Cardiac Rehabilitation Programs for Cancer Survivors: A Scoping Review

Abstract

Purpose of review:

Participation in cardiac rehabilitation is associated with improved quality of life and physical functioning and may be an effective strategy to assist in the recovery from cancer. We conducted a scoping review to identify studies that enrolled cancer survivors into cardiac rehabilitation programs.

Recent findings:

We identified nine studies that included 662 cancer survivors. Five studies integrated cancer survivors and cardiac patients into the same sessions, three studies developed cancer-only rehabilitation sessions, and one study did not report details on the rehabilitation sessions. On average, more than 60% of enrolled cancer survivors completed the rehabilitation programs and many health and psychosocial outcomes improved after rehabilitation.

Summary:

Cardiac rehabilitation appears to be acceptable and favorably impacts many health and psychosocial outcomes among cancer survivors. Future research should consider randomized controlled trial study designs, enrolling diverse survivor populations, and using a set of core physical function and psychosocial outcomes.

Introduction

Approximately 16.9 million Americans have a history of cancer, defined herein as cancer survivors, and this number is projected to increase to 22.1 million by 2030.[1] During the course of cancer treatment, many adults experience declines in cardiorespiratory fitness and may develop treatment-related side effects such as pain, fatigue, and emotional distress.[1, 2] Physical activity is beneficial for cancer survivors, and supervised exercise interventions among cancer survivors have documented improvements in cardiorespiratory fitness, fatigue, anxiety, depressive symptoms, physical functioning, and various domains of quality of life.[3-5] Additionally, observational findings suggest greater amounts of physical activity are associated with a lower risk of cancer recurrence, and all-cause and cancer-specific mortality.[6, 7] [8] Indeed, evidence-based guidelines recommend that cancer survivors should engage in physical activity to improve health outcomes related to cancer diagnosis and treatment.[3, 9]

Many cancer survivors are at an increased risk of cardiovascular disease (CVD)[10, 11] and have more CVD risk factors compared to those without a cancer history.[12] This elevated CVD risk may be due to cardiotoxic cancer treatments, accumulation of CVD risk factors, and loss of cardiorespiratory fitness due to cancer.[13] An effective strategy that lowers the risk of recurrent CVD is cardiac rehabilitation, which is a medically supervised program that includes aerobic and strength training, has educational sessions on healthy lifestyle behaviors, and provides behavioral and nutritional counseling.[14] Participation in cardiac rehabilitation is associated with increased cardiorespiratory fitness, improvements in quality of life and better physical functioning, and a lower risk of CVD recurrence and death.[15-17] Many of the components of cardiac rehabilitation could improve the health and well-being of cancer survivors. Recently, the American Heart Association (AHA) proposed a framework to refer cancer survivors at high risk of CVD to cardiac rehabilitation, and to refer those at lower risk to community-based programs.[13]

Cardiac rehabilitation may be an option to assist in recovery for cancer survivors who have a high risk of CVD or for survivors who have limited access to community-based programs, as cardiac rehabilitation may be more widely available. Given that cardiac rehabilitation has been successful at helping many adults return to daily life after a cardiac event, and has favorably impacted a number of outcomes relevant to cancer survivors, it could also improve the health and quality of life of cancer survivors. Therefore, we conducted a scoping review to identify studies that had enrolled cancer survivors into cardiac rehabilitation or had developed a cancer rehabilitation program based on the cardiac rehabilitation model. We summarized the acceptability of cardiac rehabilitation programs to cancer survivors and the impact of cardiac rehabilitation on health outcomes. Further, we identified knowledge gaps to provide directions for future research. Characterizing the scope of use of cardiac rehabilitation by cancer survivors can be informative for cardiac rehabilitation programs that already serve cancer survivors, for rehabilitation programs that plan to develop a program for cancer survivors, and for researchers who wish to investigate integrating cancer survivors into cardiac rehabilitation.

Methods

We conducted a scoping review and followed the steps outlined by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews (PRISMA-ScR).[18] We conducted a scoping review because it is well suited to summarize findings from heterogenous studies.[18, 19]

Data sources, search strategy, study selection

We searched four databases (PubMed, CINAHL, Scopus, and SPORTDiscus) on September 16, 2019 (search strategy in Appendix) for articles published prior to and inclusive of September 16, 2019. After removing duplicate citations, two authors (CC, EP, or KE) independently screened all titles and abstracts, and reviewed full-text articles using Covidence software. CC reviewed all articles and EP and KE each reviewed half of the articles. Discrepancies between pairs were resolved by consensus. Articles were included if they met the following inclusion criteria: 1) full text articles published in English-language peer reviewed journals; 2) the exercise program was described as occurring in an existing cardiac rehabilitation program or a new program was developed based on a cardiac rehabilitation model; 3) participants were adults; 4) participants were described as cancer patients, cancer survivors, or persons with a history of cancer; and 5) the study used an experimental or cohort study design.

Data abstraction

One author (CC) independently extracted data described below from included articles. Two authors (EP, KE) reviewed the extracted data and disagreements were resolved by consensus.

Study design and population characteristics

Study design characteristics that were abstracted included study aims, study design, dates of study, and geographic location. We also abstracted the following study population characteristics: gender, age, ethnicity, education, employment status, comorbidities, type of cancer, type of cancer treatment, and time since cancer diagnosis, surgery, or treatment.

