How do practitioners prescribe exercise to patients with breast cancer? Professional perspectives on the implementation of aerobic exercise guidelines for patients with breast cancer undergoing chemotherapy.

doi:10.21203/rs.3.rs-2236450/v1

Download PDF

Research Article

How do practitioners prescribe exercise to patients with breast cancer? Professional perspectives on the implementation of aerobic exercise guidelines for patients with breast cancer undergoing chemotherapy.

https://doi.org/10.21203/rs.3.rs-2236450/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Purpose:

The benefits of exercise for cancer are well established. However, how experienced accredited exercise physiologists (AEPs) and medical professionals implement exercise guidelines when prescribing/recommending aerobic exercise to patients with breast cancer undergoing chemotherapy remains unknown.

Methods:

A four round, two phase, survey was conducted. Four cancer-specific AEPs, four oncologists, and one breast cancer surgeon (median 13-yr breast-cancer-specific experience) completed phase one. Eighty-four AEPs (median 5-yr experience) completed phase two. Phase one participants answered open- and close-ended questions regarding how they implement cancer-specific aerobic exercise guidelines for patients with breast cancer patients undergoing chemotherapy, and what information they believe should be collected to guide exercise prescription. All questions agreed upon in phase one (>70% rating 7-9 on a 0-9 Likert Scale) were rated by AEPs in phase two.

Results:

Subjective questioning by AEPs should consider the stage, type, and location of breast cancer, treatments, side effects, and exercise preferences and expectations. Objective assessment should include upper-arm circumference, strength, and range of motion. Separating aerobic exercise into 5-to-9-minute bouts was considered appropriate and exercising to exhaustion should be avoided. Exercise intensity and duration should be adjusted throughout chemotherapy to improve tolerance and adherence.

Conclusion:

This study identifies how professionals approach exercise assessment and prescription in patients with breast cancer undergoing chemotherapy. These findings can help guide practice and inform future guidelines.

Implications for Cancer Survivors:

This research helps exercise professionals make better decisions when prescribing exercise to patients with breast cancer undergoing chemotherapy, improving the quality of care for this population.

physical activity

breast carcinoma

exercise prescription

Breast cancer is the most commonly diagnosed cancer in females worldwide, with over 2.1 million new cases each year [1]. Breast cancer treatment is associated with many side effects causing reductions in physical function and quality of life, both during treatment and survivorship [2, 3]. Consequently, physical inactivity is common during and following breast cancer treatment, increasing associated cardiovascular health risks [4, 5]. High level evidence demonstrates that exercise following breast cancer diagnosis is inversely associated with cardiovascular, all cause, and cancer related mortality [6]. Furthermore, it is well established that exercise reduces anxiety, depression, and fatigue, whilst improving health related quality of life and physical function, in people with cancer [3, 7, 8].

Given the significant benefits of exercise for this population, several exercise guidelines for cancer survivors have been developed. Initial guidelines were developed by Exercise and Sports Science Australia (ESSA) in 2009 [9], and the American College of Sports Medicine (ACSM) in 2010 [10]. Both concluded that exercise was safe and well tolerated during and following cancer treatment, and could improve physical fitness, quality of life and reduce cancer-related fatigue. However, specific exercise prescription recommendations (i.e., frequency, intensity, time, type (FITT principles)) were not provided for specific cancers or treatment modalities [9, 10]. Instead, exercise recommendations largely conformed to the physical activity guidelines for adults with chronic health conditions. This lack of specificity suggested that these recommendations may not be suitable for all cancer patients [9]. In 2018, the Clinical Oncology Society of Australia (COSA) released a position statement on exercise in cancer care [11]. They recommend that all cancer patients should avoid inactivity and be as physically active as their current abilities allow. They also suggested that exercise should be individualised, and where possible, prescribed and delivered by an accredited exercise physiologist or physiotherapist [11]. Like earlier guidelines, their recommendations closely aligned with population-based physical activity guidelines, and specific exercise recommendations for different types of cancer and cancer treatments were not provided. In 2019, ESSA and ACSM updated their exercise guidelines for cancer survivors through a position statement and international multi-disciplinary roundtable, respectively [7, 2]. ESSA’s updated position statement provided FITT guidelines for cancer survivors, as well as FITT recommendations, considerations, and precautions for specific cancer related side-effects and patient comorbidities [2]. ACSM provided FITT guidelines specific to improving cancer related side-effects, including anxiety, depression, fatigue, quality of life, physical function, and lymphedema [7]. ACSM’s guidelines were developed using primary evidence which supported the benefits of exercise, while ESSA’s updated position statement was developed through a combination of opinions, evidence, and clinical experience. Both guidelines were designed to inform and assist exercise professionals when planning exercise interventions for cancer survivors.

