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Attention to the principles of exercise training in exercise studies on prostate cancer survivors: a… Neil-Sztramko, Sarah E; Medysky, Mary E; Campbell, Kristin L; Bland, Kelcey A; Winters-Stone, Kerri M Apr 5, 2019

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RESEARCH ARTICLE Open AccessAttention to the principles of exercisetraining in exercise studies on prostatecancer survivors: a systematic reviewSarah E. Neil-Sztramko1* , Mary E. Medysky2, Kristin L. Campbell3, Kelcey A. Bland4 and Kerri M. Winters-Stone2,5AbstractBackground: The purpose of this review is to update previously published reviews on exercise programming inexercise trials in prostate cancer survivors. We evaluated: 1) the application of the principles of exercise training inprescribed programs; 2) the reporting of the components of the exercise prescription; and 3) the reporting ofadherence of participants to the prescribed programs.Methods: Building upon a previous review, a systematic review was conducted searching OVID Medline, Embase,CINAHL, and SPORTDiscus databases from 2012-2017. Randomized controlled trials of at least four weeks of aerobicand/or resistance exercise in men diagnosed with prostate cancer that reported physical fitness outcomes,including body composition were eligible for inclusion.Results: Specificity was appropriately applied by 93%, progression by 55%, overload by 48%, initial values by 55%,and diminishing returns by 28% of eligible studies. No study adequately applied the principle of reversibility. Most(79%) studies reported all components of the exercise prescription in the study methods, but no study reported allcomponents of adherence to the prescribed intervention in the study results.Conclusions: Application of standard exercise training principles is inadequate in exercise trials in men withprostate cancer and could possibly lead to an inadequate exercise stimulus. While many studies report the basiccomponents of the exercise prescription in their study methods, full reporting of actual exercise completed isneeded to advance our understanding of the optimal exercise dose for men with prostate cancer and promotetranslation of controlled trials to practice.Keywords: Prostate cancer, Exercise, Systematic review, Exercise prescriptionBackgroundProstate cancer is the most commonly diagnosed cancerin men in developed countries, such as Canada, and isone of the most treatable cancers, with five-year survivalrates of 95% [1]. Depending on the stage of disease,treatment options can range from active surveillance toradical prostatectomy, radiation therapy, androgendeprivation therapy, and sometimes chemotherapy [2].These treatments can have a number of deleterious ef-fects on other health outcomes such as reduced bonemineral density, physical function, and quality of life,along with altered body composition (i.e., gain in fatmass and reduction in lean mass) [3, 4]. These adversehealth outcomes are a direct result of cancer and treat-ment but may also indirectly result from a decline inphysical activity that can occur during treatment [5].Previous systematic reviews have summarized theexisting evidence for the role of exercise in improvingphysical fitness (i.e., strength and aerobic fitness), fatigueand lean body mass [4, 6], with resistance trainingappearing to be particularly beneficial in counteractingadverse changes in body composition [7]. Observationalstudies have also suggested an important role for phys-ical activity in reducing mortality after a prostate cancerdiagnosis [8]. Despite this evidence, there remains uncer-tainty around the most efficacious exercise prescriptions© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.* Correspondence: neilszts@mcmaster.ca1School of Nursing, McMaster University, 175 Longwood Road S, Suite 210a,Hamilton, ON L8P 0A1, CanadaFull list of author information is available at the end of the articleNeil-Sztramko et al. BMC Cancer          (2019) 19:321 https://doi.org/10.1186/s12885-019-5520-9for improving specific outcomes across this heteroge-neous population. This knowledge gap limits the transla-tion of prescriptions from tightly controlled efficacystudies in a research setting to practice in the broaderpopulation of prostate cancer survivors who likely varyin their exercise capacity and may exercise in less super-vised settings.In 2012 and 2014, our team published a pair of sys-tematic reviews to evaluate the application of the stand-ard principles of exercise training and to summarizereporting of and adherence to an exercise prescription instudies of breast cancer survivors [9] and in survivors ofcancers other than breast [10]. These reviews wereprompted by our observation that well-established exer-cise training principles from the field of exercise physi-ology (Table 1 [11]) were either not considered in thedesign of exercise oncology trials, or were misapplied. Inour reviews, and in a recently published update ofour first breast cancer review [12], across 113 trials,none applied all of the principles of exercise trainingand only two [13, 14] reported all of the componentsof the exercise prescription in their methods andresults.Since the publication of the 2014 review of adults withcancer other than breast, a large number of randomizedcontrolled trials (RCTs) in prostate cancer survivors havebeen published, meaning findings from our last reviewmay now be out of date. Treatments for prostate cancer,such as androgen deprivation therapy, are accompaniedby unique side effects, and strong potential for exerciseto