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Abstract

Background:

Adapted physical activity (APA) is key supportive care in cancer patients. Very few studies have evaluated APA in digestive cancers, and the eligibility and feasibility of an APA program in this population have not been clearly defined.

Objectives:

Primary objective: to analyze the reasons for failure of an APA program in digestive cancer patients. Secondary objectives: to assess patient eligibility, feasibility of an APA program, and the potential changes in patient quality of life, physical performance, and nutritional status.

Design:

APACADIG is a pilot, single-center, prospective non-randomized study.

Methods:

All consecutive patients with digestive cancer seen from January 18, 2021 to February 15, 2021, were proposed a supervised 2-month APA program.

Results:

Sixty-five consecutive patients (men 69%, median age 69.8 years old, PS 0/1: 78.5%) with mainly colorectal (38%) and pancreaticobiliary (35%) cancers were included. Forty-seven of these patients (72%) were eligible, and 22 (46.8%) accepted the APA program. The latter were more often active women, living in urban areas (59.1%) with higher socioeconomic status (40.9%). The barriers to APA were clinical, the cost of transport, lack of awareness of the benefits of APA, and a sedentary lifestyle before the cancer diagnosis. Withdrawal from APA was mainly due to changes in physical status. APA improved patients’ physical performance (6-min walk test) (distance 516.1 m ± 102.7 m vs 414.5 m ± 111.9 m; p = 0.0430).

Conclusion:

Only one-sixth of the population completed the program, and we identified several barriers to APA.

Keywords

adherence barriers digestive cancers eligibility physical activity recruitment

Background

Digestive cancers are the leading cause of cancer deaths in France. They are usually associated with impaired quality of life early on, fatigue, malnutrition, and muscle atrophy. Symptoms are often worsened by antitumor treatments.¹

In recent years, the role of adapted physical activity (APA) has become an emerging field of interest and appears to be a promising approach to improve patient quality of life and physical function.^2,3

Indeed, APA can prevent physical deconditioning, muscle atrophy, fatigue, anxiety, and depression. These benefits have been well described in various cancers, such as breast, colon, or prostate cancers, but rarely in more aggressive cancers with a poor prognosis, such as advanced oesogastric or biliopancreatic cancers.^2,4 Providing exercise guidelines to cancer patients is recommended and should include moderate intensity aerobic training for at least 30 min at least three times per week, associated with resistance training at least twice a week.⁵ Currently, these recommendations are the same as in the general population,⁶ but they are difficult to apply to patients in oncology.

The feasibility of physical activity (PA) has been studied in cancer patients, especially in breast cancer, including in the advanced and metastatic stages. One systematic review of the literature shows that studies support the safety, tolerability, and feasibility of PA for advanced breast cancer patients.⁷ Nevertheless, barriers have been identified to performing PA, such as disease- and treatment-related symptoms, less aerobic fitness, and lack of motivation or social support.^7,8 Moreover, in France, financial support is lacking, and patients must pay for APA when it is prescribed. Finally, the general population is not well informed about the benefits of APA, and most oncologists do not yet consider APA to be an integral part of cancer patient care.⁹ It is interesting to note that the intervention of a professional trainer to supervise an APA program enhances patient motivation and improves APA program completion.¹⁰ In France, a professional APA trainer is a certified exercise specialist who holds a 3-year university degree in “Sciences and Techniques of Physical and Sports Activities” (STAPS), with a specialization in APA and Health. This training includes in-depth knowledge of exercise physiology, functional assessment, and the adaptation of PA for individuals with chronic diseases, disabilities, or age-related limitations. APA professionals are specifically trained to design, implement, and supervise safe and effective exercise interventions in clinical settings. Their role is distinct from that of physiotherapists and occupational therapists: while the latter are healthcare professionals focused on rehabilitation and therapeutic care, professional APA trainers are non-medical specialists whose expertise lies in using PA as a means of prevention, functional maintenance, and health promotion in chronic disease management.

The number of studies on APA in patients with digestive cancer is limited.^11,12 A meta-analysis of 19 studies on colorectal cancer supported the feasibility and safety of APA, but only one study evaluated metastatic colorectal cancer, and 53% included post-treatment activity programs.¹³ More data are needed to confirm the value of APA in patients in all stages of digestive cancer.