While the last decade has seen improvements in the specificity of exercise recommendations for cancer survivors, they are still generalised to all cancers, regardless of treatment and cancer type. Similarly, while the updated guidelines indicate that exercise prescription should be individually tailored by experienced allied health professionals that specialise in exercise therapy (e.g., accredited exercise physiologists), they are still open to interpretation. Consequently, how exercise professionals integrate these guidelines with their own clinical experience and judgement when prescribing exercise specifically to patients with breast cancer undergoing chemotherapy remains unknown. Moreover, sound patient assessment is key to clinical decision making and prescribing individualised exercise [12]. The collection of subjective (i.e., client history) and objective (i.e., physical testing) information directly impacts the decision-making process of exercise professionals [13]. However, the specific subjective and objective information that experienced exercise professionals collect to base their clinical decisions on when prescribing exercise to patients with breast cancer undergoing chemotherapy has not been researched. It is also unclear if medical professionals that recommended exercise services to patients with breast cancer (i.e., oncologists, surgeons) interpret exercise guidelines in a similar manner, and agree with the subjective and objective information collected by exercise professionals.

Thus, the aims of this study were to 1) explore the interpretation and application of exercise oncology guidelines for providing specific individualised exercise interventions to patients with breast cancer undergoing chemotherapy by a highly experienced interprofessional group of clinicians; and 2) determine the level of agreement with these outcomes by a broader sample of accredited exercise physiologists that have experience working with people with cancer.

A four round electronic survey was conducted across two phases using RedCAP Survey Platforms (v10.0.19, TN, USA) and Survey Monkey Inc. (CA, USA) between October 2020 and September 2022. The study was granted ethical approval by the University of South Australia Human Research Ethics Committee (Protocol Number 203189).

Phase 1

Phase one comprised of three survey rounds and sought opinions from a select group of experienced accredited exercise physiologists (AEPs) specialising in cancer care, medical and radiation oncologists, and breast cancer surgeons. Phase one was designed using an established Delphi methodology [14, 15], with the number of survey rounds, analytical approach, and threshold for agreement between participants determined a priori. Although the optimal number of participants to achieve agreement is not formally established, it is suggested a minimum of 10 participants per area of expertise is suitable [15]. Therefore, we aimed to identify and recruit 15 AEPs specialising in cancer care, and 15 oncologists/breast cancer surgeons to account for potential dropouts. To be included, AEPs required a current accreditation with ESSA and a minimum of five years academic or clinical experience researching/working with patients with cancer. Oncologists and breast cancer surgeons required accreditation with their relevant governing body (i.e., Royal Australasian College of Physicians), and a minimum of five years of experience treating or operating on patients with breast cancer. AEPs, oncologists, and breast cancer surgeons that met the inclusion criteria were identified via governing body websites, profiles on business/work pages, and word of mouth, and directly invited via email to participate in phase one of this study. Once confirming interest, participants entered details into a RedCAP survey form regarding their profession, governing body, years of experience in their given field, and years of experience working with patients with breast cancer.

In the first round, AEPs, oncologists, and breast cancer surgeons provided written responses to 14 open-ended questions. Questions were designed to understand what subjective and objective information AEPs, oncologists, and breast cancer surgeons believe is necessary for AEPs to collect to prescribe a tailored exercise intervention to patients with breast cancer undergoing chemotherapy, and what information should be included in a referral from an oncologist/breast cancer surgeon to an AEP. In round one exercise guidelines for cancer survivors [7, 10, 11] were also presented, and AEPs, oncologists, and breast cancer surgeons answered open-ended questions regarding their appropriateness for patients with breast cancer undergoing chemotherapy, and if there was anything that they believe should be adapted for this specific population given their clinical knowledge and experience in their given fields. Additional open-ended questions regarding the most suitable exercise modalities, intensities, frequencies, and durations were also answered. All questions are detailed in supplementary digital content 1, table 1. Any response that appeared more than twice within areas of subjective, objective, referral, or prescription was converted into a close ended question for round two. Answers were crossed checked by a co-author (HB).

In round two, close ended questions derived from answers gathered in round one, were sent to participants to rate on a 9-point Likert scale ((1–3 = disagree; 4–6 = neither agree nor disagree; 7–9 = agree). This scale has previously been used successfully to define key domains for subjective assessments by AEPs [12]. Questions were categorised into subjective, objective, referral, and prescription parameters relating to the FITT principles. AEPs, oncologists, and breast cancer surgeons were asked to rate each question relating to its importance and suitability when receiving/giving a referral, collecting subjective and objective information, or prescribing/recommending exercise to this population. They were also given the opportunity to provide further comments at the end of each section. Agreement was considered between participants for each question if >70% scored 7-9 (agree) [16]. Questions that reached agreement were presented to participants in round three for informative purposes as “questions that have reached agreement”. The percentage of agreement achieved, median score, and interquartile range for each question were also presented.

Questions that did not reach agreement in round two were again presented to participants in round three. The median and interquartile range of each question were provided for consideration when rating each question. AEPs, oncologists, and breast cancer surgeons were also given the opportunity to consider comments (de-identified) from other participants in round two when making their decision. Questions that did not reach agreement after round three were interpreted as pieces of information AEPs, oncologists, and breast cancer surgeons could not agree upon as necessary to include in a referral to an AEP, collect subjectively or objectively, or consider when prescribing/recommending exercise to patients with breast cancer undergoing chemotherapy.