Cardiac rehabilitation characteristics

We abstracted details about the cardiac rehabilitation programs. First, we determined if the program integrated cancer survivors into sessions with cardiac patients or if the program was developed exclusively for cancer survivors. We also abstracted information on session duration, frequency of sessions per week, length of the cardiac rehabilitation program, components of the programs (aerobic, strength, balance activities, educational sessions), and if the cardiac rehabilitation program was based on a behavioral theory. We additionally abstracted the number of participants that were eligible for the programs, the number of participants that enrolled, and the number who completed the programs. Findings on feedback about the cardiac rehabilitation programs from participants were also abstracted.

Study outcomes

We abstracted the types of outcomes measured, methods of measurement of each outcome, and the results from pre to post test.

Data analysis

We summarized the results descriptively to identify key characteristics across studies.

Results

Study selection

Our search identified 1181 articles; after removing duplicates, 778 articles remained to be screened (Figure 1). Of the screened articles, 737 were determined to be irrelevant. We conducted a full text review of the remaining 41 articles, and 31 were excluded due to the following reasons: the article described an intervention that was not conducted in a cardiac rehabilitation program or patterned on the cardiac rehabilitation model (n=26), or was not a full text article (n=5). This left 10 articles from 9 studies to be included in our final synthesis.

Figure 1.

Article selection process.

Study characteristics

Five of the nine studies integrated cancer survivors into cardiac rehabilitation programs,[20-25] three developed new programs patterned on a cardiac rehabilitation model,[26-28] and one study did not report if the program was a new or an existing program[29] (Table 1). In the five studies that used existing cardiac rehabilitation programs, the cancer survivors attended the same sessions as cardiac patients who were recovering from cardiac procedures and conditions. In the three studies that developed new programs, only cancer survivors were enrolled in the rehabilitation sessions but all sessions were held in rehabilitation facilities that used existing cardiac rehabilitation resources (equipment, staff).

Table 1.

Summary of study design and study population characteristics.

Author	Design	Country	Dates	Setting	Sample size	Cancer type	% Female	Average age at baseline (years)	Mean time since diagnosis/ therapy (SD or range)	Treatment status
Hubbard et al. 2016 [22, 25]	RCT	UK	NR	cancer/cardiac	41	100% colorectal	34%	66	NR	mixed
De Jesus et al. 2017 [21]	QE	Canada	NR	cancer/cardiac	20	100% breast	100%	53	10 months after surgery (3.9 months)	mixed
Dittus et al. 2015 [26]	QE	US	2012-2013	cancer only	280	68% breast, 2% prostate, 2% colorectal, 3% lung, 3% hematological, 22% other	86%	56	2.4 years after diagnosis (3.7 years)	mixed
Hubbard et al. 2018 [23]	QE	UK	NR	cancer/cardiac	20	100% breast	NR	57	NR	mixed
Rothe et al. 2018 [29]	QE	Canada	2014-2016	NR	30	100% hematologic	20%	56	6 weeks after autologous hematopoietic stem cell transplant	post treatment
Young-McCaughan et al. 2003 [28]	QE	US	NR	cancer only	62	22% breast, 19% prostate, 8% colorectal, 3% lung, 8% hematologic, 39% other	50%	59	24% in cancer treatment; 37% completed treatmentxs < 6 months, 39% completed treatment > 6 months	mixed
Bonsignore et al. 2018 [20]	RC	Canada	2004-2014	cancer/cardiac cancer	54; 27 survivors, 27 controls	100% prostate	0	74	NR	NR
Dolan et al. 2018 [27]	RC	Canada	2010-2014	cancer only	152	100% breast	100%	54	29.2 months after surgery (41.8 months)	post treatment
Morris et al. 2009 [24]	RC	US	2005-2006	cancer/cardiac	30	13% breast, 3% prostate, 47% lung, 3% hematologic, 17% head and neck, 10% esophagus, 3% pancreas, 3% other	33%	65	21.4 months after treatment completion (range 1 month to 11 years)	mixed

Abbreviations: NR=not reported, QE=quasi experimental, RC=retrospective cohort, RCT=randomized controlled trial, UK=United Kingdom, US=United States

Mixed treatment status indicates that cancer survivors had either completed treatment or were in active treatment.

More than half of the studies used a quasi-experimental pre post design with no control group (n=5)[21, 26, 23, 29, 28] and one used a randomized controlled trial design.[22, 25] Three used a retrospective cohort design;[20, 27, 24] one of the retrospective studies included a control group of cardiac participants that did not have cancer.[20] The studies occurred in the United States (n=3),[26, 24, 28] Canada (n=4),[20, 21, 27, 29] and the United Kingdom (n=2).[22, 25, 23] The date of data collection ranged from 2005 to 2016 and was reported by five of the nine studies. The sample size ranged from 20 [21, 23] to 280 participants.[26]

Study population characteristics

In total, 662 cancer survivors and 27 control participants without cancer were included in the nine studies reviewed (Table 1). Most of the participants (cancer survivors and control participants) were female (74%). The average age at baseline was approximately 55 years for six studies, and 65 and older for three studies.[22, 20, 24] The nine studies varied in the descriptive characteristics reported. Out of the nine studies, two studies reported race/ethnicity,[21, 28] one study reported employment status,[28] two reported educational attainment,[21, 28] and three reported information on comorbidities (obesity, hypertension, diabetes, prior myocardial infarction, stroke, and heart failure).[20, 24, 29]

All nine studies reported cancer type; the most common cancer types were breast (60%), prostate (7%), colorectal (8%), hematologic (7%), and lung cancer (3%). However, reporting of other cancer characteristics varied across studies. Of the nine studies, two reported participant’s cancer stage,[22, 28] and seven reported the types of treatment participants had received.[21, 26, 27, 22-24, 29, 28]

