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51 Lymphology 47 (2014) 51-64 A HOME-BASED WEIGHT LIFTING PROGRAM FOR PATIENTS WITH ARM LYMPHEDEMA FOLLOWING BREAST CANCER TREATMENT: A PILOT AND FEASIBILITY STUDY K. Johansson, P. Klernäs, A. Weibull, S. Mattsson Department of Health Science (KJ), Lund University; Red Cross Hospital (PK), Solna; and Medical Radiation Physics (AW,SM), Department of Clinical Sciences Malmö, Lund University, Sweden ABSTRACT It is well documented that resistance exercise can be performed by patients with breast cancer-related arm lymphedema. The aim of this pilot study was to evaluate the feasibility and safety of a 12-week self- administered weight lifting program for arm and shoulder, and its influence on arm lymphedema status, upper extremity muscle strength, and disability. Twenty-three patients with breast cancer-related arm lymphedema performed the program 3 times/week. The weight resistance levels were individually adjusted for shoulder flexion and adduction, and elbow extension and flexion corresponding to a repetition range of 8-12 repetition maximum. A log book was used to evaluate adherence to the program, wearing of compression sleeve and perceived exertion. Measurements were performed before a 2-week control period without intervention, and before and after intervention, and with arm volume measurements every fortnight to check for adverse events. Results revealed no significant changes during the control period. Adherence to the intervention program was excellent, and two adverse events were registered during the first weeks. After intervention, an increase of shoulder and arm strength (measured by an isometric muscle strength device) was found in all exercises (p=0.001-0.003). A reduction of excess volume was shown, in ml (p=0.03) and percentage (p=0.005), measured by water displacement method. A tendency towards reduction (p=0.07) of fat tissue in the upper arm (n=10) in both arms was found measured by MRI. In this pilot study, we concluded that a home-based weight-lifting program performed by patients with breast cancer-related arm lymphedema is feasible and safe providing that the program includes regular follow-up for safety. Keywords: Arm lymphedema, breast cancer, exercise, weight lifting, MRI Breast cancer patients have been the most extensively studied among cancer patients in terms of exercise interventions. A systematic review and meta-analysis of 66 high quality studies of exercise interventions for cancer survivors reports positive outcomes during as well as after treatment. Some of the most notable positive outcomes from post- treatment exercise were in physical activity level, upper body strength, body weight, body fat percentage, body mass index and fatigue (1). In addition, a meta-analysis by Ibrahim and Al-Homaidh has shown evidence for an inverse relationship between physical activity and mortality in patients already treated for Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY.

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51

Lymphology 47 (2014) 51-64

A HOME-BASED WEIGHT LIFTING PROGRAMFOR PATIENTS WITH ARM LYMPHEDEMA

FOLLOWING BREAST CANCER TREATMENT:A PILOT AND FEASIBILITY STUDY

K. Johansson, P. Klernäs, A. Weibull, S. Mattsson

Department of Health Science (KJ), Lund University; Red Cross Hospital (PK), Solna; and MedicalRadiation Physics (AW,SM), Department of Clinical Sciences Malmö, Lund University, Sweden

ABSTRACT

It is well documented that resistanceexercise can be performed by patients withbreast cancer-related arm lymphedema. Theaim of this pilot study was to evaluate thefeasibility and safety of a 12-week self-administered weight lifting program for armand shoulder, and its influence on armlymphedema status, upper extremity musclestrength, and disability. Twenty-three patientswith breast cancer-related arm lymphedemaperformed the program 3 times/week. Theweight resistance levels were individuallyadjusted for shoulder flexion and adduction,and elbow extension and flexion correspondingto a repetition range of 8-12 repetitionmaximum. A log book was used to evaluateadherence to the program, wearing ofcompression sleeve and perceived exertion.Measurements were performed before a 2-week control period without intervention, and before and after intervention, and witharm volume measurements every fortnight to check for adverse events.

Results revealed no significant changesduring the control period. Adherence to theintervention program was excellent, and twoadverse events were registered during the firstweeks. After intervention, an increase ofshoulder and arm strength (measured by anisometric muscle strength device) was found in

all exercises (p=0.001-0.003). A reduction ofexcess volume was shown, in ml (p=0.03) andpercentage (p=0.005), measured by waterdisplacement method. A tendency towardsreduction (p=0.07) of fat tissue in the upperarm (n=10) in both arms was found measuredby MRI.

In this pilot study, we concluded that ahome-based weight-lifting program performedby patients with breast cancer-related armlymphedema is feasible and safe providing that the program includes regular follow-upfor safety.