mitigate these effects. Given that the high survivalrate for prostate cancer results in a large population oflong term cancer survivors, and the larger number ofnew trials in men with prostate cancer, a separate reviewfocused exclusively on exercise in prostate cancer survi-vors could best inform the research field and clinicalpractice. The purpose of this review is to summarize thepublished literature on exercise studies conducted inmen diagnosed with prostate cancer, with a particularlyfocus on evaluating 1) the principles of exercise trainingin the design of the exercise prescription; 2) reporting ofthe components of the exercise prescription (i.e., fre-quency, intensity, time and type, or ‘FITT’) in the studymethods and 3) adherence of participants to the inter-vention prescribed in the study results.MethodsUsing the same protocol as our set of previously pub-lished reviews [9, 10], and recently published update instudies of breast cancer survivors [12], Medline,CINAHL, SPORTDiscus and EMBASE databases weresearched from January 1, 2012 to August 21, 2017. Thissearch complimented our previous search (completed toDecember 31, 2011) of exercise studies conducted insurvivors of all cancers, other than breast. This reviewincludes the seven papers from the original review [10]that included only men diagnosed with prostate cancer,and any new papers published between 2012 and 2017.The previous subject heading terms related to cancer(cancer, neoplasms, carcinoma) and exercise (exercise,physical activity, aerobic, resistance, walking, etc.) specificto each database were used and combined with the ANDTable 1 Exercise training principlesPrinciple Criteria for this review ExampleSpecificity: Training adaptations are specific tothe organ system or muscles trained withexerciseAppropriate population targeted andmodality selected based on primaryoutcomeAerobic exercise such as brisk walking is moreappropriate for an intervention aimed atincreasing cardiovascular fitness than strengthtrainingProgression: Over time, the body adapts toexercise. For continued improvement, thevolume or intensity of training must be increasedStated exercise programme was progressiveand outlined training progressionIncrease duration of walking program by 5% everytwo weeks depending on exercise toleranceOverload: For an intervention to improve fitness,the training volume must exceed current habitualphysical activity and/or training levelsRationale provided that programme was ofsufficient intensity/exercise prescribedrelative to baseline capacityPrescribing intensity in a resistance trainingprogram based on % of measured and/orestimated 1-repetition maximumInitial values: Improvements in the outcome ofinterest will be greatest in those with lower initialvaluesSelected population with low level ofprimary outcome measure and/or baselinephysical activity levelsSelecting a sample with high baseline fatiguelevels to participate in an aerobic trainingprogram to increase cardiovascular fitness andreduce fatigueReversibility: Once a training stimulus isremoved, fitness levels will eventually return tobaselinePerformed follow-up assessment on partici-pants who decreased or stopped exercisetraining after conclusion of interventionParticipants who maintained training after asupervised exercise program preserved strengthwhereas those who stopped exercising returnedto baselineDiminishing returns: The expected degree ofimprovement in fitness decreases as individualsbecome more fit, thereby increasing the effortrequired for further improvements. Also knownas the ‘ceiling effect’Performed follow-up assessment of primaryoutcomes on participants who continued toexercise after conclusion of interventionGains in muscle strength are greatest in the firsthalf of a training program unless the trainingstimulus continually increasesNeil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 2 of 13term. The search was then limited to English-languagepublications in peer-reviewed journals. Key publications,including relevant systematic reviews identified during theliterature search were hand-searched for relevant trials.Included studies were conducted exclusively in mendiagnosed with prostate cancer, regardless of treatmenttype or stage of treatment. Eligible studies were requiredto be RCTs with one or more treatment arms involvingat least four weeks of aerobic and/or resistance exercise.Alternative forms of exercise, such as yoga, Pilates, orTai Chi, as well as therapeutic interventions (i.e., phys-ical therapy, stretching) were excluded. Studies that fo-cused primarily on physical activity behaviour changeand those that only reported levels of physical activity orpsychosocial outcomes were excluded. In line with ourprevious criteria, all studies were required to report atleast one relevant physiological outcome related to exer-cise (e.g., aerobic capacity, muscular strength, physicalfunction, or body composition). Secondary publicationsfrom previously included trials were added to the data-base of included articles to allow for review of previouslyextracted data and updates regarding inclusion of infor-mation on use of exercise training principles, exerciseprescription or adherence to exercise prescription databut were treated as singular studies.Two reviewers (SNS and MM) independently deter-mined eligibility using an online software system (Covi-dence Systematic Review software, Veritas HealthInnovation, Melbourne, Australia). Each reviewer firstinspected the title and abstract of each study andfull-text versions of relevant papers were obtained andfurther reviewed for