistical significance. Nutrition status (MNA) was lowest at T0 and increased from T0 to T3. Symptom distress (FACT-E) slightly decreased from T0 to T3 and increased slightly at T3, which was lower than T0. Physical fitness (IFIS) slightly decreased from T0 to T2 and then increased at T3, remained significantly higher at T3, which was higher than T0. Functional ability increased from T0 to T1, and then declined at T2, recovering at T3, and did not return to T0 (Table 2 and Fig. 1 − 6).

Table 2

Trajectories in body mass index, performance status, nutrition status, symptom distress, physical fitness, and functional ability over 4 times (N = 112)
Variables	T0 M(SD)	T1 M(SD)	T2 M(SD)	T3 M(SD)	F	Post-hoc, Pair-wise Comparison
Body Mass Index (BMI)	23.36(3.79)	23.06(4.05)	22.88(3.89)	22.32(3.97)	4.759*	T0,T1 > T2,T3
Performance status (KPS)	89.37(2.44)	88.47(3.62)	88.47(3.62)	88.65(3.43)	2.333
Nutrition status (MNA)	9.88(2.13)	11.09(2.38)	11.71(2.21)	11.77(2.16)	30.799***	T1,T2,T3 > T0
Symptom distress (FACT-E)	19.90(4.29)	18.74(3.35)	17.32(2.61)	17.71(3.28)	17.546***	T0 > T1 > T2,T3
Physical fitness (IFIS)	12.74(2.24)	12.63(2.63)	12.19(2.54)	13.26(2.03)	5.693**	T3 > T2,T1,T0
Functional ability (WHODAS 2.0)	30.96(8.46)	31.90(7.68)	30.71(6.50)	29.71(6.20)	3.277*	T0,T1 > T2,T3
Abbreviations:
SD = standard deviation
BMI, Body Mass Index
KPS, Karnofsky performance score
MNA, Mini Nutritional Assessment, theoretical scoring range 0 − 14
FACT-E, Functional Assessment of Cancer Therapy-Esophageal, theoretical scoring range 0 − 176
IFIS, International Fitness Scale, theoretical scoring range 5 − 25
WHODAS 2.0, World Health Organization Disability Assessment Schedule 2.0, theoretical scoring range 0 − 48

Significant predictors of functional ability

GEE analysis identified the factors associated with functional ability. EC patients who had BMI less than 25 kg/m² (β = − 0.324), less physical performance (β = − 0.278), and worst physical fitness (β = − 0.515) were more likely to have worse functional ability (Table 3).

Table 3

Significant predictors for the trajectories in functional ability based on GEE^a analysis (N = 112).
Variable	Beta	SE	95% CI		p
Age	0.003	0.0374	−0.071	0.076	0.947
Cancer stage (early vs. advanced)	−0.003	0.6325	−1.243	1.236	0.996
Body Mass Index (< 25 kg/m² vs. ≥25 kg/m²)	−0.324	0.0854	−0.491	−0.157	0.001
Physical performance (KPS score)	−0.278	0.0578	−0.392	−0.165	0.001
Nutrition status (MNA)	−0.039	0.1274	−0.288	0.211	0.761
Symptom distress (SDS)	0.084	0.0720	−0.057	0.225	0.242
Physical fitness (IFIS)	−0.515	0.1832	−0.874	−0.156	0.005
Time	−0.184	0.1905	−0.557	0.190	0.335
Intercept	43.036	6.1733	30.936	55.135	0.001
KPS, Karnofsky performance score
MNA, Mini Nutritional Assessment, theoretical scoring range 0 − 14
FACT-E, Functional Assessment of Cancer Therapy-Esophageal, theoretical scoring range 0 − 176
IFIS, International Fitness Scale, theoretical scoring range 5 − 25
WHODAS 2.0, World Health Organization Disability Assessment Schedule 2.0, theoretical scoring range 0 − 48
^a GEE, generalized estimating equation, was based on AR1 working correlation matrix.

This study investigated trajectories in BMI, performance status, nutrition status, symptom distress, physical fitness, and functional ability in patients with EC during treatment course and posttreatment. At T0, before treatment, nutrition status (MNA) was at its lowest. At T2, 3 months after beginning treatment (the end of treatment), BMI, symptom distress, physical fitness, and functional ability were at their lowest.

Our study found that patients with EC reported the lowest nutritional status at T0 (before treatment), which differs from the findings of Jia et al. [12] and Chang et al. In the study by Jia et al. [27], patient weight declined before diagnosis and then continued to decrease until 1 month after surgery. Most patients in the cohort of Chang et al. [11] had the greatest appetite loss before surgery to 1-month post-surgery, and then returning at 6-months post-surgery. These differences in findings may be because our patients had advanced-stage cancer and received RT or CCRT, while patients in the Chang et al. cohort had early-stage cancer and received surgery only or surgery combined CCRT. Patients in the Jia et al. [12] cohort had early stage cancer treated with surgery only or surgery combined CT. These results suggest that healthcare providers should consider clinical assessment of gastrointestinal-related problems that affect nutritional status and to provide suitable symptom management and nutrition consulting to minimize gastrointestinal symptoms and improve nutrition outcomes.

In the present study, EC patients had a mean physical ability (WHODAS) score of 29.71–31.90 (range, 0–100) during and after treatment, which was lower than reported by Lee et al. [15] and Lee et al. [18]. The differences in the level of physical ability between these studies may have been influenced by differences in cancer diagnosis and age. Our study included EC patients, with a mean age of 56.79. Lee et al. [15] included colorectal cancer patients, with a mean age of 62.1 years. Lee et al. [18] included head-and-neck cancer patients, with a mean age of 54.7–56.1 years. Clinical care requires physical activity recommendations that consider patient age and the side effects of treatment modalities.