The timing of initiation of cardiac rehabilitation after cancer diagnosis was reported by six of the nine studies. Three of the nine studies reported an average time of two years or more since either diagnosis,[26] surgery,[27] or treatment completion.[24] Two of the nine studies reported an average of less than one year from either surgery[21] or treatment completion.[29] One study reported that 24% of participants were undergoing cancer treatment, 37% of participants had completed treatment within six months and 39% had completed treatment > 6 months.[28] Of the nine studies, two studies included survivors who had completed treatment,[29, 27] six included a mixture of survivors who had either completed treatment or were in active treatment[22, 21, 26, 23, 28, 24], and one study did not report treatment status.[20]

Rehabilitation program characteristics

All nine rehabilitation programs offered supervised aerobic training, five offered strength training,[20, 26, 27, 22, 29] and eight had educational sessions (Table 2). Most studies reported a total session length of one hour and the frequency of sessions varied from one to three times per week. The length of the nine programs varied from 6 [22] to 26 weeks.[20] The most frequently reported educational sessions offered were on nutrition (n=8),[20, 26, 27, 22-24, 29, 28] exercise (n=6),[20, 27, 22-24, 28] stress management (n=5),[26, 27, 22, 29, 28] and cardiovascular disease risk factor management (n=4).[27, 22, 23, 29] The three programs that were new and included only cancer survivors also offered educational sessions on cancer (n=2),[27, 28] cancer treatment-related side effects (n=3),[26-28] and quality of life (n=1).[28] Two studies reported that the programs were based on behavioral theory (Self Determination Theory and Roy Adaptation Model);[23, 28] the remaining 7 studies did not refer to a behavioral theory or intervention framework.

Table 2.

Cardiac rehabilitation program characteristics

Author	Design	Setting	Components			Exercise frequency			Completion
			aerobic	str	educ	Duration (min)	Frequency (sessions per week)	Length (weeks)	Number entered program	% completeda
Hubbard et al. 2016 [22, 25]	RCT	cancer/cardiac	X	X	X	site 1: 50 site 2: 55 site 3: 50	site 1: 1 site 2: 2 site 3: 2	site 1: 10 site 2: 12 site 3: 6	21b	62%
De Jesus et al. 2017 [21]	QE	cancer/cardiac	X			45	3	16	20	45%
Dittus et al. 2015 [26]	QE	cancer only	X	X	X	50	2	12	221c	74%
Hubbard et al. 2018 [23]	QE	cancer/cardiac	X		X	60	1	12	3d	67%
Rothe et al. 2018 [29]	QE	NR	X	X	X	NR	1	8	45	67%
Young-McCaughan et al. 2003 [28]	QE	cancer only	X		X	NR	2	12	62	74%
Bonsignore et al. 2018 [20]	RC	cancer/cardiac	X	X	X	60	1	26	27e	NA
Dolan et al. 2018 [27]	RC	cancer only	X	X	X	NR	1	22	152	NA
Morris et al. 2009 [24]	RC	cancer/cardiac	X		X	NR	2 to 3	8 to 12	30	NA

^aPercent that completed cardiac rehabilitation programs is the number of participants that finished the entire program out of the number that started the rehabilitation program.

^bout of 40 participants enrolled, 21 were randomized to attend cardiac rehabilitation

^cout of 280 participants that were evaluated, 221 started the rehabilitation program

^dout of 20 participants enrolled, 3 picked the cardiac rehabilitation option

^efor cancer participants only and does not include the control cardiac patients

Abbreviations: Educ=education, NR=not reported, QE=quasi-experimental, RC=retrospective cohort, RCT=randomized control trial, Str=strength, NA= 3 retrospective studies selected only patients that completed the cardiac rehabilitation program

Six of the nine studies reported the number of participants that completed the rehabilitation programs (Table 2). In five studies, over 60% of enrolled cancer survivors finished the cardiac rehabilitation program,[26, 22, 23, 29, 28] and in one study, 45% of participants completed the program.[21] Three retrospective cohort studies selected only participants who completed the cardiac rehabilitation programs. [27, 24, 20] Only two studies reported reasons why participants were not able to complete cardiac rehabilitation programs. In Rothe et al.[29], 15 participants were not able to complete cardiac rehabilitation due to geographic limitations and hematopoietic stem cell transplantation-specific symptoms, such as peripheral neuropathies and severe fatigue. Hubbard et al. [22] reported that eight out of 21 did not complete cardiac rehabilitation because of poor health, musculoskeletal issues, further surgery, uncontrolled hypertension, mental health issues, and chemotherapy side effects.

Feedback from participants

Four studies collected participant feedback on cardiac rehabilitation, either with focus group interviews [22, 23] or questionnaires[21], and one study did not report the method of data collection for gathering feedback[28]. Positive findings included that cardiac rehabilitation gave participants the motivation to be active, provided peer support, enhanced their return to normal activity, helped them to rebuild stamina and have more energy, and reduced feelings of depression.[22, 28] De Jesus et al.[21] administered a patient satisfaction survey. In this study, the highest scores were for statements of “The education materials I received were helpful to become more physically active” and “The supervised sessions and/or phone calls I received have helped me to become more active”.

Reported barriers to participating in cardiac rehabilitation programs included travel, difficulty recovering from surgery, and limited availability of cardiac rehabilitation sessions.[22, 23] Findings from De Jesus et al. [21] that administered a satisfaction survey reported that the lowest scores were for statements of “I would tell a friend to become a participant in a program like this” and “My time as a participant has been enjoyable”.