eligibility. Discrepancies were re-solved by consensus and the input of another memberof the study team (KWS) when required.All relevant data were extracted using the online soft-ware system, in duplicate, with discrepancies resolved byconsensus. Data extracted included sample size, timingof intervention delivery (during or after treatment),treatment type, intervention delivery mode (supervisedor home-based), intervention duration, timing offollow-up measures, primary and secondary outcomes,and study findings. The exercise prescription was ab-stracted according to the ‘FITT’ format from each publi-cation’s methods section, including frequency (numberof sessions per week), intensity (relative or absolute in-tensity of exercise), time (duration of exercise) and typeof exercise.For every described exercise prescription, the two re-viewers independently assigned a rating for the use ofeach principle of exercise training (see Table 1). Applica-tion of a principle was assigned a ‘+’ when the applica-tion was clearly reported and an ‘NR’ (not reported) ifthere was no indication that the principle was used inthe exercise prescription. A ‘?’ was assigned when theprinciple was mentioned but not described, inconsist-ently applied, or otherwise unclear. Adequate reportingof the prescription according to the FITT format, andparticipant adherence to the prescription was alsoassigned a ‘+’, ‘NR’ or ‘?’. For multi-arm trials comparingdifferent exercise interventions, the application of theprinciples of exercise training, and the exercise prescrip-tion was evaluated separately for each intervention arm.For trials that were previously included, newly identifiedarticles were screened for new information, to determinewhether the previously assigned ratings should be al-tered, but were not counted as another independenttrial.As described previously, the number and percentageof studies that met each criterion for attention to princi-ples of exercise training and reporting of exercise pre-scribed and completed was calculated and reported. Dueto the small number of prostate cancer studies includedin the first review, previously included and newly identi-fied studies are presented together in this review. Due tothe relatively small number of prostate cancer trials, wewere not powered for comparisons of reporting patternsbetween studies in our first review (< 2012) and newstudies identified in this review (> 2012). Thus, wepresent descriptive data only.ResultsStudy identification, screening, and eligibility informa-tion is outlined in the PRISMA diagram (Fig. 1). In total,41 papers were identified from our search and includedhere. Of these, there were 37 papers from 18 unique tri-als published after 2012, and four secondary papers [15–18] from the seven trials included in our previous review[19–25], for a total of 25 included trials. Of the four newpapers from previously included studies two reported ondifferent outcome measures [16, 18] and the other two re-ported secondary analyses of original outcomes [15, 17].After reviewing newly published papers from previouslyincluded trials, none of their ratings were changed fromour previous review.Across included trials, seven (28%) prescribed aer-obic exercise only [22, 25–30], five (20%) prescribedresistance exercise only [23, 31–34], ten (40%)prescribed combined aerobic + resistance exercise[19–21, 35–41] and three (12%) were multi-arm trials(seven intervention arms) comparing aerobic to resist-ance or aerobic + resistance exercise [24, 42, 43](Table 2). The interventions themselves ranged fromfour weeks to two years in duration and consisted of ei-ther entirely supervised (n = 10, 40%) [21–24, 30, 32, 34,35, 38, 39], entirely home-based (n = 5, 20%) [25–27, 40,41] or a combination of supervised + home-based exercise(n = 10, 40%) [19, 20, 28, 29, 31, 33, 36, 37, 42, 43].Neil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 3 of 13Application of the principles of exercise trainingRatings of the principles of exercise training for all in-cluded trials are displayed in Table 3. No included trialreported attention to all six evaluated principles of exer-cise training. Only nine (33%) trials appropriately appliedmore than half of the principles (i.e., four or five of apossible six), eight (28%) trials applied half of the princi-ples, and twelve (41%) trials applied fewer than halfother principles (Fig. 2).Specificity was appropriately applied by three (43%)aerobic trials [22, 25, 28], all five (100%) resistance trials[23, 31–34], nine (90%) combined trials [19–21, 35–40]and all seven (100%) multi-arm trials [24, 42, 43]. Speci-ficity was unclear in one (14%) aerobic [27] and one(10%) combined study [41]. Three (43%) aerobic studiesdid not attend to the principle of specificity [26, 29, 30].Progression was appropriately reported by three(43%) aerobic [27, 28, 30], all five (100%) resistance[23, 31–34], three (30%) combined [19, 35, 40] andfive (71%) multi-arm trials [24, 43]. Progression wasunclear in one (14%) aerobic [22], and four (40%)combined trials [21, 36, 37, 39]. The principle of pro-gression was not attended to in three (43%) aerobic[25, 26, 29], three (30%) combined [20, 38, 41] andtwo (29%) multi-arm trials [42].Across all studies, three (43%) aerobic [22, 27, 28], allfive (100%) resistance [23, 31–34], one (10%) combined[40], and five (71%) multi-arm trials [24, 43] adequatelyreported use of the principle of overload. One (14%) aer-obic [25] and one (10%) combined study [36] were un-clear in their application. The remaining three (43%)aerobic [26, 29, 30], eight (80%) combined [19, 20, 