The link to access each round of the survey in phase one was sent to AEPs, oncologists, and breast cancer surgeons individually via email. Weekly email reminders were sent for three consecutive weeks for each round, or until a response had been gathered. AEPs, oncologists, and breast cancer surgeons had to complete round one to be involved in round two, and round two to be involved in round three. If no response had been received following three email reminders (across three consecutive weeks), participants were deemed to have withdrawn from the study.

Phase 2

AEPs are routinely tasked with interpreting exercise guidelines in practice. Therefore, phase two was designed to determine how well the interpretation of exercise oncology guidelines by a highly experienced interprofessional group of AEPs, oncologists, and breast cancer surgeons, was supported by practicing AEPs with experience prescribing exercise to cancer populations. AEPs currently accredited with ESSA and with any level of experience prescribing exercise to cancer populations were eligible to participate in this phase. Potential participants were identified by searching the ESSA website using the “find an AEP” function [17]. The study was also advertised via social media to find additional participants.

In phase two, all questions, assessments, and exercise prescription parameters/considerations that met agreement in phase one were presented, with AEPs asked to rate their level of agreement on a 9-point Likert scale ((1–3 = disagree; 4–6 = neither agree nor disagree; 7–9 = agree). Agreement was considered for each question if >70% of AEPs scored 7-9 (agree) [16]. Responses for phase two were collected over a four-week period (August to September 2022), with one follow-up email sent to those identified AEPs and/or AEP practices a fortnight following the original email. At the beginning of phase two, AEPs provided information regarding their years of experience as an AEP, and the percentage of their clientele that are cancer patients.

Statistical analysis

Responses for each question for rounds two, three, and four were collated to determine the level of agreement between AEPs, oncologists, and breast cancer surgeons (rounds two and three) and AEPs (round four). Agreement for each question across each round was considered if >70% of participants scored 7-9 (agree) on the Likert scale [16]. Results from each round were presented descriptively (percentage, median, interquartile range). To explore whether years of experience and cancer-specific clientele impacted the results, a Mann Whitney U test was performed on data collected in phase two to determine if there were any differences between AEPs with more or less than five years’ experience, and AEPs with more or less than 50% of their clientele as cancer patients.

A total of 29 AEPs, oncologists, and breast cancer surgeons were identified and approached to be involved in phase one. Seven AEPs, four oncologists (medical (n=3), radiation (n=1) and one breast cancer surgeon meeting the inclusion criteria responded and agreed to participate in phase one. The median years of experience working with patients with breast cancer across participants was 9.5 years (IQR = 6 years). Eleven participants completed round one (91.7%), nine of the eleven participants completed round two (81.2%), and all nine participants that completed round two completed round three (100%). Dropout occurred due to participants not responding to the survey questionnaire nor replying to email prompts. One AEP dropped out in round one, and a further two AEPs dropped out in round two. The median number of years of experience for those that completed phase one was 13 years (IQR = 8 years). In phase two, a total of 84 AEPs met the inclusion criteria and responded to the survey, with a median of 5 years (IQR = 6.25 years) experience, and a median of 20% (IQR = 40%) of their clientele being patients with cancer. Five participants were excluded from phase two for reporting no experience prescribing exercise to cancer populations.

Figure 1 summarises the progression through each phase of the study and the final number of questions that reached agreement between AEPs at the completion of phase two. At the completion of phase one, 51 questions reached agreement across the five domains between AEPs, oncologists, and breast cancer surgeons, with 50 of these 51 questions reaching agreement between AEPs in phase two (figure one). All questions rated by participants across phases one and two, including those that did not meet agreement, are detailed in supplementary digital content, tables 2-6.

Table 1 presents all questions, assessments, and exercise prescription parameters/considerations that reached agreement at the completion of phase two. The level of agreement achieved (%), and median and interquartile range for each question is presented.

Table. 1

Questions that reached agreement after phase two across all domains. Level of agreement (%) displayed in subscript. n = number of AEPs responding to each domain in phase two.