The main goal of the prospective APACADIG (Activité Physique Adaptée dans les Cancers DIGestifs) study was to identify the challenges and barriers of an APA program in digestive cancer patients in daily clinical practice and whether program failures were due to ineligibility, refusal, or non-achievement.

Method

Study design

This was a pilot prospective, single-center, non-randomized study in patients during follow-up for digestive cancer. The oncologist’s team participated in a 1-h meeting and were informed about APA in cancer and its modalities.

Patient eligibility and recruitment

Inclusion criteria: All consecutive patients with digestive cancer, over 18 years old, who consulted a digestive oncologist from January 18, 2021, to February 15, 2021, were included. The oncologist proposed a 2-month protocol of supervised APA. Included patients were receiving treatment (chemotherapy, radiotherapy, and/or immunotherapy) or had stopped antitumor treatment for no more than 1 year.

Non-eligibility criteria were as follows: (1) more than 100 km from the residence to the hospital; (2) ongoing participation in another external APA program; (3) symptomatic bone metastases, central nervous system disorder; symptomatic anemia, cardiovascular contraindications, stage IV respiratory insufficiency; (4) ECOG PS (Eastern Cooperative Oncology Group Performance Status) >2 or uncontrolled pain; (5) incapacity to complete questionnaires or to be followed for medical, social, familial, geographical, or psychological reasons; and (6) insufficient time to explain the APA program estimated by the medical referent during the consultation.

After a clinical examination, the program was explained to the patients. Patients who accepted were seen by the APA monitor. In case of refusal, the reasons were registered.

The acceptance rate was the proportion of eligible patients who agreed to complete the program. The adherence rate was the mean number of sessions attended by the patients over the total number of scheduled sessions (n = 18).

This study was performed according to the World Medical Association Declaration of Helsinki research principles. Data collection was anonymized prior to analysis, and the database was created in accordance with the reference methodology MR004 of the National Commission for Information Technology and Civil Liberties (CNIL). Patients were informed of and were not opposed to the study. This was registered in the clinical chart. Patients were provided written information and oral information from the investigator and provided oral informed consent. The Ethics Committee of the University Hospital Centre of Rennes approved the study protocol as well as the oral consent procedure after information about the patients (No. 25.06). APA is part of the cancer care for digestive cancer patients according to French Guidelines¹⁴ and is recommended by ESMO Guidelines for cancer-related fatigue¹⁵; thus, this study was not registered in a WHO-approved registry.

Endpoints

The primary endpoint of the study was to analyze the reasons for APA program failure in the entire population based on different criteria: eligibility, consent, or achievement.

Secondary endpoints were as follows: (a) the rate of APA program failures due to ineligibility, refusal, or withdrawal; (b) changes in (1) the European Organization for Research and Treatment of Cancer (EORTC) Quality of Life Questionnaire (QLQ-C30) score, and the Multidimensional Fatigue Inventory (MFI-20) score, (2) physical fitness, assessed by performing the 6-min walk test (6-MWT), and (3) anthropometric, sarcopenia, and biological nutritional parameters.

Exercise intervention

The supervised exercise-based intervention consisted of two weekly sessions over an 8-week period. Each session lasted 45–60 min and included a 10-min warm-up, a main phase structured as a circuit of 7–10 full-body resistance exercises, and a 5-min cool-down. The exercises primarily targeted muscular strength, with minimal emphasis on aerobic components. The program incorporated bodyweight exercises—some performed with chair assistance—and the use of small equipment, including resistance bands (7 kg resistance) and light dumbbells (500 g to 1 kg). Each exercise followed a time-based protocol of 45 s of effort interspersed with 20 s of rest. All sessions were delivered in small groups (2–4 participants) under the supervision of a certified professional APA trainer.

Data collection

Patient characteristics were recorded when the APA program was proposed during the medical consultation. Physicians had to complete a checklist of potential reasons for ineligibility or refusal.

Demographic data were collected at inclusion from the patient’s electronic medical record. This included gender, birth date, age at baseline, ECOG PS, social status (living alone and/or with a caregiver or not), employment status, comorbidities assessed by the adjusted Charlson comorbidity index,¹⁶ social environment, site of cancer, date of diagnosis, tumor stage, and antitumor treatment administered.

Physical fitness was assessed by the 6-MWT in a 20-m flat corridor. The patients were asked to go as far as possible, in meters, for 6 min.