35–39, 41] and two (29%) multi-arm trials [42] did not re-port applying the principle of overload in the develop-ment of the exercise intervention.The principle of initial values was adequately reportedwithin three (43%) aerobic [27, 28, 30], four (80%) resist-ance [31–34], six (60%) combined [19, 35, 36, 38–40]Fig. 1 PRISMA diagram of study selectionNeil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 4 of 13Table 2 Description of included studiesAuthors, Year Timing Treatment N Intervention Length (weeks) Follow-up(weeks) Primary Outcome* (Tool) Other Outcomes (Tool)Aerobic Exercise OnlyEriksen et al,2017 [26]During AS 26 Home 26 12, 37, 52 NR VO2 peak (max cycle), lipids,insulin, glucose, PSA, FFM, FM,BMI, WCHvid et al,2016 [27]Mixed AS or RP 25 Home 104 12, 24, 36, 52, 78 NR VO2 peak (max cycle), BC (DXA),HOMA-IR (OGTT), TC, LDL, HDL,TG, TNF-α, IL-6, adiponectin, lep-tin, IGF-1, IGFBP-1, glucose, PSAJones et al,2014 [28]Mixed RP 50 Sup + Home 26 12, 52 Erectile Function (IIEF) VO2 peak (max TM), peripheralartery FMD, glucose, TC, TG, BC(BodPod)Monga et al,2007 [22]During RT 21 Sup 8 – Fatigue (PFS) VO2 peak (submax TM), strength(sit-stand)Pernar et al,2017 [29]After Mixed 41 Sup + Home 11 – NR BW, WC, BP, CRP, C-peptide, HDL,LDL, testosterone, SHBGUth et al,2014 [30]During ADT 57 Sup 12 32 LBM (DXA) BMD, BMC, FM (DXA), BW, BMI,WC, HC, WHR, VO2 peak (submaxTM), sit-stand, counter-movement jump, stair climb,strength (1RM, knee ext), bonemarkersWindsor et al,2004 [25]During RT 66 Home 4 – Fatigue (BFI), Aer fitness(Shuttle walk)NRResistance Exercise OnlyNilsen et al,2015 [31]During ADT 58 Sup + Home 16 – NR LBM, BMD, FM, %BF, BW, BMI(DXA), 1RM (knee ext., leg, chest,shoulder press), sit-stand, stairclimb, aer fitness (shuttle walk);muscle cell markers, fiberNorris et al,2015 [32]Mixed Mixed 30 Sup (High) 12 – Strength (est 1RM,bench press, leg press)Physical function (6MWT, 8 ft.TUG, 30s chair stands, 30s armcurls, S&R, back scratch); BW, BMI,Sup (Low)Segal et al,2003 [23]During ADT 155 Sup 12 – Fatigue (FACT-F) Muscle endurance (StandardLoad), BW, BMI, WC (SkF)Winters-Stone et al,2014 [33]During ADT 51 Sup + Home 52 – BMD (DXA) Bone turnover, LM, FM (DXA),insulin, IGF-1, SHBG, testosterone,strength (1RM, leg and chestpress), physical function (5 chairstand time, 4 m walk speed)Winters-Stone et al,2016 [34]After RT ± CT 64 Sup 24 12 Function (SPPB), MM,FM, %BF (DXA), fatigue(PFS), QoL (SF-36),strength (1RM leg,bench press)NRAerobic + Resistance ExerciseBourke et al,2011 [19]During ADT 100 Sup + Home 12 6, 24 QoL (FACT-P), DBP VO2 peak (submax TM), strength(Iso-dyn, subgroup), BMI, IGF-1,IGFBP-1, IGFBP-3, insulin, PSA, an-drogen, testosterone, SHBG; Sub-group: Brachial artery FMD, GTN-mediated brachial artery dilationCormie et al,2015 [35]During ADT 63 Sup 12 – LM, FM (DXA) BMD (DXA), aer fitness (400 mwalk), strength (1RM leg press,chest press, seated row), chairstand, stair climb, BP, CRP, TC, TG,insulin, glucose, HbA1C, boneturnover, vitamin D, testosterone,PSACulos-Reedet al, 2010 [20]During ADT 100 Sup + Home 16 8, 26 SR-PA (Godin) Aer fitness (6MWT), strength (Iso-dyn), S&R, BP, HRNeil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 5 of 13Table 2 Description of included studies (Continued)Authors, Year Timing Treatment N Intervention Length (weeks) Follow-up(weeks) Primary Outcome* (Tool) Other Outcomes (Tool)Galvao et al,2010 [21]During ADT 57 Sup 12 – LBM, FM, %BF (DXA) Strength (1RM), Endurance (Timeat 70% 1RM), physical function(sit-stand, 6 & 400 m walk),testosterone, PSA, insulin,glucose, lipids, CRPGalvao et al,2014 [36]After ADT + RT 100 Sup + Home 52 26 Aer fitness (400 m walk) Physical function (chair stands),WC, testosterone, PSA, insulin,TC, TG, LDL, HDL, HbA1C,glucose, BPSubgroup: Strength (1 RM, chestand leg press), FM, %BF,adiposity (DXA)Gaskin et al,2017 [37]After Mixed 320 Sup + Home 12 26, 52 SR-PA (LTEQ) RHR, BP, aer fitness (6MWT),strength (1RM), physical function(30s sit-stand), BW, BMI, WC, HC,upper arm, chest, thighcircumferenceHojan et al,2016 [38]During RT + ADT 55 Sup 8 – NR PSA, Hb, WBC, RBC, neutrophil,lymphocytes, platelets,monocytes, IL-B, IL-6, TNF-α, Aerfitness (6MWT)Hojan et al,2017 [39]During RT + ADT 72 Sup 52 8 Aer fitness (6MWT), IL-1B, IL-6, TNF-a, BMI,WHR, WC, TC, HDL, LDL,TG, AST, ALTNRKim, 2018[40]During ADT 51 Home 24 – BMD (DXA), Boneturnover markers (bs-ALP, NTx)Strength (grip, hip, HHD), 30schair-stand, TUGSajid et al,2016 [41]During ADT 19 Home 6 12 Function (SPPB) Aer fitness (6MWT), strength(grip, chest press reps), FM, LM,MM (DXA)TechnologyAerobic or Resistance Exercise (Multi-Arm Trials)Santa Mina etal, 2013 [42]During ADT 26 Sup +Home Aer24 12, 52 QoL (FACT-P, Patient-Oriented Prostate UtilityScale), Fatigue (FACT-F)VO2 peak (Submax TM), gripstrength, BW, BMI, %BF, WC, IGF-1, IGFBP-3, leptin, adiponectinSup +Home ResSegal et al,2009 [24]During RT 121 Sup Aer 24 – Fatigue (FACT-F) VO2 peak (max TM), strength(8RM), BW, BC (DXA),testosterone, PSA, Hb, lipidsSup ResWall et al,2017 [43]During ADT 163 Sup + HomeAer + Res52 (26) – BMD (DXA), LM, FM,Trunk fat, % BF, (DXA),VO2 peak (Max TM)RMR, BP, arterial stiffness, HbA1C,testosterone, insulin, PSA, TG,LDL, HDL, TC, glucose, CRP, bs-ALP, PINP, BW, strength (1-RM),endurance (#reps @ 70% 1RM,chest & leg press), chair stands,stair climb, 6 m backward walk,400 m walk timeSup + HomeImpact +ResHome Aer 26 –Legend: 6MWT: 6 min walk test; ADT: androgen deprivation therapy; Aer: aerobic; ALT: alanine transaminase; AS: active surveillance; AST: aspartatetransaminase; BC: body composition; BFI: brief fatigue