Hubbard et al. [22] interviewed cardiac rehabilitation staff about the integration of colorectal cancer survivors into a cardiac rehabilitation program. In this study, cancer survivors attended the same sessions as the cardiac patients. During the interviews, cardiac rehabilitation staff reported they were concerned that they lacked cancer-specific knowledge and were not able to meet the psychological needs of the cancer survivors. The staff also mentioned concerns about the capacity of the rehabilitation program to accommodate a larger volume of patients. The staff reported that they felt knowledgeable about prescribing appropriate exercises for everyone, regardless of if they had a cardiac or cancer diagnosis.

Quantitative outcome findings

There was wide variability in the outcomes measured; seven of the nine studies reported on changes over time for 22 different outcomes (Table 3). Two studies by Hubbard et al., the only RCT in this review,[22] and a quasi-experimental study[23], focused solely on feasibility results (adherence, qualitative findings) and did not present data on health or psychosocial outcomes from pre to post test.

Table 3.

Summary of types of outcomes measured.

				Cardiorespiratory fitness, physical function, and cardiovascular health							Anthropometrics & physical activity					Psychosocial				Other
	Design	Setting	Feasibility	CRF	Walk	Grip	Balance	Strength	Heart rate	BP	BMI	Body fat	Weight	Waist	PA	Fatigue	Depression	Anxiety	QOL	Safety	SB	Lym	Exertion	Dyspnea	Sleep
Hubbard et al. 2018 [22, 25]	RCT	C/C	X
De Jesus et al. [21]	QE	C/C		-								-	-		-	-	-	-	+		-
Dittus et al. 2015 [26]	QE	C			+			+								+	+	+
Hubbard et al. 2018 [23]	QE	C/C	X
Rothe et al. 2018 [29]	QE	NR			+	+	-													+
Young-	QE	C		+											-				+	+
McCaughan et al. 2003 [28]
Bonsignore et al. 2018 [20]	RC	C/C		+					+	-	-	-
Dolan et al. 2018 [27]	RC	C		+									+	+			+		+			+
Morris et al. 2009 [24]	RC	C/C			+															+			-	-
Number of studies that measured each outcome			2	4	3	1	1	1	1	1	1	2	2	1	2	2	3	2	3	3	1	1	1	1	1
% reported improvement			NA	75	100	100	0	100	100	0	0	0	50	100	0	50	67	50	100	100	0	100	0	0	0

Setting C/C=cancer/cardiac mixed, C=cancer only;

+ indicates improvement from pre to post test; − indicates no change from pre to post test

Abbreviations: BMI=body mass index, BP= blood pressure, CRF=cardiorespiratory fitness, Grip=grip strength, Lym=lymphedema, NR=not reported, PA=physical activity, QOL=quality of life, QE=quasi-experimental, RC=retrospective cohort, SB=symptom burden, RCT=randomized control trial, Waist=waist circumference,

Cardiorespiratory fitness, physical function, cardiovascular health

Participants generally had better cardiorespiratory fitness, walking ability, strength, and heart rate after participating in cardiac rehabilitation (Table 4). These findings were observed in studies that used quasi-experimental and retrospective cohort designs and in cancer/cardiac mixed and cancer only settings. In three of the four studies, estimated cardiorespiratory fitness improved pre to post test.[20, 27, 28] Three studies measured walking ability with a 6-minute walk test or a gait speed test; in all studies the distance walked and gait speed improved after participating in cardiac rehabilitation.[26, 24, 29] Grip strength and balance were measured by one study [29] and only grip strength improved over time. Strength was measured with chest and leg press in one study and improved pre to post test.[26] Only one study measured heart rate and blood pressure, and in this study, resting heart rate decreased over time and no changes were observed in resting systolic and diastolic blood pressure.[20]

Table 4.

Summary of findings from cardiac rehabilitation studies.