Anthropometric and nutritional parameters included height, body weight, body mass index in kg/m². Fat, mass, and bone masses were assessed using a body composition analyzer (DC-360; TANITA Corporation, Tokyo, Japan). Albumin and pre-albumin were measured in a blood sample from each patient in the same laboratory. Nutrition was evaluated using a numerical visual scale (0–10).¹⁷

Sarcopenia was assessed by measuring the psoas muscle area at L3 on computed tomography (CT), which was performed as near as possible to baseline (T0) and the end of the program (T1), but no additional CT was performed for this specific indication.

Quality of life was assessed using the QLQ-C30, a 30-item, self-administered questionnaire that evaluates a global quality-of-life domain, five functional domains (i.e., physical, role, emotional, cognitive, and social), three symptom domains (i.e., pain, fatigue, and nausea), and six single items (i.e., dyspnea, insomnia, appetite loss, diarrhea, constipation, and financial impact).

Fatigue was assessed by the MFI-20 questionnaire on five items (global fatigue, physical and mental fatigue, reduction of activities, and reduction of motivation).

Level of physical activity (low, moderate, or high) was estimated according to the International Physical Activity Questionnaire (IPAQ) criteria and the ECOG PS, which can be summarized as sedentary (low), active at home (moderate), or active even outdoors (high).

All the physical and biological parameters described above were assessed at both T0 (beginning of the APA program) and T1 (end of the APA program, 2 months later).

This study was reported according to the STROBE guidelines statement¹⁸ (Supplemental File).

Statistical analysis

Prism6© (GraphPad Software, San Diego, CA, USA) was used for the statistical analysis. The results were analyzed by the Pearson chi-square test for the primary outcome, and by ANOVA for the secondary outcomes. Differences were considered significant when the p value was⩽0.05.

Results

Recruitment and follow-up

Sixty-five consecutive patients were prospectively included during the 1-month inclusion period. Eighteen of these patients (27.7%) were ineligible, mainly for geographical (n = 8, 44%) or medical (n = 6, 33%) reasons (Figure 1). Among the 47 eligible patients, the acceptance rate was 47% (22/47), and among the 22 patients who accepted, 11 performed at least one session of the APA program (50%). The flow chart summarizes the reasons for ineligibility, refusal, and drop-out (Figure 1). The overall adherence rate to the APA program was 60.8% (Figure 2).

Figure 1.

Flow chart of the 65 patients consecutively included to integrate the APA program.

Figure 2.

Rate of patients performing the planned APA program.

Patient’s characteristics at baseline

The median age of the population was 72 (39–85 years old; Table 1). Most patients were men (69.2%), and most were fit with an ECOG PS of 0 or 1 (78.5%) and highly active (64.6%). Patients lived equally in urban or rural areas, and most lived with a partner (80%). There was a high burden of comorbidities, with a mean Charlson index of 8.2. The socioprofessional distribution was similar to that of the general population (according to data from the National Institute of Statistics and Economic Studies for the year 2022 in France); however, there were more craftsmen, merchants, or company directors (16.9% vs 8.8% in the general population) and fewer managers and intellectual professions (15.4% vs 22.4%). Most patients had colorectal (n = 28, 38.5 %) or biliopancreatic (n = 25, 35.4 %) cancers (Table 1) with distant metastases (64.6%). Most patients were receiving antitumor treatments (69.2%).

Table 1.

Baseline patient demographics and clinical characteristics of patients included in the study (n = 65).

Patient characteristics	N (%)
Sex, n (%)
Male	45 (69.2)
Female	20 (30.8)
Median age, years	72
ECOG PS, n (%)
0	17 (26.1)
1	34 (52.3)
2	12 (18.5)
3	1 (1.5)
4	1 (1.5)
Comorbidities (Charlson index/24)	8.2
Estimated activity at T0, n (%)
Low	6 (9.2)
Moderate	17 (26.2)
High	42 (64.6)
Living area, n (%)
Urban	30 (46.2)
Rural	35 (53.8)
Socioprofessional category, n (%)
Farmers, operators	3 (4.6)
Craftmen, merchants, company directors	11 (16.9)
Managers, higher intellectual professions	10 (15.4)
Intermediate professions	9 (13.9)
Employees	18 (27.7)
Workers	3 (4.6)
Without professional activity	5 (7.7)
Missing data	6 (9.2)
Social environment, n (%)
Social isolation	6 (9.2)
Living alone with regular intervention of a relative	7 (10.8)
Living with a partner	52 (80)
Type of cancer, n (%)
Colon: rectum	25 (38.5)
Pancreas: cholangiocarcinoma	23 (35.4)
Esophagus: stomach	8 (12.3)
Neuroendocrine tumor	4 (6.2)
Anal	1 (1.5)
GIST	1 (1.5)
Intestine	1 (1.5)
Other	2 (3.1)
Metastases, n (%)	42 (64.6)
Sites of metastases, n (%)
Liver	27 (41.5)
Peritoneum	13 (20.0)
Lymph nodes	12 (18.5)
Lung	10 (15.4)
Bone	4 (6.1)
Ongoing antitumor treatment, n (%)	45 (69.2)