Keywords: Arm lymphedema, breast cancer,exercise, weight lifting, MRI

Breast cancer patients have been themost extensively studied among cancerpatients in terms of exercise interventions. A systematic review and meta-analysis of 66high quality studies of exercise interventionsfor cancer survivors reports positive outcomesduring as well as after treatment. Some of the most notable positive outcomes from post-treatment exercise were in physical activitylevel, upper body strength, body weight, bodyfat percentage, body mass index and fatigue(1). In addition, a meta-analysis by Ibrahimand Al-Homaidh has shown evidence for aninverse relationship between physical activityand mortality in patients already treated for

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breast cancer (2). Both meta-analyses supportthe observation that appropriate physicalactivity should be embraced by all breastcancer survivors.

Reduced muscle strength is an impair-ment following breast cancer treatment,which interferes with physical activity. In aprospective longitudinal study of 61 breastcancer patients with axillary lymph nodedissection, Johansson et al (3) found reducedshoulder muscle strength not only after 6months but also 2 years after surgerycompared to preoperative values. This wasconfirmed in a study by Rietman et al (4)examining a mixed group of patients withaxillary lymph node dissection (n=124) orsentinel lymph node biopsy (n=57). Anothersimilar study of 23 breast cancer patientsshowed a negative influence of the breastcancer treatment on work ability and sparetime activities in 60% of the patients (5). The impact on work ability for breast cancerpatients, also having arm lymphedema, wasfound in a qualitative interview study by Fuconcluding that women, whose jobs requiredheavy lifting and constant use of the affectedlimb, suffered profoundly from the physicaland functional impact of having lymphedema(6). It may therefore be of importance forbreast cancer patients to retain musclestrength in their arms, and it may be ofparticular importance for patients with armlymphedema.

An issue interfering with muscle strengthtraining is that breast cancer patients areoften advised, based on empiricism, to avoidheavy work with the arm and not to“overload” the lymphatic system and “to becareful.” Such advice promotes the idea thatinactivity is beneficial. On the other hand,they are advised to be active with the arm tostimulate the same system and to preventstrength reduction. This seeming contradic-tion obviously is confusing for the patient andrequires clarification. However, recently asystematic review of exercise in patients withlymphedema has been performed by Kwan et al, and they state that strong evidence is

now available on the safety of resistanceexercise without risk of development orexacerbation of breast cancer-relatedlymphedema (7).

Most studies on exercise for women with arm lymphedema have been based onsupervised activities, single or in groups (7).However, many women may not want to orare not able to take part in group activities on a regular basis. Therefore, we wanted toevaluate a home-based exercise program.

The main objective of the present pilotstudy was to evaluate the feasibility of a 12-week self-administered weight liftingprogram and its influence on arm lymphe-dema status, upper extremity muscle strength and disability.

METHODS

Subjects and Recruitment

Patients were eligible if they were lessthan 70 years old, had a history of unilateralbreast cancer, but were disease-free, hadcurrent arm lymphedema (arm volumedifference of 5%) (8) that was pre-existingfor more than 6 months, but had not receivedactive treatment for lymphedema during thelast month, except for use of compressiongarments. Patients with a pre-existingmedical condition considered contraindicatedto participating in a home-based exerciseintervention (e.g. chronic neck pain, skindisorder, dementia) were excluded fromparticipating. Permission to contact eachpatient by phone was obtained through theirphysiotherapists.

Forty-two patients with arm lymphe-dema following breast cancer treatment wereidentified through physiotherapists’ registryof lymphedema patients at the LymphedemaUnit, Skane University Hospital and RedCross Hospital, Solna and met inclusioncriteria. Five patients did not answer phonecalls, or mails that were sent out. Elevenpatients declined to take part due to lack oftime (n=2) or long travel distance from

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hospital to perform measurement procedure(n=9). Twenty-six patients were finallyincluded in the study.

The study was approved by the RegionalEthical Review Board at Lund University(Dnr: 55/2006).

Design

The study design of this pre-post pilotand feasibility study is presented in Fig. 1.Before the start of the study the patients hadto wear a compression sleeve for at least 2 weeks to maintain a steady arm volume. The compression sleeves were of standardtype or custom-made, and were worn duringday and night or daytime according to theirusual procedures during the last 3 months.The compression grade was at least ccl II (23-32 mmHg) according to the EuropeanCommittee for Standardisation (9), and mostof them had a silicon top band. The sleevewas no older than 1 month.