Questions that reached agreement (>70%)	Median (IQR)
Subjective (n = 84)
The stage, type, and specific location of a patient's cancer. ^{91.7% agreement}	9 (0)
The forms of treatment a patient has been/will be exposed to (i.e., surgery, radiation, chemotherapy). ^{97.6% agreement}	9 (0)
A patient's surgery type and outcomes (i.e., mastectomy vs breast conserving, axillary dissection etc.) ^{94.0% agreement}	9 (0)
A patient's fatigue levels (i.e., changes in fatigue in response to treatment, daily fluctuations). ^{97.6% agreement}	9 (0)
A patient's nausea levels (i.e., changes in nausea in response to treatment, daily fluctuations).^{95.2% agreement}	9 (2)
A patient's changes in cognition. ^{90.5% agreement}	9 (2)
A patient's dyspnoea experiences/symptoms. ^{95.2% agreement}	9 (1)
A patient's peripheral neuropathy symptoms. ^{95.2% agreement}	9 (1)
A patient's sleep quality since beginning treatment.^{86.9% agreement}	9 (2)
A patient’s weight changes since beginning treatment. ^{85.7% agreement}	9 (2)
Any metastases a patient may have, including their location. ^{92.9% agreement}	9 (0)
A patient's sites and severity of lymphedema. ^{95.9% agreement}	9 (0)
If a patient has a port or peripherally inserted central catheter (PICC). ^{89.3% agreement}	9 (0)
A patient's past medical history, including any co-morbidities and/or chronic health conditions. ^{96.4% agreement}	9 (0)
A patient's cardiometabolic risk profile, including any history of heart disease, high blood pressure or type 2 diabetes. ^{96.4% agreement}	9 (0)
The medications a patient is taking to manage any comorbidities/chronic health conditions. ^{96.4% agreement}	9 (1)
A patient's current mental health status. ^{95.2% agreement}	9 (1)
A patient's current pain experiences, including specific sites of pain. ^{95.2% agreement}	9 (1)
Any physical weaknesses or limitations a patient may have (i.e., weakness of specific muscles, limitations in functional ability or aerobic fitness). ^{95.2% agreement}	9 (1)
A patient's physical activity levels prior to breast cancer diagnosis. ^{88.1% agreement}	9 (2)
A patient's current physical activity levels since breast cancer diagnosis. ^{96.4% agreement}	9 (1)
A patient's physical activity/exercise preferences (i.e. likes and dislikes). ^{95.2% agreement}	9 (1)
A patient's motivators to exercise during and following their treatment (i.e., for health benefit, or due to oncologist recommendation etc.) ^{94.0% agreement}	9 (1)
A patient's short-term goals during their treatment. ^{95.2% agreement}	9 (1)
A patient's long-term goals after their treatment (once in remission). ^{91.7% agreement}	9 (1)
A patient's social and support networks (i.e., family, friends, access to facilities, travel arrangements). ^{85.7% agreement}	8 (1)
A patient's work/family commitments during their treatment. ^{83.3% agreement}	8 (2)
A patient's expectations after completing an exercise intervention. ^{90.5% agreement}	9 (1)
Objective (n = 80)
Resting blood pressure. ^85.0^{% agreement}	9 (2)
Resting heart rate. ^78.8^{% agreement}	8.5 (2)
Upper limb range of motion. ^85.0^{% agreement}	9 (2)
Upper limb strength (i.e. grip strength, bicep curl etc.) ^86.3^{% agreement}	9 (2)
Lower limb strength (i.e. sit to stand etc.) ^87.5^{% agreement}	8 (2)
Balance. ^81.3^{% agreement}	8 (2)
Aerobic capacity either directly (gas-analysis etc.) or in-directly (6-minute walk test, step test etc.) ^90.0^{% agreement}	8.5 (1)
Heart rate recovery from cardiovascular testing ^76.3^{% agreement}	8 (2)
Circumference measures of upper arm to measure risk of/changes in lymphedema. ^72.5^{% agreement}	8 (2.25)
Referral (n = 79)
The sites of patient metastases ^96.2^{% agreement}	9 (0)
Results from any scans performed (Echo, PET, CT, X-Ray, DEXA) ^84.8^{% agreement}	9 (2)
A patient's comorbidities/chronic health conditions ^98.7^{% agreement}	9 (0)
A patient's medications related to any comorbidities/chronic health conditions ^96.2^{% agreement}	9 (0.5)
General considerations (n = 72)
If a patient is unable to meet the FITT (frequency, intensity, time, type) principles proposed (i.e. the options you have selected above), the advice should be to reduce sedentary behaviour and avoid inactivity ^86.1^{% agreement}	9 (1)
Exercise guidelines should always be adapted to a patient's individual circumstance and/or capabilities ^97.2^{% agreement}	9 (0)
Exhaustive exercise (i.e. exercising to a state of exhaustion) should be avoided with breast cancer patients undergoing chemotherapy ^72.2^{% agreement}	9 (3)
If possible, resistance training should be included alongside aerobic exercise in breast cancer patients undergoing chemotherapy ^95.8^{% agreement}	9 (0)
Prescription Parameters (n = 72)
Most appropriate aerobic exercise modality.
The most appropriate aerobic exercise modality is any modality preferred by the patient, with cycling or walking most preferred cancer specialist AEPs, oncologists, and breast cancer surgeons. ^87.5^{% agreement}	8 (2)
Methods for prescribing aerobic exercise intensity.
Heart rate (HR) and ratings of perceived exertion (RPE) are appropriate to prescribe exercise intensity. ^91.7^{% agreement}	9 (1)
Most appropriate aerobic exercise intensity.
Agreement not met for most appropriate exercise intensity band.	nr
Individual circumstances may warrant low or vigorous aerobic exercise intensities. ^91.7^{% agreement}	9 (1)
Most appropriate aerobic exercise frequency.
3-5 sessions per week is the most suitable and/or appropriate aerobic exercise frequency for breast cancer patients undergoing chemotherapy. ^70.8^{% agreement}	7 (3)
Most appropriate aerobic exercise duration.
Agreement not met for most appropriate exercise duration range.	nr
Individual circumstances may warrant aerobic exercises sessions up to 60 minutes in duration. ^70.8^{% agreement}	8 (3)
Aerobic exercise duration (increments).
Breaking aerobic exercise into 5-to-9-minute bouts to reach a total of 20-to-30 minutes per day is appropriate if required. ^84.7^{% agreement}	9 (1)
Monitoring during aerobic exercise.
Heart rate (HR), ratings of perceived exertion (RPE), and oxygen saturation (SpO2) are appropriate to monitor exercise intensity. ^91.7^{% agreement}	9 (1)
Altering aerobic exercise intensity and/or duration based on chemotherapy schedule (n = 67)
The week prior to chemotherapy treatment: Either increase or maintain intensity and/or duration ^80.6^{% agreement}	8 (2)
The week of chemotherapy treatment: Either maintain or decrease intensity and/or duration ^71.6^{% agreement}	8 (2.5)
The week after chemotherapy treatment: Either decrease or maintain intensity and/or duration ^70.0^{% agreement}	7.0 (2)