ECOG PS, Eastern Cooperative Oncology Group Performance Status; GIST, Gastrointestinal stromal tumor.

Primary outcome

Characteristics of eligible versus ineligible patients

Forty-seven of the 65 included patients were eligible for the APA program. The main reasons for ineligibility were the distance between the residence and the hospital (n = 8; 44%) and impaired physical function or uncontrolled pain (n = 5; 28%; Figure 1). The characteristics of eligible patients are presented in Table 2. Eligible and ineligible patients differed in sex ratio (55% vs 74.5% of men, respectively), living area (rural: 66.7% vs 48.9% respectively), and socioprofessional categories (higher and intermediate intellectual profession: 33.1% vs 16.6% and farmers, workers, merchants, or employees: 50.3% vs 60.1%), but the differences were not statistically significant. More eligible patients had metastatic disease (p = 0.023).

Table 2.

Comparison of characteristics of the 47 eligible patients and the 18 ineligible patients in the APA program.

Characteristics	Eligible patients (n = 47)	Ineligible patients (n = 18)	p Value
Sex, n (%)
Male	35 (74.4)	10 (55.5)	0.13
Female	12 (25.6)	8 (45.5)
Median age, years	71	72
ECOG, n (%)
0	13 (27.7)	4 (22.5)	0.18
1	24 (51.1)	10 (55.5)
2	10 (21.3)	2 (11)
3	0 (0)	2 (11)
Comorbidities (Charlson index/24)	8.3	7.9	0.59
Estimated activity at T0, n (%)
Low	4 (8.5)	2 (11)	0.73
Moderate	12 (25.5)	5 (27.8)
High	31 (66.0)	11 (61.2)
Living area, n (%)
Urban	24 (51.1)	6 (33.3)	0.19
Rural	23 (48.9)	12 (66.7)
Socioprofessional category, n (%)
Farmers, operators	1 (2.1)	2 (11)
Craftmen, merchants, company directors	10 (21.3)	1 (5.6)
Managers, higher intellectual professions	9 (19.1)	1 (5.6)
Intermediate professions	7 (14.9)	2 (11)
Employees	11 (23.4)	7 (38.9)
Workers	2 (4.3)	1 (5.6)
Without professional activity	4 (8.5)	1 (5.6)
Missing data	3 (6.4)	3 (16.7)
Social environment, n (%)
Social isolation	4 (8.5)	2 (11.1)	0.78
Living alone with regular intervention of a relative	5 (10.6)	2 (11.1)
Living with a partner	38 (80.9)	14 (77.8)
Type of cancer, n (%)
Colon: rectum	18 (38.3)	7 (38.9)	0.92
Pancreatobiliary	18 (38.3)	5 (27.8)
Esophagus: stomach	5 (10.7)	3 (16.7)
Neuroendocrine tumor	2 (4.3)	2 (11.1)
Anal	1 (2.1)	0 (0)
GIST	1 (2.1)	0 (0)
Intestine	1 (2.1)	0 (0)
Other	1 (2.1)	1 (5.5)
Metastases, n (%)	32 (68.1)	10 (55.6)	0.023
Site of metastases, n (%)
Liver	20 (62.5)	7 (70)
Peritoneum	10 (31.3)	3 (30)
Lung	8 (25)	2 (20)
Lymph nodes	6 (18.7)	6 (60)
Bone	4 (12.5)	0 (0)
Ongoing antitumor treatment, n (%)	34 (72.3)	11 (61.1)
Treatment toxicity, n (%)
Any grade	16 (72.2)	9 (50)	0.30
Grade 3–4	3 (13.5)	^a

Missing data.