inventory; BMC: bone mineral content; BMD: bone mineral density; BMI: body mass index; BP:blood pressure; bs-ALP: bone specific alkaline phosphatase; BW: body weight; CRP: c-reactive protein; CT: chemotherapy; DBP: diastolic bloodpressure; DXA: dual energy x-ray absorptiometry; ext: extension; FACT-F: functional assessment of cancer therapy – fatigue; FACT-P: functionalassessment of cancer therapy – prostate; FFM: fat free mass; FM: fat mass; FMD: flow mediated dilation; Hb: hemoglobin; HbA1C: glycosylatedhemoglobin; HC: hip circumference; HDL: high density lipoprotein; HHD: hand held dynamometry; HOMA-IR: homeostatic assessment of insulinresistance; IGF: insulin-like growth factor; IGFBP: insulin-like growth factor binding protein; IIEF: international index of erectile function; IL:interleukin; Iso-dyn: isometric dynamometry; LBM: lean body mass; LDL: low density lipoprotein; LM: lean mass; LTEQ: leisure time exercisequestionnaire; Max: maximum; MM: muscle mass; NR: not reported; NTx: type 1 cross-linked N-telopeptide; OGTT: oral glucose tolerance test; PFS: piperfatigue scale; PINP: Pro collagen Type 1 N-Terminal Propeptide; PSA: prostate specific antigen; QoL: quality of life; RBC: red blood cell; Res: resistance;RHR: resting heart rate; RM: repetition maximum; RMR: resting metabolic rate; RP: radical prostatectomy; Res: resistance training; RT: radiation therapy;S&R: sit and reach; SHBG: sex hormone binding globulin; SkF: skin fold; SPPB: short physical performance battery; SR-PA: self-reported physical activity;submax: submaximal; Sup: supervised; TC: total cholesterol; TG: triglycerides; TM: treadmill; TNF-α: tumour necrosis factor-alpha; TUG: timed up and go;VO2 peak: peak oxygen consumption; WBC: white blood cell; WC: waist circumference; WHR: waist-hip ratio; *Where specifically statedNeil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 6 of 13Table 3 Application of the principles of exercise training and outcomesAuthors, Year Sp Pr OV IV Rev DR Significant resultsAerobic Exercise OnlyEriksen et al, 2017 [26] NR NR NR NR ? ? ↑VO2 peak (6mo only)Hvid et al, 2016 [27] ? + + + ? ? 6 mo: ↑VO2 peak, adiponectin, IGFBP-1; ↓FM, trunk mass, gynoid FM, android fat; 24 mo:↓ FM, trunk mass, gynoid FM, android fat, TG, IGF-1, glucoseJones et al, 2014 [28] + + + + ? ? ↑FMD, VO2 peakMonga et al, 2007 [22] + ? + NR NR NR ↑ VO2 peak, Strength; ↓ Fatigue*Pernar et al, 2017 [29] NR NR NR NR NR NR ↑ HDLUth et al, 2014 [30] NR + NR + ? ? EoS: ↑LBM*, strength, BMC, P1NP, osteocalcin; 32 w: ↑BMD, counter jump, stair climbWindsor et al, 2004 [25] + NR ? NR ? ? ↑ Aer fitness*Resistance Exercise OnlyNilsen et al, 2015 [31] + + + + NR NR ↑Muscle fiber cross-sectional area, strength (leg ext., leg, chest, shoulder press),sit-stand; LBM (lower & upper)*Norris et al, 2015 (High) [32] + + + + NR NR No between group differenceNorris et al, 2015 (Low) [32] + + + + NR NR No between group differenceSegal et al, 2003 [23] + + + NR NR NR ↓ Fatigue*; ↑Muscle enduranceWinters-Stone et al, 2014 [33] + + + + NR ? ↓ FM, ↑strengthWinters-Stone et al, 2016 [34] + + + + NR + ↑Upper body strength*Aerobic and Resistance ExerciseBourke et al, 2011 [19] + + NR + ? ? ↑QoL (12w only)*; VO2 peak, strength, FMD, skeletal MM, SHBG (subgroup only)Cormie et al, 2015 [35] + + NR + NR NR ↑Appendicular LM*, Aer fit, strength, chair stands; ↓ FM*, % BF*, TCCulos-Reed et al, 2010 [20] + NR NR NR NR NR ↑ SR-PA*Galvao et al, 2010 [21] + ? ? NR NR NR ↑ LBM*, Strength, Endurance, 6 m walk; ↓ CRPGalvao et al, 2014 [36] + ? NR + NR + ↑ Aer fitness*, chair stands, strength (6 & 12 mo); appendicular MM (6 mo only), HDL;↓ TC (12 mo only)Gaskin et al, 2017 [37] + ? NR NR ? ? ↑ Vigorous SR-PA (12wk & 6 mo only)*; Aer fitness, strength, sit-stand;↓ HC, RHR (12w only)Hojan et al, 2016 [38] + NR NR + NR NR ↑Aer fitnessHojan et al, 2017 [39] + ? NR + NR + ↓ BW, BMI*, WHR*, PSA, IL-6*, ↑ Aer fitness*Kim et al, 2018 [40] + + + + NR NR ↑ Grip strength (left hand), 30s chair standsSajid et al, 2016 (Home) [41] ? NR NR NR NR NR ↑ SPPB (vs. control)*Sajid et al, 2016 (Tech) [41] ? NR NR NR NR NR NoneAerobic or Resistance Exercise (Multi-Arm Trials)Santa Mina et al, 2013 (Aer) [42] + NR NR NR ? + ↓ BW, WC, BMI (3 mo only)Santa Mina et al, 2013 (Res) [42] + NR NR NR ? + ↑ IGFBP-3 (6 mo only)Sega et al, 2009 (Aer) [24] + + + NR NR NR ↑ VO2 peakSegal et al, 2009 (Res) [24] + + + NR NR NR ↑ VO2 peak, Strength; No %BF; ↓ TGWall et al, 2017(Aer + Res)+ + + + NR + ↑ Strength (6 mo only); Vs. control only: ↑VO2 peak, LM*;↓ glucose, FM*, trunk FM*, % BF*Wall et al, 2017(Impact + Res) [43]+ + + + NR + ↑ Strength (6, 12 mo)Wall et al, 2017 (Aer) [43] + + + + NR + NoneLegend: Aer: aerobic; BMC: bone mineral content; BMD: bone mineral density; BMI: body mass index; BW: body weight; CRP: c-reactive protein; DR:diminishing returns; ext: extension; FM: fat mass; FMD: flow mediated dilation; HC: hip circumference; HDL: high density lipoprotein; IGF: insulin-likegrowth factor; IGFBP: insulin-like growth factor binding protein; IL: interleukin; IV: initial values; LBM: lean body mass; LM: lean mass; MM: muscle mass;mo: months; NR: not reported; OV: overload; Pr: progression; PSA: prostate specific antigen; QoL: quality of life; Res: resistance; Rev: reversibility; RHR:resting heart rate; SHBG: sex hormone binding globulin; Sp: specificity; SPPB: short physical performance battery; SR-PA: self-reported physical activity;TC: total cholesterol; TG: triglycerides; VO2 peak: peak oxygen consumption; WC: waist circumference; WHR: waist-hip ratio; * Primary outcomeNeil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 