* Median (IQR) represents the Likert ratings for each question from all experts. nr = not reported

Table 2 outlines the FITT principles from the three guidelines presented to cancer specialist AEPs, oncologists, and breast cancer surgeons in phase one, alongside the final recommendations agreed upon at completion of phase two. Similarities are observed for all elements of the FITT principle between exercise guidelines and participants interpretations (table 2).
Table. 2

Comparison between exercise guidelines for cancer survivors presented in phase 1 round 1, and the final recommendations for women with breast cancer undergoing chemotherapy at the completion of phase two.

*FITT Principle*	*Guideline 1 (ACSM 2013)*	*Guideline 2 (ACSM Consensus Roundtable 2019)*	*Guideline 3 (COSA 2019)*	*Findings upon completion of phase 2*
*Frequency*	3-5x per week.	2-3x per week.	3-5x per week.	3-5x per week
*Intensity*	Moderate to vigorous.	60-85% HRmax, 45-85% VO2max or 11-15 RPE.	Moderate to vigorous.	Agreement not met.
*Time*	75 minutes of vigorous or 150 minutes of moderate exercise per week.	20-60 minutes per exercise session.	75 minutes of vigorous or 150 minutes of moderate exercise per week.	Agreement not met.
*Type*	Walking or cycling.	Walking or cycling.	Walking, cycling, or swimming	Any modality preferred by patient. Walking or cycling most preferred.
*Notes/Other Recommendations*	Aligned with physical activity guidelines for general population.	n/a	Avoid inactivity. Progress towards achieving physical activity guidelines for general population (above). Exercise delivered by AEP or physiotherapist.	Breaking aerobic exercise into 5-to-9-minute bouts to reach a total of 20-to-30 minutes per day is appropriate if required. Avoid exercising to a state of exhaustion. Individual circumstances may warrant low or vigorous aerobic exercise intensities, and aerobic exercise durations of up to 60 minutes. Exercise intensity or duration should be altered based on a patient’s chemotherapy schedule in the following manner: 1) Week prior to chemotherapy infusion: Increase or maintain intensity or duration. 2) Week of chemotherapy infusion: Maintain or decrease intensity or duration. 3) Week after chemotherapy infusion: Decrease or maintain intensity or duration.

Figure 2 presents an infographic summary of the findings from each domain upon the completion of phase two.

To our knowledge, this is the first study to explore how a highly experienced interprofessional group of clinicians interpret, apply, and recommend exercise oncology guidelines when working with patients with breast cancer undergoing chemotherapy, and how well this is supported by a broader group of AEPs that have experience prescribing exercise to people with cancer. Results from this study provide insight into the specific questions and assessments AEPs, oncologists, and breast cancer surgeons consider necessary to discuss and perform with patients with breast cancer undergoing chemotherapy when prescribing exercise. Importantly, it also identifies how AEPs apply and adapt exercise guidelines to tailor exercise prescription for patients with breast cancer undergoing chemotherapy.

At the completion of phase two, 50 items met agreement across five domains (Table 1). It is recommended that AEPs consider these questions, assessments, prescriptions principles, and general considerations a when prescribing exercise to a patient with breast cancer undergoing chemotherapy. Only one question agreed upon in phase one did not meet agreement in phase two, demonstrating a high degree of agreement between professional groups. Whilst these findings provide useful guidance for AEPs and other professionals working with this cohort (due to the number and experience of AEPs involved in this study), not all individuals that present for exercise services will have the same needs or physical capacities. Therefore, AEPs must still clinically reason and individualise exercise assessments and prescriptions for this population – a key point agreed upon by participants throughout each phase of the present study. While oncologists and breast cancer surgeons are not trained in the specifics of exercise prescription, they do recommend exercise services and oversee treatment for this population. As such, their perspectives of exercise may raise important questions and/or concerns not always considered by AEPs. Their inclusion has ensured a wholistic, multidisciplinary approach to outcomes of this study, with the agreement observed between phases one and two suggesting their opinions are appropriate and relevant in clinical exercise settings.