APA, adapted physical activity; ECOG, Eastern Cooperative Oncology Group.

Characteristics of participants versus patients who refused the APA program

Twenty-five of the 47 eligible patients refused to participate in the protocol for various reasons (Figure 1). Patients who accepted the program were more active (p = 0.040), more frequently women (36.4% vs 16%, p = 0.09), had a better performance status (PS 0:41% vs 16%; p = 0.032), and had more treatment toxicities at inclusion (p = 0.017) than those who did not accept (Table 3). There was also a difference in gender distribution (84% of men who refused vs 63% of the patients who accepted), socioprofessional categories (20% of managers, intellectual professions, and intermediate professions in patients who refused vs 50% of the participants), type of cancer, and the presence of metastases (76% vs 59%, respectively).

Table 3.

Comparison of characteristics of the 47 eligible patients depending on whether they refused (n = 25) or accepted (n = 22) the APA program.

Characteristics	Eligible patients (n = 47)	N (%)		p Value
Characteristics	Eligible patients (n = 47)	Patients who refused (n = 25)	Patients who accepted (n = 22)	p Value
Sex, n (%)
Male	35 (74.4)	21 (84)	14 (63.6)	0.09
Female	12 (25.6)	4 (16)	8 (36.4)
Median age, years	72	71	71
ECOG, n (%)
0	13 (27.7)	4 (16)	9 (41)	0.032
1	24 (51.1)	17 (68)	7 (31.8)
2	10 (21.3)	4 (16)	6 (27.3)
3	0 (0)	0 (0)	0 (0)
Comorbidities (Charlson index/24)	8.3	8.6	7.9	0.36
Estimated activity at T0, n (%)
Low	4 (8.5)	3 (12)	1 (4.6)	0.040
Moderate	12 (25.5)	9 (36)	3 (13.6)
High	31 (66.0)	13 (52)	18 (81.8)
Living area, n (%)
Urban	24 (51.1)	11 (44)	13 (59,1)	0.24
Rural	23 (48.9)	14 (56)	9 (40,9)
Socioprofessional category, n (%)
Farmers, operators	1 (2.1)	1 (4)	0 (0)
Craftmen, merchants, company directors	10 (21.3)	6 (24)	4 (18.2)
Managers, higher intellectual professions	9 (19.1)	4 (16)	5 (22.7)
Intermediate professions	7 (14.9)	1 (4)	6 (27.4)
Employees	11 (23.4)	8 (32)	3 (13.6)
Workers	2 (4.3)	1 (4)	1 (4.5)
Without professional activity	4 (8.5)	4 (16)	0 (0)
Missing data	3 (6.4)	0 (0)	3 (13,6)
Social environment, n (%)
Social isolation	4 (8.5)	2 (8)	2 (9.1)	0.49
Living alone with regular intervention of a relative	5 (10.6)	3 (12)	2 (9.1)
Living with a partner	38 (80.9)	20 (80)	18 (81.8)
Type of cancer, n (%)
Colon: rectum	18 (38.3)	12 (48.0)	6 (27.3)	0.69
Pancreatobiliary	18 (38.3)	8 (32.0)	10 (45.5)
Esophagus: Stomach	5 (10.7)	3 (12.0)	2 (9.2)
Neuroendocrine tumor	2 (4.3)	1 (4)	1 (4.5)
Anal	1 (2.1)	0 (0)	1 (4.5)
GIST	1 (2.1)	0 (0)	1 (4.5)
Intestine	1 (2.1)	0 (0)	1 (4.5)
Other	1 (2.1)	1 (4)	0 (0)
Metastases, n (%)	32 (68.1)	19 (76)	13 (59.1)	0.36
Site of metastases, n (%)
Liver	20 (42.6)	12 (48)	8 (36.4)
Peritoneum	10 (21.3)	3 (12)	7 (31.8)
Pulmonary	8 (17)	5 (20)	3 (13.6)
Lymph nodes	6 (12.8)	4 (16)	2 (9.1)
Bone	4 (8.5)	2 (8)	2 (9.1)
Ongoing antitumor treatment, n (%)	34 (72.3)	18 (72)	16 (72.7)
Treatment toxicity, n (%)
Any grade	26 (47)	10 (40)	16 (72.2)	0.017
Grade 3–4	5 (10.6)	1 (4)	3 (13.5)

APA, adapted physical activity; ECOG, Eastern Cooperative Oncology Group.