7 of 13and three (43%) multi-arm trials [43]. Attention to initialvalues was not at all reported in the remaining four(57%) aerobic [22, 25, 26, 29], one (20%) resistance [23],four (40%) combined [20, 21, 37, 41] and four (57%)multi-arm trials [24, 42]. No trials were assigned an un-clear rating for initial values.No included trial adequately reported attention to theprinciple of reversibility. Five (71%) aerobic [25–28, 30],two (20%) combined [19, 37], and two (29%) multi-armtrials [42] were assigned an unclear for this principle.The remaining two (29%) aerobic [22, 29], all five (100%)resistance [23, 31–34], eight (80%) combined [20, 21, 35,36, 38–41] and five (71%) multi-arm trials [24, 43] didnot report reversibility at all.Finally, diminishing returns was reported by one (20%)resistance training trial [34], two (20%) combined trials[36, 39], and five (71%) multi-arm trials [42, 43]. Dimin-ishing returns was unclear in five (71%) aerobic [25–28,30], one (20%) resistance [33], and two (20%) combinedinterventions [19, 37]. It was not at all reported in theremaining two (29%) aerobic [22, 29], three (60%) resistance[23, 31, 32], six (60%) combined [20, 21, 35, 38, 40, 41] andtwo (29%) multi-arm trials [24].Reporting of the components of the exercise prescriptionReporting of each component of the exercise prescriptionare displayed in Fig. 3a. Reporting of the components ofthe exercise prescription was generally high, with five(71%) aerobic [22, 25–28], all five (100%) resistance [23,31–34], seven (70%) combined [19, 21, 35–39] and six(86%) multi-arm trials [24, 42, 43] adequately reporting allfour components of the exercise prescription. Prescribedintensity was unclear in one (10%) combined [41] and one(14%) multi-arm trial [43] and was not at all reported intwo (29%) aerobic [29, 30] and one (10%) combined trial[20]. Prescribed duration of exercise was unclear in one(10%) combined [41] and one (14%) multi-arm trial [43],and was not reported in one (10%) combined study [20].Prescribed type of exercise was unclear in two (20%) com-bined studies [40, 41].Reporting of adherence to the prescribed interventionReporting of adherence to the prescribed interventions,or actual exercise completed by participants is displayedin Fig. 3b. No studies adequately reported adherence toall four components of the prescribed exercise program.Two (29%) aerobic [22, 26], four (40%) combined [20,36, 40, 41] and two (29%) multi-arm interventions [42]did not adequately report any component of adherence.Frequency of exercise completed was the most com-monly reported component, with three (43%) aerobic[27, 28, 30], all five (100%) resistance [23, 31–34], six(60%) combined [19, 21, 35, 37–39] and five (71%)multi-arm trials [24, 43] adequately reporting frequencyof exercise completed. One (14%) aerobic [29], two(20%) combined [36, 40], and two (29%) multi-arm trials[42] were unclear in their reporting of frequency of exer-cise completed, and three (43%) aerobic [22, 25, 26] andtwo (20%) combined studies [20, 41] did not report ad-herence to prescribed frequency at all.Fig. 2 Number of exercise training principles applied across included trialsNeil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 8 of 13Intensity of exercise completed was reported fully in onlytwo (29%) aerobic studies [25, 27]. Adherence to intensitywas unclear in three (43%) aerobic [26, 28, 30], two (40%)resistance [33, 34], and three (30%) combined studies [19,35, 40]. Adherence to intensity prescribed was not at all de-scribed in the remaining two (29%) aerobic [22, 29], three(60%) resistance [23, 31, 32], seven (70%) combined [20, 21,36–39, 41] and all seven (100%) multi-arm trials [24, 42, 43].Duration of exercise completed was only reported inone (14%) aerobic trial [25]. Duration was unclear inthree (43%) aerobic [26–28], one (20%) resistance [34],and three (30%) combined studies [19, 39, 40]. Durationwas not at all reported in the remaining three (43%) ofaerobic [22, 29, 30], four (80%) of resistance [23, 31–33],seven (70%) combined [20, 21, 35–38, 41], and all seven(100%) multi-arm trials [24, 42, 43].The type of exercise completed was fully reported byfour (57%) aerobic studies [25, 28–30]. Adherence to ex-ercise type was unclear in one (14%) aerobic [27], one(20%) resistance [34], and one (10%) combined study[40], and was not at all reported in the remaining two(29%) aerobic [22, 26], four (80%) resistance [23, 31–33],abFig. 3 a Reporting of exercise prescription in study methods. b Reporting of adherence to exercise prescription in study resultsNeil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 9 of 139 (90%) combined [19–21, 35–39, 41] and all seven(100%) multi-arm trials [24, 42, 43].DiscussionThe papers included in this review of exercise program-ming and compliance in RCTs in men diagnosed withprostate cancer include data from 1891 men receivingvarious types of treatment for prostate cancer currentlyor in the past. The efficacy of exercise reported variedacross trials and outcomes, but was generally positive; ofthe twenty papers that specified a primary outcome, 75%reported statistically significant changes in that outcome,and all but two trials found significant changes in atleast one secondary outcomes.Consistent with our previous findings in women withbreast cancer, reporting of adherence to the exercise pre-scription was poor. Without greater information on com-pliance to the exercise prescription, it remains unclear whatexercise dose is actually needed to achieve desired out-comes mirroring those observed in the studies presented.No