When prescribing aerobic exercise, AEPs sampled in phase two agreed 3-to-5 exercise sessions per week of any aerobic exercise modality (i.e., walking, cycling, dancing, cross-trainer) preferred by a patient with breast cancer undergoing chemotherapy is suitable. AEPs did not agree on the most suitable aerobic exercise intensities or durations, but instead agreed that aerobic exercise intensity and duration should be dictated by individual capabilities. This highlights the importance of assessing previous exercise history and tolerance to exercise during an initial consultation, as it will have a notable impact on what exercise is suitable for a patient during chemotherapy. Whilst similarities exist between exercise prescription recommendations from this study and the most updated guidelines for cancer survivors, results identified further considerations for patients with breast cancer undergoing chemotherapy that are not discussed in the updated ESSA and ACSM guidelines [2, 7]. AEPs agreed exercising to a complete state of exhaustion should be avoided during chemotherapy to prevent significant post-exercise fatigue and/or a ‘crash’ when symptoms of fatigue are heightened. However, as mentioned above, AEPs agreed vigorous intensity exercise (70-90% HRmax) and exercise durations of up to 60 minutes may be appropriate for this population, especially in individuals with extensive exercise experience pre-diagnosis [18]. Results gathered regarding adjustments to intensity and duration of exercise based on a patient’s chemotherapy schedule (table 2) would suggest that if prescribed, vigorous intensity exercise and durations of up to 60 minutes may be most suitable in the week prior to each chemotherapy dose. Conversely, AEPs suggested that exercise intensity and duration should be decreased and/or maintained in the 7 days following chemotherapy infusion. A maintenance in intensity and duration is likely appropriate in the first 1-3 days post chemotherapy, as nausea and fatigue are often blunted due to the effect of steroid medication prescribed prior to infusion [19], with a decrease in intensity and duration appropriate 4-5 days post infusion, when fatigue typically peaks [20]. This may also be the timepoint in treatment when 5-to-9-minute bouts of exercise are implemented, which was agreed by AEPs as appropriate for patients who cannot achieve 20-to-30 minutes of exercise in one bout. AEPs agreed heart rate (HR) and ratings of perceived exertion (RPE) should be monitored during exercise. The measurement of RPE and HR will allow AEPs to understand how a patient feels during exercise, which will likely fluctuate throughout the chemotherapy cycle, whilst still monitoring physiological responses to exercise. These considerations agreed upon by AEPs at the completion of phase two provide useful insight into their approaches to exercise prescription for patients with breast cancer undergoing chemotherapy.

A non-cancer specific subjective assessment framework for individuals presenting for clinical exercise services has been previously developed through a Delphi consensus survey [12]. This survey identified 22 domains that AEPs believe should be covered to ensure all relevant subjective information is collected to base their clinical decisions on [12]. ESSA’s updated exercise guidelines for cancer survivors also outlined information that should be collected during patient assessment [2]. Many subjective questions reaching agreement in our study align with the domains identified in each of these papers, suggesting a level of agreement between AEPs across multiple studies. Bahl et al. [12] identified a patient’s ‘condition profile’ as one domain that should be discussed. Results from this work outline the key condition specific questions AEPs would discuss with a patient with breast cancer undergoing chemotherapy. These include the stage, type, and location a patient’s breast cancer diagnosis, the type of treatments performed to date (i.e., surgery, radio/chemotherapy) and those currently being undertaken/planned, outcomes of surgery, side effects experienced by the patient (i.e., fatigue, nausea, peripheral neuropathy, sleep quality, weight changes, lymphedema) and how these side-effects fluctuate at different periods of their treatment cycles, adding depth to the previous research findings for this specific population. AEPs also agreed that understanding a patient’s expectations of partaking in an exercise intervention during chemotherapy is important to obtain, as it can aid clinical decision making with respect to exercise prescription. Support networks, responsibilities and access to services was not a part of the subjective framework developed in the study by Bahl et al. [12]. However, AEPs in the present study agreed these factors should be discussed in a subjective assessment with a patient with breast cancer undergoing chemotherapy. Given the side-effects associated with breast cancer treatment, and the regular need to attend external facilities to receive treatment and undertake exercise, understanding a patient’s support networks and ability to access these services is particularly relevant.