The study started with a 2-week controlperiod with the intention to determine thatthe arm volume was steady. The time toascertain a steady arm volume with at least 2 weeks with a compression sleeve followedby the 2-week control period was chosenaccording to the results of a study of 4 weeksof treatment including compression garmentand isometric exercises (10). The resultsshowed that the largest volume reduction wasfound during the first week, whereas over the

course of the next three weeks the benefitdecreased sharply.

After the control period, a 4-weekintroduction of gradually increasingresistance levels, starting with 50% of 10repetition maximum (RM) and ending withcompleted 10RM, was applied for thepatients to adjust to the interventionprogram. If no lymphedema exacerbationswere found, the weights were increased by0.5-1.0 kg every second session until theyreached 10RM. After 4 weeks of introduction,the patients performed an 8-week programaccording to the criteria of intervention.

Intervention

The patients were provided with a boxwith flexible dumbbells for performance ofthe weight lifting exercises at home, 3 timesper week with at least one day in between.The lowest possible weight was 0.5 kg and the highest 12.0 kg.

Four different exercises were eachperformed in the following order: (I) shoulderflexion in a standing position, (II) shoulderadduction and (III) elbow extension in asupine position and (IV) elbow flexion insitting position. These exercises had beentested in a prior study of low resistancetraining (11).

The weight resistance levels wereindividually adjusted according to guidelinesof the American College of Sports Medicine

Fig. 1. Study design of the 12-week exercise program; Measurements: V = Volume of the arms, B = Bioimpedance,M = Muscle strength, D = DASH (Disability of arm, hand and shoulder)

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(12) for untrained individuals recommendingloads corresponding to a repetition range of8-12 repetition maximum (RM) and trainingfrequency of 2-3 days per week. In thepresent study the patients were requested tocomplete at least 8 repetitions for each setand if they could complete more than 12, the resistance was increased with 0.5kg forsubsequent sets. Four sets of each exercisewere completed at each session with the firstset using 50% of the 10RM weight as a warm-up and the subsequent three sets completedwith the 8-12 RM weight. A 1-3 minute restperiod was taken in between each set.

During the exercise the women were freeto choose whether they wanted to use thecompression sleeve or not as long as they putit on again immediately following training.This recommendation was based on resultsfrom a prior weight-lifting exercise studyshowing an increase of total arm volume ofthe lymphedema arm immediately after theexercise intervention for both with andwithout sleeve conditions. However, after 24 hours of wearing the compression sleeve,no volume increase was found compared topre-exercise volume (11).

Measurements

Outcomes of interest for this trial werefeasibility, lymphedema status, upperextremity muscle strength and disability.Measurements were performed by the samephysiotherapists (KJ and PK) who gaveinstructions to the patients.

Feasibility: Retention and adherence

Retention was assessed by withdrawalrates and adherence was assessed by a logbook, including date for session, wearing ofcompression sleeve, weight resistance andperceived exertion for each exercise. Theminimum performance for acceptable adher-ence was set so that the sessions should beperformed at least on level 13 (hard) on theBorg scale for each exercise, 2 times per week.

Lymphedema status

Water displacement method (WDM):Arm volume was measured with the waterdisplacement method which is used as thegold standard of limb volume measurements(13) and was described by Kettle (14).Bednarczyk et al (15) carried out a validitytest for the method with a computerized limbvolume measurement system and found ahigh correlation coefficient (r=0.992), andSander et al (16) found ICC to be 0.99 forboth inter- and intra-rater reliability.

Each arm was submerged in a containerwith water with the contralateral arm as thecontrol on each occasion. The volumedisplacement was measured in grams andthen converted into milliliters. The armvolume of the arm was expressed as total armvolume (TAV). Arm lymphedema, wasdefined as >5% excess volume compared tothe contralateral arm (8) obtained bycalculating the difference in volume betweenthe affected arm and the contralateral arm.Arm lymphedema was expressed in millilitersas lymphedema absolute volume (LAV) and in percentage as lymphedema relativevolume (LRV).

Bioelectrical impedance spectroscopy(BIS): Extracellular fluid in the arm wasmeasured using a swept frequencybioelectrical impedance meter (model SFB3,SEAC Brisbane, Australia). The resistance atzero frequency, R0, has been shown to be areliable predictor of extracellular water (17).Using a multi-frequent current, R0 can beestimated by extrapolation of the impedancedata at higher frequencies, and changes in R0 can be used to monitor changes in theextracellular fluid space (18). A tetrapolarelectrode arrangement was applied using the equipotential principle to standardize thelength of measured upper limb (19). Thevalidity has been determined to rc= 0.92 usinginter-limb ratio for BIS (R0 of unaffectedarm/R0 of affected arm; R0 resistance at zerofrequency) versus perometer (volume of

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affected limb/volume of unaffected limb) andintrarater reliability showed ICC = 0.96 (0.93to 0.98, 95% CI) (20).