Author; Design	Cancer types	Follow up, weeks	N	Measurement method, units	Baseline Mean (SD)	Follow-up Mean (SD)	Change Mean	P-value	Direction pre-post
Cardiorespiratory fitness
De Jesus et al. 2017[21]; QE	Breast	16	17	Bruce protocol, VO2 peak mL/kg/min	20.2 (4.7)	20.8 (4.6)	+0.55	0.50	No change
Young-McCaughan et al. 2003 [28]; QE	Mixed	12	45	Bruce protocol, VO2 peak converted to METs	7.3 (2.1)	8.4 (2.1)	NR	0.001	Increased
Bonsignore et al. 2018 [20]; RC	Prostate	26	27 with cancer	Bruce protocol, VO2 peak mL/kg/min	16.9 (5.1)	19.6 (6.2)	+2.7	group difference p=0.71, within subject p= 0.001; between subject p= 0.98	Increased
			27 controls		16.4 (4.2)	20.2 (5.8)	+3.8		Increased
Dolan et al. 2018 [27]; RC	Breast	22	152	Bruce protocol, VO2peak mL/kg/min	20.96 (6.4)	23.94 (6.8)	+3.0 (95% CI 2.4, 3.5)	<0.001	Increased
Walk test/ gait speed
Dittus et al. 2015 [26]; QE	Mixed	12	142	6-minute walk test, meters	534 (171)	583 (157)	+8.3%	0.003	Increased
Rothe et al. 2018 [29]; QE	Hem	14	30	6-minute walk test, meters	484 (95)	532 (98)	NR	< 0.001	Increased
Morris et al. 2009 [24]; RC	Mixed	8 to 12	30	6-minute walk test, meters	360 (126)	437 (122)	+77.1	< 0.001	Increased
Rothe et al. 2018 [29]; QE	Hem	14	30	gait speed, meters/second	1.35 (0.22)	1.47 (0.22)	NR	< 0.05	Increased
Grip strength
Rothe et al. 2018 [29]; QE	Hem	14	30	left grip strength, kg	38 (13)	40 (12)	NR	NR	Increased
Rothe et al. 2018 [29]; QE	Hem	14	30	right grip strength, kg	39 (13)	42 (13)	NR	<0.01	Increased
Balance
Rothe et al. 2018 [29]; QE	Hem	14	30	timed-up-and-go, seconds	6.6 (2.2)	6.5 (2.2)	NR	NR	No change
Strength
Dittus et al. 2015 [26]; QE	Mixed	12	142	chest press, 1 repetition maximum, pounds	63.7 (41.2)	81.3 (44.2)	+21.6%	< 0.0001	Increased
Dittus et al. 2015 [26]; QE	Mixed	12	130	leg press, 1 repetition maximum, pounds	115.7 (40.7)	147.4 (39.9)	+21.5%	< 0.0001	Increased
Cardiovascular health
Bonsignore et al. 2018 [20]; RC	Prostate	26	27 with cancer	resting heart rate, beats per minute	70.7 (15.1)	64.7 (10.5)	−6	group difference p=0.41, within subject p= 0.002; between subject p= 0.55	Decreased
			27 controls	(bpm)	67.6 (13.2)	64.1 (12.3)	−3.5
Bonsignore et al. 2018 [20]; RC	Prostate	26	27 with cancer	resting systolic blood pressure, mmHg	126.9(18.8)	125.7(12.7)	−1.2	group difference p=0.22, within subject p=0.56; between subject p=0.10	No change
		27 controls		133.7 (18.5)	132.5 (17)	−1.2
Bonsignore et al. 2018 [20]; RC	Prostate	26	27 with cancer	resting diastolic blood pressure, mmHg	73.1 (7.5)	72.7 (7.5)	−0.4	group difference p=0.64, within subject p=0.12; between subject p=0.99	No change
			27 controls		74.2 (10.2)	71.0 (9.9)	−3.2
Anthropometries
Bonsignore et al. 2018 [20]; RC	Prostate	26	27 with cancer	BMI, kg/m2	27.7 (5.3)	27.7 (5.2)	0	group difference p=0.68, within subject p= 0.51; between subject p=0.67	No change
		27 controls		27.9 (3.5)	28.0 (3.3)	+0.1
De Jesus et al. 2017 [21]; QE	Breast	16	17	Body fat, dual X-ray absorptiometry, %	45.8 (5.3)	46.8 (6.9)	+1.0		No change
Bonsignore et al. 2018 [20]; RC	Prostate	26	27 with cancer	Body fat, %	29.2 (8.6)	28.7 (8.4)	−0.5	group difference p=0.93, within subject p=0.41; between subject p=0.72	No change
			27 controls		28.9 (8.8)	30.9 (10.5)	+2.0
De Jesus et al. 2017 [21]; QE	Breast	16	17	weight, kg	84.3 (15.0)	85.9 (15.9)	+1.6	0.31	No change
Dolan et al. 2018 [27]; RC	Breast	22	152	weight, kg	72.7 (17.7)	72.1 (17.3)	−0.6 (94% CI −0.1, −1.1)	0.031	Decreased
Dolan et al. 2018 [27]; RC	Breast	22	151	waist circumference, cm	88.5 (14.1)	86.4 (131.4)	−2.2 (91% CI −1.3, −3.0)	<0.001	Decreased
Physical Activity
De Jesus et al. 2017 [21]; QE	Breast	16	17	Actical, moderate-to-vigorous physical activity, hours	2.5 (7.4)	0.5 (1.0)	−2.0	0.35	No change
Young-McCaughan et al. 2003 [28]; QE	Mixed	12	31	Motionlogger Actigraph, counts per minute	199.3(24.7)	197.3(30.9)	NR	0.10	No change
Fatigue
De Jesus et al. 2017 [21]; QE	Breast	16	17	Piper Fatigue Scale	5.4 (2.6)	4.6 (2.3)	−0.73	0.09	No change
				Edmonton Fatigue Scale	4.8 (3.2)	3.6 (2.7)	−1.2	0.09	No change
Dittus et al. 2015 [26]; QE	Mixed	12	141	Fatigue Symptom Inventory	15.7 (12.2)	10.0 (11.8)	+36.3%	<0.0001	Decreased
Depression
De Jesus et al. 2017 [21]; QE	Breast	16	17	Edmonton Symptom Assessment System	2.8 (3.4)	1.9 (2.7)	−0.96	0.06	No change
Dittus et al. 2015 [26]; QE	Mixed	12	152	Patient Health Questionnaire-9	5.3 (4.0)	3.7 (3.5)	+25.1%	<0.0001	Decreased
Dolan et al. 2018 [27]; RC	Breast	22	130	Center for Epidemiologic Studies Depression Scale (CES-D)	13.3 (9.4)	11.8 (8.7)	−1.5 (95% CI −0.2, −2.7)	0.019	Decreased
Anxiety
De Jesus et al. 2017 [21]; QE	Breast	16	17	Edmonton Symptom Assessment System	3.0 (3.5)	2.7 (3.1)	−0.3	0.45	No change
Dittus et al. 2015 [26]; QE	Mixed	12	154	Generalized Anxiety Disorder-7	2.9 (3.5)	2.3 (3.2)	+18.5%	0.042	Decreased
Quality of life
De Jesus et al. 2017 [21]; QE	Breast	16	17	Functional Assessment of Cancer Therapy-Breast (FACT-B)	72.8 (18.3)	77.6 (17.4)	+4.8	0.02	Increased
Young-McCaughan et al. 2003 [28]; QE	Mixed	12	42	Cancer Rehabilitation Evaluation System Short Form (CARES-SF)	46.8 (8.6)	44.3 (10.1)	NR	0.03	Increased
Dolan et al. 2018 [27]; RC	Breast	22	83	Functional Assessment Of Cancer Therapy – Breast (FACT-B)	101.5(23.9)	110.6(20.0)	+9.0 (95%CI 5, 13.1)	<0.001	Increased
Dolan et al. 2018 [27];RC			ranged from 80-85	Short Form-36 Health Status (SF-36), 8 scale domains	pre scores ranges from 40 to76	post scores ranged from 58 to 83	all domains improved from pre to post except for bodily pain	bodily pain p=0.311; other 7 domains p ranged from < 0.001 to 0.020	Increased