Characteristics of patients according to their participation in or not in the program

Eleven of the included patients (n = 22) dropped out before the beginning of the program because of the rapid onset of disabling symptoms and fatigue (Figure 1). There were 4 patients with colorectal cancer and 6 with pancreatobiliary cancer, up to 11 who dropped out before the program, compared to 2 and 4, respectively, in the group of 11 patients that began the program. Indeed, the types of cancer varied more in the group of patients that began the program (intestine n = 1, anus n = 1, GIST n = 1). These patients were also more fit (PS 0–1: 10/11 vs 6/11) and highly active (11/11 patients vs 7/11 patients; Table 4). There was no clear difference in the other characteristics, including metastasis stage. The limited number of patients in each group prevented statistical analysis.

Table 4.

Comparison of patient’s characteristics between those who began the program (n = 11) and those who dropped out before the beginning (n = 11), among the patients who accepted the APA program (n = 22).

Characteristics	n = 22
Characteristics	Patients who dropped out (n = 11)	Patients who began the program (n = 11)
Sex, n
Male	7	7
Women	4	4
Median age, years	73	71
ECOG PS, n
PS 0–1	6	10
PS 2	5	1
Comorbidities (Charlson index /24)	8.4 (2.8)	7.5 (3.4)
Estimated activity, n
Low	1	0
Moderate	3	0
High	7	11
Living area, n
Urban	7	6
Rural	4	5
Socioprofessional categories, n
Farmers, operators	0	0
Craftmen, merchants, company directors	2	2
Managers, higher intellectual professions	1	4
Intermediate professions	3	3
Employees	1	2
Workers	1	0
Without professional activity	0	0
Missing data	3	0
Social environment, n
Social isolation	0	2
Living alone with regular intervention of a relative	2	0
Living with a partner	9	9
Type of cancer, n
Colon: rectum	4	2
Pancreas: cholangiocarcinoma	6	4
Esophagus: stomach	1	1
Neuroendocrine tumor	0	1
Anal	0	1
GIST	0	1
Intestine	0	1
Other	0	0
Metastases, n	7	6
Site of metastasis, n
Liver	4	4
Peritoneum	4	3
Pulmonary	2	1
Lymph nodes	1	1
Bone	1	1
Ongoing antitumor treatment, n	10	6
Treatment toxicity, n
Toxicity	7	9
Grade 3–4	3	3

ECOG, Eastern Cooperative Oncology Group Performance Status.

Secondary outcomes

Rate of APA program failure

The non-eligibility rate was 27.7% (18/65), the refusal rate was 53% (25/47), and the withdrawal rate was 50% (11/22; Figure 1).

Associations between physical activity and quality of life and fatigue

The global quality of life score and the global fatigue score remained stable during the APA program (MFI-20; Table 5). There was no significant difference in the items of QLQ-C30 between the beginning and the end of the program.

Table 5.

Secondary outcomes.

Outcomes	Baseline (T0)	End of the study (T1)	p Value
Physical fitness, mean (SD)
6-min walking distance (m)	414.5 (117.2)	516.1 (102.7)	0.0430
Quality of life (EORTC QLQ-C30), mean (SD)^a
Global health	56.25 (18.23)	65.62 (10.39)	0.2869
Fatigue (MFI-20), mean (SD)
Global score	57.09 (12.28)	52.09 (10.66)	0.3201
Antropometrics, mean (SD) or n (%)^b
Weight (kg)	71.32 (18.59)	69.94 (17.68)	0.8740
BMI (kg/m²)
Mean (SD)	24.11 (4.743)	23.71 (4.749)	0.8603
Fat mass (kg)	20.81 (7.082)	19.58 (7.280)	0.7204
Muscle mass (kg)	47.97 (11.65)	47.82 (10.97)	0.9787
Basal metabolic rate (Kcal)	1485 (361)	1475 (341.4)	0.9547
Muscle atrophy measurement, mean (SD)
L3 psoas area (cm²)	10.63 (4.83)	10.25 (4.39)	0.9487
Nutritional parameters, mean (SD)
Albumin^c	37.29 (3.90)	33.81 (5.36)	0.3303
Pre-albumin^d	0.23 (0.08)	0.21 (0.06)	0.7053
Ingests ^e(0–10 numerical scale)	8.20 (2.39)	9.50 (0.85)	0.3684

There are missing data for EORTC QLQ-C30 (n = 8/11).