Our results show that EC patients with less engagement in physical activity were more likely to have worse functional ability. This finding supports that of a previous study [15] reporting that patients were more likely to experience activity limitation (understanding and communicating, getting around, and self-care) and participation restrictions (getting along with people, household activities, and participation in society) if they had poor physical health. One-fifth of the subjects in our study were over 65 years old, and approximately one-third of the subjects were living alone. Aging and living alone decrease the likelihood of regular engagement in physical activity due to less safe conditions and the lack of social participation. These findings suggest that clinicians should educate patients to use assistive devices during movement and to create a friendly exercise environment in order to encourage increasing their level of physical activity.

Low BMI less than 25 kg/m² was significantly associated with lower functional ability. This finding supports those of previous studies [11, 12] reporting that EC patients experienced weight loss before diagnosis and continued to lose weight with the progression of cancer treatment, negatively affecting their quality of life [12]. Given that weight loss developed during treatment and post-treatment, these findings suggest that physicians should develop programs to monitor BMI and provide nutritional support care for EC patients, especially those with a BMI less than 25 kg/m².

Our results indicate that patients of older age were more likely to report worse physical functioning, but without statistical significance. Agreement between our results and those of previous studies [15–17, 38] supports the assumption that older patients have less participation in social life, activities of daily living, and mobility, and patients who are unmarried, older, and have a large number of chronic diseases are more likely to have disabilities. These findings suggest that patient evaluation and attention are needed to provide care based on the personal needs of each patient to promote their engagement in physical activity.

Limitations

This study has several limitations. First, the cohort was recruited from a single medical center in northern Taiwan, and thus does not represent the whole population of EC patients in Taiwan. The generalizability of the results of this study is limited. Future studies should be expanded to include multiple institutes to explore changes in physical ability in EC patients. Second, we did not consider exercise habits and social networks. These variables may affect physical ability. More studies are required to examine the potential factors affecting physical ability. Finally, as many patients had stage IIIA, IIIB, IIIC, or IV cancer, careful interpretation of the findings is needed as they apply to EC patients with other stages of cancer. Future studies should recruit EC patient populations with more heterogeneity to compare the differences in physical ability between patients with different cancer stages.

In this prospective study of EC patients, the nutrition status was lowest before treatment and increased after starting treatment through 6 months after the start of treatment. Their functional ability increased from pre-treatment to 1 month after starting treatment, declining at 3 months after starting treatment and reaching its lowest at 6 months after starting treatment. Lower functional ability was associated with BMI less than 25 kg/m², less engagement in physical activity, and a lower level of physical fitness.

Clinical implications

In cancer care, patient-tailored exercise training and personalized follow-up care (such as prehabilitation programs, optimizing nutrition, and using assistive devices) provided before treatment and persisting through posttreatment should increase patients’ physical ability.

Conflicts of interest/Competing interests:

None declared.

Ethics approval:

All procedures performed in studies involving human participants were in accordance with the ethical standards of the University of Wisconsin Health Sciences IRB (Number: 201801842B0) and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Consent to participate:

Informed consent was obtained from all individual participants included in the study.

Consent for publication:

This manuscript is original, is not plagiarized, and has not been published elsewhere.

Funding:

Support to Shu-Ching Chen was provided by the National Science and Technology Council (NSTC) Research Program (grant number MOST 108-2314-B-255-00-MY3) and Chang Gung Memorial Hospital Research Program (CMRP) (grant number NMRPF3J0181, NMRPF3J0182, and NMRPF3J0183) in Taiwan.

Author Contribution

Authors' contributions: All authors have agreed on the ﬁnal version and meet at least one of the following criteria [recommended by the ICMJE (http://www.icmje.org/recommendations/)]: • substantial contributions to conception and design, acquisition of data or analysis, and interpretation of data; • drafting the article or revising it critically for important intellectual content.Study design: HY Lee, BS Huang & SC Chen; Data collection and analysis: HY Lee, BS Huang, CK Tseng, PC Pai, TM Hung, YK Chao, & SC Chen; Manuscript preparation: HY Lee, BS Huang & SC Chen

Availability of data and materials:

The data supporting the findings of this study are available from the corresponding author. Restrictions apply to the availability of these data, which were used under license for this study. Data are available from the authors with the permission of the National Science and Technology Council (NSTC) and Chang Gung Memorial Hospital Research Program (CMRP).

Code availability:

Not applicable

This manuscript is not under consideration for publication in another journal and will not be submitted elsewhere until the Supportive Care in Cancer editorial process is completed.

All authors consent to the publication of the manuscript in Supportive Care in Cancer should the article be accepted by the Editor-in-chief upon completion.

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Factors associated with functional ability in patients with esophageal cancer undergoing chemoradiotherapy: a prospective longitudinal study Running head: Patient functional ability in unresectable EC

Status:

Version 1

Abstract

Purpose

Methods

Results

Conclusion

Figures

INTRODUCTION

METHODS

Design and sample

Ethical considerations

Data collection

1. Demographic and disease characteristics form

2. Karnofsky Performance Status (KPS)

3. Mini Nutritional Assessment (MNA) short form

4. Functional Assessment of Cancer Therapy-Esophageal (FACT-E)

5. International Fitness Scale (IFIS)

6. World Health Organization Disability Assessment Schedule 2.0 (WHODAS 2.0)

Statistical analysis

RESULTS

Patient characteristics

Significant predictors of functional ability

DISCUSSION

Limitations

Conclusion

Clinical implications

Declarations

Conflicts of interest/Competing interests:

Ethics approval:

Funding:

Author Contribution

Availability of data and materials:

Code availability:

References

Additional Declarations

Status:

Version 1