All jewelry, watches, etc. were removed.Prior to the application of surface electrodes,the skin was cleaned with an alcohol wipe.With the patient lying supine on a bench witharms along her side, the electrodes werepositioned on the upper limbs, in line withthe ulna styloid and 5 cm distal of this spot,on the dorsum of the hands. One electrodewas placed on the dorsal surface of the rightfoot over the third metatarsal bone. Botharms were measured, and the resistance at afrequency of 0 Hz (R0) was estimated for each arm.

MRI: Images were obtained with thepatient in a supine position using a SiemensSymphony 1.5 T (Siemens Medical Systems,Erlangen, Germany) with a large flex coilcovering the upper arm. The field of view was175 mm in the registered axial plane toensure upper arm coverage. The images were

T1-weighted to enhance anatomical informa-tion (fat is bright, muscle is greyish and wateris dark). Twenty-five slices with a thicknessof 5 mm and a distance between the slices of1.5 mm were chosen representing the upperarm region between the axilla and elbow joint(Fig. 2). The slice at the level for lower m.deltoideus tendon attachment was identifiedas the first slice. The 11 consecutive sliceslocated distally to this first slice were subse-quently included in the study. A softwareprogram built in-house, using Matlab, wasused for image analysis. Each slice wassegmented into subcutaneous fat, muscle andbone/marrow. The pixel intensity distributionswere used to discriminate fatty tissue andwater in the subcutaneous fat. The volume ofdifferent tissues and water were calculatedalong the slice segments. Due to repositioningfactors and the diffuse border between themuscle and fat segment, the CV for intra-rater reliability are 2.5% in the subcutaneousfat segment and 4.7% in the muscle segment(own series in 4 patients).

Fig. 2. MRI slices with a thickness of 5 mm and a distance between the slices of 1.5 mm were chosen representingthe upper arm region between the axilla and elbow joint. The slices were localized using coronal (left) and axial(right) scout images. During evaluation, the slice presenting the lower m. deltoideus tendon attachment and the 11 slices distal of the first slice were included.

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Body weight was registered in kg on ascale with a precision of ±0.1 kg in order toverify changes in weight that could influencethe arm volume.

Upper extremity status

Isometric muscle strength device (IMSD):Isometric shoulder muscle strength wasmeasured with an electronic device connectedto a strain gauge (Steve Strong HB, Växjö,Sweden) with a measuring range of 0-1999Newton (N) and a precision of ±5N. A break-ing force technique was used, which has beenshown to be a reliable method (21). Thetechnique was applied for shoulder flexorsand adductors, and for elbow flexors andextensors, with the patient in a supine position.

Gripping strength was measured with aJamar Hydraulic Hand Dynamometer with arange of 0-90 kp/cm2. The instrument showshigh concurrent validity (r = 1.0) tested withcertified standard weights (22) and highintra/inter-rater reliability (ICC 0.85-0.98)(23). The measurements were performed withthe patient in a sitting position, and the armheld close to the body with a 90-degreesflexion of the elbow.

All muscle strength measurements wererepeated 3 times and the highest value wasregistered.

Disability of arm, hand and shoulderoutcome questionnaire (DASH): To assess the disability of the upper-extremity, theSwedish version of The Disability of the Arm,Shoulder and Hand questionnaire (DASH)was used (24). DASH is a self-administratedregion-specific instrument with a 30-itemscale developed to measure upper extremitydisability and symptoms. Each item is scoredon a 1 to 5-point scale. The total score of allitems are used to calculate a composite scorecalled the DASH score, ranging from 0 (nodisability) to 100 (most severe disability) (25).The Swedish version has been tested forcultural adaption and showed high internal

consistency (Cronbach alpha 0.96) and hightest-retest reliability (ICC 0.92) in patientswith upper-extremity orthopedic conditions(24). A 10-point difference in mean DASHscore is considered as a minimal clinicallyimportant change (26).