There are missing data for anthropometrics (n = 9/11).

There are missing data for albumin (n = 7/11).

There are missing data for pre-albumin (n = 6/11).

There are missing data for ingests (n = 10/11).

BMI, body mass index; EORTC, European Organization for Research and Treatment of Cancer; MFI, Multidimensional Fatigue Inventory; SD, standard deviation.

Changes in physical performance

A significant improvement of 24% was observed in the 6-MWT between T0 (414.5 m ± 111.9 m) and T1 (516.1 m ± 102.7 m; p = 0.0430; Table 5).

Changes in anthropometric measurements and nutritional parameters

There was no change between T0 and T1 for muscle or fat mass, baseline metabolic ratio, food intake, or biological parameters (Table 5).

Changes in muscle atrophy measurement

There was no difference in the L3-psoas area before (10.63 cm²± 4.83 cm²) and after (10.25 cm² ± 4.39 cm²) the PA program (Table 5).

Discussion

This APACADIG study evaluated the participation in a supervised APA program that was systematically proposed to unselected patients with digestive cancer. In the few studies on APA in cancer patients, the ineligibility rate (87% in advanced breast cancer, 82% in prostate cancer, and 39% in advanced lung cancer) was often high, due to stricter exclusion criteria, including old age or a life expectancy <6 months,^19,20 even though APA has very few absolute physical contraindications. In our study, 27% of unselected patients were ineligible for APA according to their oncologists. We identified several barriers to performing APA in patients with digestive cancers. These included the following: living more than 100 km from the hospital, impaired physical function, and the presence of uncontrolled pain, while traditional physical contraindications to APA (heart disease, etc.) were uncommon. Eligible patients more frequently had metastatic disease than ineligible patients (p = 0.023), suggesting that metastatic disease should not be an exclusion criterion on its own. Moreover, although explaining APA during a consultation may be considered time-consuming by the oncologist, only one patient in our study was found to be ineligible for this reason. The main reasons for ineligibility in the literature are ECOG PS >2, medical contraindications (e.g., heart disease), life expectancy <6 months, symptomatic bone metastases, patients who already meet APA objectives, and living too far from the hospital. The ineligibility rates in studies evaluating digestive cancers ranged from 30%²¹ to 63.9%.²² The reasons were similar but also included ileus and enteral nutrition. Improving the definitions of eligibility criteria for exercise protocols in digestive cancers could increase the number of participants and help standardize the population for the evaluation of APA in future studies.

The acceptance rate for participation in the APA program in the APACADIG study was 47%. In the literature, these rates range from more than 90% in patients with breast cancer¹⁹ to 30% in those with lung²³ or prostate cancer.²⁰ Obviously, the more highly selected the patients are, the better the participation rate. In our study, the protocol was followed by more active women, living in urban areas, and/or patients with a higher socioeconomic status. The participation of more women in the APA program is supported by a higher participation in breast cancer studies than in prostate cancer studies.^20,24,25 A high PA level and a higher socioprofessional status have also been associated with participation in breast cancer patients.^20,26 Patients with higher socioprofessional status may have a better understanding of the benefits of APA in their disease and in treatment tolerance. Moreover, these patients may spend more time practicing APA because of greater awareness of its potential benefits. The barriers preventing participation in APA in our study were geographical (distance from the hospital, especially rural areas), financial (lack of financial support for transport), social (lower socioeconomic status), personal (no perception of the need for APA in their disease), and a sedentary lifestyle before the cancer diagnosis. The distance to the treatment center is a well-known barrier.²³ Treatment side effects are another supposedly important barrier to the practice of APA, which was identified in 50%–80% of patients with various cancers in a systematic review.⁸ Unexpectedly, patients who consented to the APA program in our study had twice as many side effects (including severe grade 3–4 toxicity) as those who did not, thus questioning this barrier. Hypothetically, oncologists promote PA to reduce treatment side effects such as oxaliplatin neurotoxicity or fatigue, which could increase participation in the program. Financial issues were also a major barrier, because patients could not afford to pay the membership fee for the PA program.²⁷ Considering the benefits of APA²⁶ and especially supervised APA²⁸ in oncology, reimbursement of APA and transportation by healthcare systems are important, especially for patients living in rural areas.