Abbreviations: BMI=body mass index, cm=centimeters, Hem=hematological, kg=kilogram, METs=metabolic equivalent of task, NR=not reported Rothe et al. measured outcomes at three time points – before stem cell transplant, 6 weeks after transplant which was pre-cardiac rehabilitation, and at post-cardiac rehabilitation. Data presented in table is from pre and post cardiac rehabilitation and p-values are reported pairwise comparisons between pre and post cardiac rehabilitation time points.

CARES-SF QOL – lower scores indicate better QOL

Anthropometrics and physical activity

Few changes were observed in body composition after participation in cardiac rehabilitation in both quasi-experimental and retrospective cohort studies. Body composition measures were measured in three studies; one study measured body mass index (BMI),[20] two measured body fat,[20, 21] two measured weight,[21, 27] and one measured waist circumference.[27] No changes were observed for BMI and body fat.[20, 21] In one study, weight and waist circumference minimally decreased.[27]

Physical activity was measured by accelerometry in two quasi-experimental studies. De Jesus et al. [21] asked participants to wear a hip-worn Actical accelerometer for 7 days during waking hours at baseline and 16 weeks later and found no significant differences over the time period in light or moderate-to-vigorous intensity activity. Young-McCaughan et al. [28] asked participants to wear the wrist-worn Motionlogger Actigraph for a consecutive 48-hour period at baseline and 12 weeks later. Average counts per minute, an indicator of total volume of physical activity, did not significantly change over time.

Psychosocial outcomes

Almost half of the nine studies (n=4, 44%) collected psychosocial outcomes and, for the most part, participants had improved depression and quality of life after participation in cardiac rehabilitation; however, the results were mixed for fatigue and anxiety. Fatigue was measured in two studies; Dittus et al. [26] used the Fatigue Symptom Inventory and participants reported less fatigue by the end of cardiac rehabilitation. De Jesus et al. [21] measured fatigue with two different questionnaires and with both instruments observed no changes in fatigue over time. Depression was measured by three studies [21, 26, 27] with three different instruments (Edmonton Symptom Assessment System, Patient Health Questionnaire, and Center for Epidemiologic Studies Depression Scale (CES-D)), and in two studies participants reported less depression after the end of cardiac rehabilitation.[26, 27] Anxiety was measured by two studies [21, 26] with two different instruments (Edmonton Symptom Assessment System and Generalized Anxiety Disorder), and in one study participants had less anxiety by the end of cardiac rehabilitation.[26] Three studies measured quality of life; two studies used the Functional Assessment of Cancer Therapy-Breast (FACT-B) instrument,[21, 27] Dolan et al. [27] additionally used the Short Form-36 Health Status (SF-36), and Young-McCaughan et al. [28] used a Cancer Rehabilitation Evaluation Short Form (CARES-SF). In all three studies, participants reported better quality of life post-intervention.

Three of the four studies that included psychosocial outcomes were set in a cancer-only setting and these studies reported improvements for all psychosocial outcomes.[26, 28, 27] The other study, De Jesus et al., [21] was set in a mixed cancer/cardiac setting and reported improvements for quality of life but no changes for fatigue, depression, and anxiety. Improvements in psychosocial outcomes were observed in both quasi-experimental and retrospective cohort studies.

Safety

Safety was reported in three studies, and in these studies no adverse events, deaths, injuries, or cardiovascular disease complications occurred.[24, 29, 28]

Other outcomes

Other outcomes measured by one study each were symptom burden,[21] lymphedema,[27] perceived exertion,[24] dyspnea,[24] and sleep duration.[28] For all these outcomes, no changes were observed from pre to post test.

Discussion

In this scoping review, we identified nine studies that enrolled 662 cancer survivors into cardiac rehabilitation programs. More than half of the studies integrated cancer survivors into cardiac rehabilitation programs with cardiac patients, three studies developed rehabilitation programs exclusive to cancer survivors, and one study did not report details on if the rehabilitation program was integrated with cardiac patients or was for only cancer survivors. Many of the core components of cardiac rehabilitation were included across studies: supervised exercise sessions, strength training, and educational sessions on health behaviors. A high proportion of survivors completed the rehabilitation programs. Few of the studies sought feedback from participants or staff involved in the programs, and the sparse data available suggests mixed findings for participant and provider satisfaction. Although the programs were similar, a wide variety of outcomes were measured. A number of physical function and psychosocial outcomes improved with participation in cardiac rehabilitation and programs that measured safety found the programs were safe.