Log book

Adherence to the program was controlledevery fortnight by reviewing the log bookkept by each patient to register date, weights,use of compression sleeve and perceivedexertion on:

The Borg scale: A scale that measures thepatient’s perceived exertion. The scale rangesfrom 6 (minimum) to 20 (maximum), whereevery other step is provided with a verbalstatement (24).

Measurement procedure and safety

Arm volume (WDM), extracellular fluid(BIS), muscle strength (IMSD and grippingstrength), arm shoulder and hand disability(DASH) and body weight were measured atthe beginning of the control period and at thestart and end of the intervention (Fig. 1). Inaddition, arm volume was measured everyfortnight to check for volume increase > 5%compared to the total arm volume at the startof the intervention period, in case the patientdropped out and was offered immediatetreatment. Also, other symptoms of worseningof the lymphedema, like increased experienceof tension and heaviness in the arm orincrease of hand edema, were consideredreasons for drop-out. Images (MRI) of theupper arm were obtained in the first tenpatients at the beginning of the control periodand at the start and end of the intervention in order to determine whether any increase ofarm volume might be caused by an increasein muscle mass or in fluid.

No exercises were performed beforemeasurements on the same day as measure-ments were taken.

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Statistics

Descriptive statistics of variables includerates for binary variables and mean andstandard deviation for continuous variables.Pre-intervention variables for continuous datawere calculated as a mean of the pre- andpost-control period values.

Comparisons of pre-intervention versuspost-intervention values for continuousvariables were made using a non-parametrictest, the related samples Wilcoxon sign ranktest, for continuous variables, since thepatient group was small and values did notexhibit Gaussian distribution. All p-values are presented and a level of p<0.05 waschosen to indicate statistical significance.

All statistical analyses were performedusing IBM SPSS Statistics 21.

RESULTS

Feasibility: Retention and Adverse Events

Twenty-six patients were included in the

study. Three patients dropped out during the4-week introduction program, one due topneumonia, one because of pain in the armduring the first week of exercise, and one dueto swelling of the hand that later on developedinto an increased arm volume >5% comparedto the total arm volume at start of the intro-duction. The last two were considered to beadverse events related to the exercises.

Feasibility: Adherence

All patients fulfilling the 8-week interven-tion program (n=23) performed the minimumcriteria set for the intervention. Nineteen ofthe patients completed all 3 sessions weeklyfor all 8 weeks. Four patients performed 2sessions weekly for 1-3 weeks and 3 sessionsweekly for the rest of the 8 weeks.

Patient Characteristics

Table 1 shows baseline characteristics of the 23 patients that completed theintervention.

TABLE 1Patient Characteristics of the Total Intervention Group (n=23) and of the

Patients with Additional MRI (n=10)

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All of them had had axillary node dissec-tion. During the intervention, all patients hadbeen wearing a compression sleeve accordingto their usual procedures, which was at least daily. All patients also chose to wear acompression sleeve during exercise.

Images by MRI were obtained in the first10 patients from Skane University Hospital.This group (n=10) did not differ from thetotal group (n=23) concerning baselinecharacteristics (Table 1).

Lymphedema Status

All patients included in the intervention(n=23) had arm lymphedema with a meanlymphedema relative volume (LRV) of 19.6 ±11.7% at the start of the control period. At the start of the introduction, LRV was19.0 ± 11.7% (range 5.1-53.5%).

During the control period, there were nosignificant changes for the TAV of each arm,LAV or LRV measured by WDM, or for theBIS ratio. After the intervention there was areduction of the LAV, LRV and a tendency

towards reduction of BIS ratio (p=0.069)compared to at the start of the intervention.No significant change of TAV was found inthe lymphedema arm or in the healthy arm(Table 2).

Mean ± SD body weight was 71.4 ± 10.0kg for all patients and 71.7 ± 10.1 for theMRI group at start of the control period anddid not change during the intervention.

Similar to the total group (n=23), theMRI group (n=10) showed a reduction of BIS ratio and a tendency to reduction in LAV and LRV after intervention. The resultsalso showed a tendency towards reduction of fat (p=0.067) in the upper arm of botharms after intervention (Table 3).

Upper Extremity Status

The shoulder and arm strength did notchange during the control period butincreased significantly in all four shoulderand arm muscle groups after intervention,and showed a tendency towards an increasein gripping strength (p=0.059). No changes

TABLE 2Muscle Strength, DASH Score, Total Arm Volume, Excess Volume (n=23) and Tissue Fluid (n=16) in Patients With Breast Cancer-Related Arm Lymphedema

at the Start and End of the 12-Weeks Intervention Program

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were found in the DASH score afterintervention (Table 2).