The lack of understanding of the potential benefits of APA in patients may be partly due to oncologists’ lack of knowledge. One recent study showed that about 80% of oncology care providers were not aware of any exercise guidelines for cancer and stated that their knowledge of when, how, and which patients to refer to exercise programs was poor.²⁹ A French survey reported that although 72% of oncologists acknowledged the benefits of PA in early-stage disease, only 55% agreed to propose it to patients with advanced disease. Only 26% of oncologists recommended PA to their metastatic patients.⁹ However, as recently shown by the APACAP study,³⁰ which only included patients with advanced pancreatic cancer, PA recommendations should not be limited by the type, severity, or stage of cancer.³¹ In fact, special attention should be paid to patients who may be reluctant to participate for the reasons mentioned above, and consultations to help motivate the patient should be organized regularly throughout follow-up.

In our study, 50% of patients dropped out before beginning the APA program due to disabling symptoms and fatigue, which are particularly frequent in digestive oncology. Indeed, patients who dropped out mainly had colorectal or pancreatobiliary cancers, which have well-known symptom burdens, while those who participated had other, less severe cancers, including intestine, anus, and GIST. Physical function was rapidly impaired, preventing participation in the APA program. Thus, it could be important for the oncologists to propose supervised APA early in the disease, especially in colorectal and pancreatobiliary cancer patients, and even in sedentary patients.

We observed a significant improvement in physical performance in patients who completed the APA program, with no deterioration in quality of life or increase in fatigue. This was similar to previous studies.³² Lack of statistically significant improvement in the patients in the APA group in our study, especially of anthropometric measurements and nutritional parameters, may have been due in part to a lack of power from the number of patients studied.

This study has limitations. The single-center design with a small number of patients limits the generalizability of the results, and the lack of alternative options, such as interventions from other professionals (physiotherapists) or virtual APA sessions. A selection bias related to the distance between the patient’s home and hospital cannot be excluded because the cutoff was 100 km. Patients who were already active tended to be lost to follow-up at each step of the study (Figure 1).

Also, although participating oncologists were informed about the benefits of APA and participated in the APACAP study,³⁰ their motivation and involvement probably varied. Regular professional APA training is needed for oncologists. Measurement of patient activity is another limitation of the study. For more relevant analysis of the population, the IPAQ should be systematically assessed at inclusion.

Finally, there are many ways of overcoming these barriers. The use of digital aids can be increased (connected watches, visio conferences, or motivational calls), access to local associations can be facilitated, awareness of the benefits of APA should be increased in doctors and caregivers, and disease symptoms that could prevent patient participation must be taken into account.

Conclusion

While most patients in our study were eligible for APA, the participation rate was low. This study identified barriers to participation in a supervised APA program in patients with digestive cancer (distance, impaired physical function, lack of awareness of the benefits, etc.). Certain sociodemographic characteristics could help predict APA program failure. A delay between the diagnosis of the disease and the beginning of APA may restrict the feasibility of this program. To increase feasibility, APA should begin as rapidly as possible after diagnosis. Because of the positive effect of these programs on physical performance and quality of life in digestive cancer patients, it is urgent for public health policies to facilitate access to APA.

Supplemental Material

sj-pdf-1-tam-10.1177_17588359251378284 – Supplemental material for Potential barriers to performing adapted physical activity in patients with digestive cancer: results of the prospective observational APACADIG study

Supplemental material, sj-pdf-1-tam-10.1177_17588359251378284 for Potential barriers to performing adapted physical activity in patients with digestive cancer: results of the prospective observational APACADIG study by Clémence Trihan, Cindy Richard, Emeric Boisteau, Thomas Grainville, Géraldine Perkins, Claire Gouriou, Eugénie Rigault, Anne-Sophie Guerard, Etienne Le Brelot, Amélie Rebillard, Pascal Hammel and Astrid Lièvre in Therapeutic Advances in Medical Oncology

Footnotes

Acknowledgements

Miss Dale Roche-Lebrec for English editing.

Declarations

ORCID iDs

Clémence Trihan

Emeric Boisteau

Pascal Hammel

Supplemental material

Supplemental material for this article is available online.

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