In addition to subjective assessment, AEPs agreed upon relevant objective tests they would conduct to inform exercise prescription for patients with breast cancer undergoing chemotherapy. As certain types of chemotherapy can negatively affect heart function [21, 22], and breast cancer treatment can increase the risk of developing cardiovascular comorbidities [21, 23], assessments that can identify such risk including resting blood pressure and resting heart rate were considered relevant and practical by AEPs. Further assessments that could identify the risk of developing cardiovascular comorbidities, such as weight, body mass index, and waist circumference were not considered relevant to collect by AEPs in phase two, despite participants in phase one agreeing on the relevance of these measures. Given chemotherapy can cause unfavorable changes in body composition [24], such measures may still be relevant to monitor in patients at an increased risk of developing cardiovascular disease. AEPs agreed the measurement of upper arm circumference, to identify signs of swelling related to lymphedema should be performed. Although there is a discord in the literature regarding the risk of lymphedema following taxane-based chemotherapy [25, 26], such a measurement is useful given the other treatments typically performed in conjunction with chemotherapy for breast cancer (i.e., surgery). Such a measurement is practical and inexpensive, making it a feasible addition, and any change in upper arm circumference relating to lymphedema is information that can be relayed to the treating oncologist, supporting a multi-disciplinary approach to care. Additionally, AEPs recommended the assessment of upper arm range of motion and strength given the functional limitations that can occur following breast surgery. The assessment of full body strength and cardiorespiratory fitness are further measures AEPs would perform to monitor the effectiveness of their exercise intervention and any potential declines in function due to chemotherapy. These findings highlight the thorough objective assessment battery that should be considered by AEPs to ensure exercise prescription is tailored and effective for patients with breast cancer undergoing chemotherapy.

Strengths, limitations, and future research:

The active identification of experienced cancer specialist AEPs, oncologists, and breast cancer surgeons in phase one was a strength of this study. The difficulties in recruitment and limited sample size in phase one are a limitation. However, phase two validated these findings by seeking the opinion of a broad sample of AEPs with experience prescribing exercise to cancer patients. A key strength of this research is practical applicability. These findings can be immediately implemented by AEPs and medical professionals working with breast cancer patients. Moreover, as they were derived from, and validated by, experienced professionals working with this population, there is a high degree of confidence in the findings. Although oncologists and breast cancer surgeons are not trained in the specifics of exercise prescription and assessment, the high level of agreement seen between phase one and two suggests their opinions are appropriate and relevant in clinical exercise settings, with the wholistic, multidisciplinary approach viewed as a strength of this study. The difficulty in recruitment of experienced cancer specialist AEPs, oncologists, and breast cancer surgeons in phase one is an important consideration to note when planning future research in this field.

This study provides novel insight into approaches to exercise assessment and prescription in patients with breast cancer undergoing chemotherapy. Agreement between medical professionals and AEPs indicated that there are a number of factors’ medical professionals deem important to consider when prescribing exercise to patients with breast cancer undergoing chemotherapy that are not evident in existing guidelines. Breaking daily exercise goals into five-to-nine-minute bouts was seen to be useful and avoiding exercising to a complete state of exhaustion whilst undergoing chemotherapy was recommended. It was also agreed that exercise intensity and duration should be adjusted upon chemotherapy schedules to improve tolerance and adherence. These findings contribute to our understanding of the factors that experienced interprofessional clinicians and AEPs consider important when working with this population, which may be useful for novice AEPs and help inform future guidelines.

Funding:

J.M. is supported by an Australian Government Research Training Program Scholarship. The authors declare that no funds, grants, or other support were received during the preparation of this manuscript

Author contributions:

All authors were involved in the conceptualization of the study. James Murray carried out recruitment, data collection, analysis, and manuscript drafting. Hunter Bennett was involved in recruitment, analysis, and manuscript drafting. Rebecca Perry, Eva Bezak and Kade Davison were involved in recruitment and final manuscript drafting. All authors have read and approved the final version of the manuscript and agree with the order of presentation of the authors.

Competing interests:

The authors have no relevant financial or non-financial interests to disclose.

Data availability:

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Ethics approval:

The study was granted ethical approval by the University of South Australia Human Research Ethics Committee (Protocol Number 203189).

Consent to participate:

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

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: a cancer journal for clinicians. 2018;68(6):394-424.
Hayes SC, Newton RU, Spence RR, Galvão DA. The Exercise and Sports Science Australia position statement: Exercise medicine in cancer management. . J Sci Med Sport. 2019;22(11):1175-99.
Fuller JT, Hartland MC, Maloney LT, Davison K. Therapeutic effects of aerobic and resistance exercises for cancer survivors: a systematic review of meta-analyses of clinical trials. Brit J Sports Med. 2018;52(20):1311-.
Eakin EG, Youlden DR, Baade PD, Lawler SP, Reeves MM, Heyworth JS et al. Health behaviors of cancer survivors: data from an Australian population-based survey. Cancer Causes & Control. 2007;18(8):881-94.
Patterson R, McNamara E, Tainio M, de Sá TH, Smith AD, Sharp SJ et al. Sedentary behaviour and risk of all-cause, cardiovascular and cancer mortality, and incident type 2 diabetes: a systematic review and dose response meta-analysis. Eur J Epidemiology. 2018;33(9):811-29.
Spei M-E, Samoli E, Bravi F, La Vecchia C, Bamia C, Benetou V. Physical activity in breast cancer survivors: A systematic review and meta-analysis on overall and breast cancer survival. The Breast. 2019;44:144-52.
Campbell KL, Winters-Stone KM, Wiskemann J, May AM, Schwartz AL, Courneya KS et al. Exercise guidelines for cancer survivors: consensus statement from international multidisciplinary roundtable. Med & Sci Sports & Ex. 2019;51(11):2375-90.
Stout NL, Baima J, Swisher AK, Winters-Stone KM, Welsh J. A systematic review of exercise systematic reviews in the cancer literature (2005-2017). Contemporary Issues in Cancer Rehab. 2017;9(9):S347-S84.
Hayes SC, Spence RR, Galvão DA, Newton RU. Australian Association for Exercise and Sport Science position stand: optimising cancer outcomes through exercise. J Science Med Sport. 2009;12(4):428-34.
Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, Galvão DA, Pinto BM et al. American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. Med & Sci Sports & Ex. 2010;42(7):1409-26.
Cormie P, Atkinson M, Bucci L, Cust A, Eakin E, Hayes S et al. Clinical Oncology Society of Australia position statement on exercise in cancer care. Med J Aus. 2018;209(4):184-7.
Bahl JS, Dollman J, Davison K. The development of a subjective assessment framework for individuals presenting for clinical exercise services: A Delphi study. J Sci Med Sport. 2016;19(11):872-6.
McKenna L, Innes K, French J, Streitberg S, Gilmour C. Is history taking a dying skill? An exploration using a simulated learning environment. Nurs Ed Prac. 2011;11(4):234-8.
Hasson F, Keeney S, McKenna HJJoan. Research guidelines for the Delphi survey technique. J Adv Nurs. 2000;32(4):1008-15.
Okoli C, Pawlowski SD. The Delphi method as a research tool: an example, design considerations and applications. Information & Management. 2004;42(1):15-29.
Hinchliffe RJ, D'Abate F, Abraham P, Alimi Y, Beard J, Bender M et al. Diagnosis and management of iliac artery endofibrosis: results of a delphi consensus study. 2016;52(1):90-8.
Exercise and Sports Science Australia. ESSA Find an Accredited Exercise Professional Search. 2021. https://www.essa.org.au/find-aep/. Accessed 7th August 2022.
Ormel H, Van Der Schoot G, Sluiter W, Jalving M, Gietema J, Walenkamp A. Predictors of adherence to exercise interventions during and after cancer treatment: a systematic review. Psycho‐Oncology. 2018;27(3):713-24.
Ioannidis J, Hesketh PJ, Lau J. Contribution of dexamethasone to control of chemotherapy-induced nausea and vomiting: a meta-analysis of randomized evidence. J Clin Onc. 2000;18(19):3409-22.
El Mehdi Tazi HE. Evaluation and management of fatigue in oncology: A multidimensional approach. Indian J Palliative Care. 2011;17(2):92.
Gernaat S, Ho P, Rijnberg N, Emaus M, Baak L, Hartman M et al. Risk of death from cardiovascular disease following breast cancer: a systematic review. Breast cancer research and treatment. 2017;164(3):537-55.
Murray J, Bennett H, Bezak E, Perry R. The role of exercise in the prevention of cancer therapy-related cardiac dysfunction in breast cancer patients undergoing chemotherapy: systematic review. Eur J Prev Cardiol. 2021;29(3):463-72. doi:https://doi.org/10.1093/eurjpc/zwab006.
Edgington A. Looking beyond recurrence: comorbidities in cancer survivors. Clin J Onc Nurs. 2011;15(1):E3.
Freedman RJ, Aziz N, Albanes D, Hartman T, Danforth D, Hill S et al. Weight and body composition changes during and after adjuvant chemotherapy in women with breast cancer. Journal Clini Endocrin & Metab. 2004;89(5):2248-53.
Lee M-J, Beith J, Ward L, Kilbreath S. Lymphedema following taxane-based chemotherapy in women with early breast cancer. Lymphatic Research and Biology. 2014;12(4):282-8.
Swaroop MN, Ferguson CM, Horick NK, Skolny MN, Miller CL, Jammallo LS et al. Impact of adjuvant taxane-based chemotherapy on development of breast cancer-related lymphedema: results from a large prospective cohort. Breast Cancer Research and Treatment. 2015;151(2):393-403.

No competing interests reported.

SupplementaryDigitalContent.docx
Supplementary Digital Content: Supplementary Digital Content.

Download PDF

Version 1

posted

You are reading this latest preprint version

How do practitioners prescribe exercise to patients with breast cancer? Professional perspectives on the implementation of aerobic exercise guidelines for patients with breast cancer undergoing chemotherapy.

Status:

Version 1

Abstract

Figures

Introduction

Methods

Results

Discussion

Conclusion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1