On average, a high proportion of survivors completed the cardiac rehabilitation programs, which suggests that cardiac rehabilitation was acceptable to many participants. Additionally, many participants reported a positive view of the cardiac rehabilitation programs during focus group interviews. However, participants reported concerns such as travel, difficulty recovering from surgery, and inconvenient program hours. Some of these issues could be addressed by cardiac rehabilitation programs with approaches such as delaying the time after surgery when participants start rehabilitation and offering flexible hours for sessions. Staff mentioned concerns about lack of cancer knowledge. Cardiac rehabilitation programs that admit cancer survivors may need to consider further staff training on cancer-related topics. The AHA statement on identifying high risk cancer survivors for cardiac rehabilitation[13] describes cancer-specific topics that may need to be considered when working with patients with cancer in the cardiac rehabilitation setting, such as developing exercise prescriptions with special considerations for treatment-related symptoms and comorbidities and developing a referral network of mental health professionals who work with cancer survivors. Additionally, the American College of Sports Medicine (ACSM) offers professional certification to exercise professionals who work with cancer survivors (ACSM/American Cancer Society Cancer Exercise Trainer Certification).[30, 31]

A wide variety of outcomes and methods of measurement were used in the reviewed studies. Cardiorespiratory fitness, walking ability, depression, and quality of life were each measured by more than one study and these outcomes, for the most part, improved after rehabilitation. These findings are consistent with supervised exercise interventions with cancer survivors that have found strong evidence for improving cardiorespiratory fitness, anxiety, depressive symptoms, fatigue, quality of life, lymphedema, and physical function.[5, 3] Many of the supervised exercise interventions with cancer survivors have been similar in design to cardiac rehabilitation – both tended to have aerobic and resistance training, a session length that ranged from 30 to 60 minutes, the frequency of sessions ranged from one to three times per week, and an intervention length of 12 weeks. Additionally, evaluations with the LIVESTRONG program at the YMCA, a 12-week supervised aerobic training program for cancer survivors which is similar to cardiac rehabilitation, have also observed improvements in many of the same outcomes used in the cardiac rehabilitation studies (i.e., physical activity, walking ability, and quality of life).[32] In our review, the findings were mixed for fatigue and anxiety; however, the study in which no improvements were observed had enrolled fatigued breast cancer patients. In this study, the participant’s fatigue may have affected their energy and motivation levels to participate in cardiac rehabilitation.[21] Other improvements were observed for strength, resting heart rate, and grip strength, and exercise appeared to be safe for participants at risk of breast cancer-related lymphedema. However, it should be noted that each of these outcomes were measured by only one study each. For the outcomes measured by more than two studies (cardiorespiratory fitness, walk ability, depression, quality of life) similar findings were observed in both quasi-experimental and retrospective cohort studies. Almost all the psychosocial outcomes were collected by studies that had rehabilitation programs exclusive to cancer survivors which limits our ability to determine if these types of outcomes can improve in the cancer/cardiac integrated settings.

Two models of care were used in the included studies, cancer survivors either attended the same sessions as cardiac participants or attended sessions that included only cancer survivors. Although fewer studies developed rehabilitation programs exclusive to cancer survivors, these studies had much larger sample sizes than the integrated rehabilitation studies. In fact, 75% of the included participants were from rehabilitation programs that had only cancer survivors. Due to the small number of studies and the high proportion of participants that attended cancer exclusive rehabilitation programs, it is difficult to determine if one type of setting was more acceptable or yielded better outcomes than the other. Qualitative findings suggest further research is needed to understand the best way to integrate cancer survivors into cardiac rehabilitation programs. De Jesus et al. [21] integrated cancer survivors into an existing cardiac rehabilitation program and the authors hypothesized that the cancer survivors may not have socially identified with the larger group of cardiac patients because they did not have a cardiac condition. In contrast, Hubbard et al. [22] integrated colorectal cancer survivors into an existing cardiac rehabilitation program. The authors reported that none of the participants had problems with both cancer and cardiac patients attending the same sessions. In fact, the cancer survivors reported gaining social support from the group sessions.

Implications and directions for future research

Although cancer survivors using a cancer/cardiac integrated rehabilitation or a cancer only rehabilitation program improved in several health outcomes, there are many limitations to this body of research to consider. Most studies used pre-post quasi-experimental designs and did not include a control group. Without control groups for comparison, it is unclear if cancer survivors improved over time due to the intervention or if they would naturally improve without the intervention. The only randomized controlled trial was conducted by Hubbard et al. [22] who did include a control group of cancer survivors who received a booklet on colorectal cancer instead of attending cardiac rehabilitation. In this study, the authors reported on feasibility outcomes and not about changes in outcomes over time. Bonsignore et al. [20] used a retrospective design and included a control group of cardiac patients that did not have cancer. In this study, both participants with prostate cancer and those without cancer improved in heart rate and cardiorespiratory fitness after participating in cardiac rehabilitation. Future research on integrating participants with cancer into cardiac rehabilitation should consider using randomized controlled trial study designs that have a control group.

The population of cancer survivors represented by the included studies may be younger and healthier than the current United States survivor population. Older cancer survivors were less well represented in this review, as only three of the nine studies had an average age of 65 years. Cancer survivors 65 and older account for 64% of the national survivor population[1] and projections suggest that they will account for 73% of the survivor population by 2040.[33] Additionally, cancer survivors are estimated by one population-based study to have an average of five comorbid conditions.[34] Another report suggests the most common types of comorbidities among cancer survivors are heart failure, chronic obstructive pulmonary disease, and diabetes.[33] Many of these conditions are common among cardiac rehabilitation patients and participation in cardiac rehabilitation has been associated with a number of improved outcomes even among participants who have these conditions.[35-37] The studies included a majority of breast cancer survivors (60%). While other common types of cancers among survivors were represented (prostate, colorectal), participants with other common types of cancers were less well represented (thyroid, uterine, bladder).[1] Additionally, almost none of the studies reported on race/ethnicity of participants. Future research should consider enrolling diverse populations of survivors based on cancer type, age, race/ethnicity, and comorbidity burden to improve the generalizability of findings and to examine if outcomes and acceptability vary by these types of population characteristics.