study reported all components, and three studiesfailed to report any indication of adherence. Frequencyof exercise performed was most commonly reported,usually as a percentage of sessions attended in a super-vised program or number of exercise sessions per weekin a home-based intervention. This is not surprisinggiven the relatively straightforward methods needed tocollect this data. Reporting adherence to prescribed in-tensity may be more logistically challenging but is none-theless important for replication and implementation. Inan aerobic exercise intervention for example, averageheart rate during an exercise session would require useof a heart rate monitor. Other methods, such as ratingof perceived exertion (RPE) could be used if objectivemonitoring is not possible due to budgetary or logisticconstraints. In addition to the actual FITT adherence,modifications needed to the exercise prescription, or thenumber of participants requiring substantial modifica-tions would be interesting and important data to report.As found in our previous reviews of breast and allother cancer types, attention to the standard principlesof exercise training was not strong across the literaturereviewed. No studies included in this review appropri-ately applied all principles of exercise training, and onlynine studies appropriately reported more than half (i.e.,four or five of the six) principles. Lack of attention toprinciples of exercise training may result in an under-estimation of the true benefit that exercise may have at alarger population level. From a practice standpoint, in-attention to training principles leaves the fitness profes-sional without the information s/he may need toprescribe a training program for an individual client.When the exercise prescribed does not match the de-sired outcomes or inappropriate populations are selected(lack of attention to specificity), failure to see improve-ments in the primary outcome of interest may be due tothe prescription chosen rather than lack of efficacy ofexercise itself. In the papers included, we saw a substan-tial difference in attention to specificity between aerobiconly (43%) and resistance only (100%) interventions.Body composition, and bone mineral density are keyconcerns for men with prostate cancer, particularly thoseon androgen deprivation therapy, and are a common tar-get for exercise interventions. It is well known thatweight bearing exercise, specifically moderate-high in-tensity resistance training is required to elicit changes inbone mineral density in healthy populations [44]. Apopular type of exercise that is known to reduce fatigueduring prostate cancer treatment is walking, but thismodality would be ineffective if the goal were to preventADT-induced bone loss. Thus interventions who choseaerobic exercise only for this purpose were assigned aNR for this principle. In this review, specificity was ap-propriately applied most commonly, and is a more eas-ily determined component of the prescription andshould be continued in future trials and in translationto practice.The principle of progression considers that as the bodyadapts over time to the training stimulus, in order to seeclinically meaningful improvements, and continued im-provement and maintenance of outcomes over time thetraining volume (intensity, frequency and duration) mustcontinue to be altered over time [45]. In this review, justover half of studies included adequately reported pro-gressive exercise prescriptions throughout the interven-tion period. Progression, and specifically the rate ofprogression of the exercise prescription is also importantto note from a safety perspective. This information iscritical for exercise professionals, as translation of exer-cise into community- or clinical- settings should bebased on the RCT evidence accumulated to date. Pro-gression that occurs too quickly could result in increasedrisk of injury, and too slowly could reduce efficacy, andlead to frustration and ultimately lack of compliance ifindividuals fail to see results. Similar to our previous re-views, we note that resistance training interventions aretypically better at reporting progression in their pre-scription than aerobic interventions. This may be due tothe perceived ease of instruction and recording of in-creased resistance weight. Although there is a reasonableupper limit to aerobic exercise frequency and durationthat individuals will be able to complete from a logisticsperspective, progression of intensity of exercise, througheither heart rate target or RPE is important to elicit anadequate training stimulus.Equally important considerations in ensuring that anadequate exercise stimulus or dose of exercise is deliv-ered in order to expect improvements in a particularNeil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 10 of 13health outcome are the related principles of overloadand initial values. Each of these principles were ad-equately reported by roughly half of included studies. Toensure participants experience gains in physical fitness,it is essential that exercise interventions be prescribed ata higher volume relative to measured baseline levels.Without knowing whether or not adequate overload wasapplied relative to an individual’s initial value of an out-come, participants may be prescribed less activity thanreported at baseline, which introduces the potential fordetraining during the intervention. On the other hand, aparticipant could receive a prescription that is too vigor-ous for them increasing the risk of adverse events ordropout. The population of men with prostate cancerrepresent a