Other limitations were small sample sizes and limited overlap in outcomes measured across studies. Future research should consider a set of outcomes such as cardiorespiratory fitness, walk speed/gait, strength, physical activity, cardiovascular health (heart rate and blood pressure) and psychosocial outcomes. These outcomes are related to the goals of cardiac rehabilitation and relevant to cancer survivors – to recover physical function, to improve psychosocial well-being, and to lower the risk of cardiovascular disease. For psychosocial outcomes, comparisons across studies could be improved by using the same questionnaires. The FACT questionnaires have been validated in mixed cancer populations and the SF-36 and CES-D are widely used measures of health status and depression.[38, 39] In this review, qualitative data highlighted issues with integrating cancer survivors into cardiac rehabilitation programs but less than half of the studies used these methods; future research should consider mixed-methods to better understand the implementation and evaluation of cardiac rehabilitation programs among cancer survivors. Long term outcomes that should eventually be considered are risk of cancer recurrence, development of new cancers, CVD, and mortality.

Conclusions

In this scoping review of nine studies, 662 cancer survivors participated in cardiac rehabilitation or in a program modeled on cardiac rehabilitation. Feedback from participants and staff suggested further research was needed to understand the best way to integrate cancer survivors into cardiac rehabilitation. Participation in cardiac rehabilitation was associated with improvements in many health-related and psychosocial health outcomes. Future research should consider randomized controlled trial study designs, enrolling diverse survivor populations according to age, race/ethnicity, type of cancer, and comorbidity burden, and using a set of core physical function and psychosocial outcomes. The results from this review can be used to improve research on implementing and evaluating cardiac rehabilitation to help cancer survivors improve health and quality of life. Further, these results may be informative for cardiac rehabilitation programs that already serve cancer survivors or for rehabilitation programs that plan to develop a program for cancer survivors.

Appendix

PubMed search

("cancer survivors"[MeSH Terms]) OR ((neoplasms[Mesh] OR neoplasms[tiab] OR cancer[tiab]) AND (survivor[tiab] OR survivors[tiab] OR patient[tiab] OR patients[tiab] OR persons[tiab]))

AND ("exercise therapy"[MeSH Terms] OR Exercise therapy[tiab] OR physical activity[tiab] OR exercise[tiab] OR physical fitness[tiab] OR LIVESTRONG[tiab])

AND (Community-based[tiab] OR community[tiab] OR YMCA[tiab] OR "cardiac rehabilitation"[MeSH Terms] OR cardiac rehabilitation[tiab] OR cardiovascular rehabilitation[tiab] OR coronary rehabilitation[tiab] OR heart rehabilitation[tiab] OR cardio-oncology[tiab] OR cardiooncology[tiab] or oncology rehabilitation[tiab])

CINAHL search

(MH "Cancer Survivors") OR (MH "Cancer Patients") OR ((neoplasm* OR cancer*) N3 (survivor OR survivors OR patient OR patients OR persons)) OR (AB((neoplasm OR cancer) AND (survivor OR survivors OR patient OR patients OR persons))) OR (TI((neoplasm OR cancer) AND (survivor OR survivors OR patient OR patients OR persons)))

AND (MH exercise or physical activity) OR (AB(exercise therapy OR physical activity OR exercise OR physical fitness OR LIVESTRONG)) OR (TI(exercise therapy OR physical activity OR exercise OR physical fitness OR LIVESTRONG))

AND (AB(community based programs OR community based rehabilitation OR community OR community-based OR YMCA OR cardiac rehabilitation OR cardiac rehab OR cardiovascular rehabilitation OR cardiac rehabilitation program OR oncology rehabilitation OR cardio-oncology)) OR (TI(community based programs OR community based rehabilitation OR community OR community-based OR YMCA OR cardiac rehabilitation OR cardiac rehab OR cardiovascular rehabilitation OR cardiac rehabilitation program OR oncology rehabilitation OR cardio-oncology))

Scopus search

TITLE-ABS-KEY

((cancer OR oncology OR neoplasm) AND (survivor OR survivors OR survivorship OR patient OR patients OR persons))

AND (exercise OR “exercise therapy” OR “physical activity” OR “physical fitness” OR LIVESTRONG)

AND ("community based" OR "community-based" OR ymca OR "cardiac rehabilitation" OR "oncology rehabilitation" OR "cardio-oncology" OR "community care" OR "community health services" OR “community program”)

SPORTDiscus search

(DE "CANCER patients" OR ((neoplasm* OR cancer*) N3 (survivor OR survivors OR patient OR patients OR persons)) OR (AB((neoplasm OR cancer) AND (survivor OR survivors OR patient OR patients OR persons))) OR (TI((neoplasm OR cancer) AND (survivor OR survivors OR patient OR patients OR persons)) OR (TI(cancer)) OR (SU((CANCER diagnosis”))

AND ((DE "PHYSICAL activity") OR (AB(exercise therapy OR physical activity OR exercise OR physical fitness OR LIVESTRONG)) OR (TI(exercise therapy OR physical activity OR exercise OR physical fitness OR LIVESTRONG)) OR SU(“EXERCISE therapy” OR “EXERCISE”))

AND ((AB(community based programs OR community based rehabilitation OR community OR community-based OR YMCA OR cardiac rehabilitation OR cardiac rehab OR cardiovascular rehabilitation OR cardiac rehabilitation program OR oncology rehabilitation OR cardio-oncology)) OR (TI(community based programs OR community based rehabilitation OR community OR community-based OR YMCA OR cardiac rehabilitation OR cardiac rehab OR cardiovascular rehabilitation OR cardiac rehabilitation program OR oncology rehabilitation OR cardio-oncology)) OR (SU(“CARDIAC rehabilitation”))