heterogeneous group; they tend to be older,have a variety of comorbidities, be physically inactive andreceive treatments with side effects that accelerateage-related fitness declines. Given this, as well as individualdifferences in responses to exercise, prescribing exerciserelative to a man’s starting capacity is critically important.In this review, no study evaluated the principle of re-versibility, and only 28% of studies examined theprinciple of diminishing returns. Understanding the tra-jectory of change over time in expected outcomes acrossan intervention is necessary to ensure that adequateoverload is maintained by progressing the training pro-gram. For example, in resistance training interventionsmen will increase muscle strength over time such that agiven weight represents less of their maximum capacity(e.g., 1-RM) and thus weakens the training stimulus.Knowing that diminishing returns is likely to occur, par-ticularly in longer intervention periods, investigators andfitness professionals should build in periodic reassess-ments to recalibrate training volume. Measuring andreporting on these components may be logistically morechallenging during an exercise intervention, as multipletime points of assessment are needed. When a full out-come assessment is not feasible, we urge investigators toconsider the use of a shorter test battery or even proxymeasures of the outcome of interest (example self-reportbody weight vs. in-person weigh in) at time pointsthroughout the intervention to help us to better under-stand trajectory of change and adjust the exercise pre-scription as needed.Reversibility is also a challenging principle to attendto, especially outside of the context of a supervisedintervention. Reversibility of training effects may occurwhen a specific intervention ends and participants donot continue on their own, or due to lack of complianceduring the intervention period. Understanding the longterm effects on relevant outcomes after an intervention,particularly a supervised intervention, ends is importantfor the translation of research to practice. Knowledge ofthese aspects will help improve exercise prescriptionfrom an exercise physiology perspective, but may alsoinform incorporation of behaviour change techniquesfor long-term maintenance and sustainability.One consideration that must be made when interpret-ing findings from this review is that study authors werenot contacted for missing data. With respect to the at-tention to principles of exercise training, some of thesestudies may have carefully considered these in the designof their intervention but assigned a rating of unclear orNR in this review. We strongly urge all authors of exer-cise trials to carefully report all details of the interven-tion. Given that online appendices or supplementarymaterials are now common in most scientific journals,there is a greater opportunity to report these aspects infuture studies while still adhering to strict word andpage limits of the articles themselves. We also recom-mend authors follow the guidelines published in the re-cently published Consensus on Exercise ReportingTemplate (CERT), including the frequency, intensity,duration and type of exercise prescribed under section13, “When, How Much” and exercise actually completedunder section 16, “How Well: Planned, actual” [46].ConclusionsAs the evidence base for the effect of exercise in men di-agnosed with prostate cancer grows, it is important forresearchers to apply the basic principles of exercisetraining in the design of their intervention, and to fullyreport all components of the exercise prescription (ordose) assigned and received, in order to continue tomove the field of exercise oncology forward. This willallow better translation of evidence-based research intoclinical practice and allow for greater fidelity of the an-ticipated response to a prescribed exercise program.AbbreviationRCT: Randomized Controlled TrialAcknowledgementsNot applicable.FundingSNS is supported by a postdoctoral fellowship from the Canadian Institutesfor Health Research. The funding body had no involvement in the studydesign, analysis or interpretation of data.Availability of data and materialsAll data generated or analysed during this study are included in thispublished article.Authors’ contributionsKWS and KLC conceived of the original review. SENS conceived of theupdate. SENS and MM screened references and extracted all data. SENSdrafted the manuscript. SENS, MM, KB, KLC and KWS critically reviewed themanuscript and provided final approval.Ethics approval and consent to participateNot applicable.Neil-Sztramko et al. BMC Cancer          (2019) 19:321 Page 11 of 13Consent for publicationNot applicable.Competing interestsNot applicable.Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims inpublished maps and institutional affiliations.Author details1School of Nursing, McMaster University, 175 Longwood Road S, Suite 210a,Hamilton, ON L8P 0A1, Canada. 2School of Nursing, Oregon Health andScience University, Portland, Oregon, USA. 3Department of Physical Therapy,University of British Columbia, Vancouver, British Columbia, Canada. 4MaryMacKillop Institute for Health Research, Australian Catholic University,Melbourne, Victoria, Australia. 5Knight Cancer Institute, Oregon Health andScience University, Portland, Oregon, USA.Received: 4 October 2018 Accepted: 25 March 2019References1. Canadian Cancer Society's Advisory Committee on Cancer Statistics: CanadianCancer Statistics 2017. In. Toronto, ON: Canadian Cancer Society; 2017.2. 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