Log Book

The mean ± SD (range) weight resistanceduring the introduction period (week 3) was1.6 ± 0.6 (0.5-3.0) kg for long-lever arm(exercise I and II) and 2.3 ± 0.8 (1.0-4.0) kgfor short-lever arm (exercise III and IV) withthe mean rating of perceived exertion beingabout 13 (somewhat hard) on the Borg scale.During the last week of the interventionperiod, the mean ± SD (range) weightresistance levels were 3.0 ± 1.0 (1.0-5.5)kilograms for long-lever arm and 4.1 ± 1.7(2.0-9.0) kilogram for short-lever arm. Therating of perceived exertion on Borg’s scale

the last week of intervention approached 17 (very hard) and was rated in mean 16.4 ± 0.6 (range 13-19) during the 8-weekfull intervention.

DISCUSSION

In this pilot study we found that a 12-week home-based weight-lifting programis feasible and relatively safe. A significantincrease of shoulder and arm muscle strengthwas found and results also supported otherstudies showing that weight lifting exercisescan be performed without worsening of thelymphedema. Results also indicate thatregular exercise may even reduce excessvolume and fat tissue.

TABLE 3Total Arm Volume and Excess Volume Measured by Water Displacement Method,

Tissue Fluid Measured by Bioimpedance and Fat, Water and Muscle Measured by MRI in Patients with Breast Cancer-Related Arm Lymphedema

at the Start and End of Intervention (n=10)

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Recruitment and Subjects

The recruitment of the patients was made through the register of twoLymphedema Units assuring that a variety of patients fulfilling the inclusion criteriawere approached, not only those particularlyinterested in exercise, but also those whoprovided different reasons for not takingpart. We believe this procedure is more likelyto reflect the total breast cancer populationthan recruitment through, for example,advertisement.

One of the inclusion criteria was an ageof less than 70 years. Some studies haveshown that older persons can exercise andincrease their strength with no problems (28).However, our experience from prior studies isthat older patients are more likely to drop-out. This may be because breast cancerpatients also suffer from other impairmentslike stiffness and pain, which sometimesreduces their ability to carry through aphysically taxing study. However, this doesnot mean that elderly breast cancer patientscannot do muscle strengthening exercises, but rather, the exercises should be adjusted tosuit individual capacity just as in healthyelderly persons.

Feasibility

As we could not foresee the feasibility ofthe planned study, both regarding theadministration and the number of patientsbeing able to complete the interventionprogram, we chose to perform a pilot study.However, we also chose to include a controlperiod, meaning that the patients were theirown controls during two weeks. The aim ofthis procedure was mainly to assure thatthere was no bias from the normal biologicalvolume fluctuations (29) and make sure thata steady arm volume could be maintained.This kind of design does not reach thescientific level of a randomized controlledtrial, but may ascertain that no major biaswill interfere with the results.

Feasibility is shown both in that it can besatisfactorily administered and that thepatients can be recruited and retained withhigh adherence (100%) to the intervention.The high adherence to the interventionprogram indicated that there were no majorproblems carrying it through for the patients,but the patients’ experiences of the programadministration and intervention were notevaluated. However, possible advantages canbe the ability to choose when and where toexercise, and not having to perform in agroup setting or in any way together withothers. This was also supported by the factthat only two out of eleven patients whodeclined to take part claimed that lack oftime was their reason. The rest of thesepatients (n=9) did not have time to attend tothe measurement procedure but may verywell have been able to carry through theintervention.

The safety of the program is relativelyhigh, and no adverse events were reportedduring the full intervention period. However,during the introduction period, starting witha load of 50% of 10RM and ending withcompleted 10RM, two adverse eventsappeared. One was an increased swelling ofthe hand. The other was aching in the entireaffected arm when repeating arm lifting withweights suggesting a neurological problem,however, this was never examined. These twoevents indicate that a regular follow-up of thepatients should be done in particular duringthe first weeks of the program. Though basedon a small amount of material, we stillrecommend that special focus be put on smallsigns of increasing lymphedema, in case thepatient could be recommended to come for acheck-up every fortnight, similar to thisstudy. If there are no signs of increasinglymphedema or even a reduction during thefirst weeks, the frequency of follow-upsfurther on might be less.

Lymphedema Status and Subcutaneous Fat

Swedborg et al (29) has demonstrated

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that, without a compression garment, there isnormal biological fluctuation of the healthyarm volume over a fortnight. To be able tokeep a steady volume during the study periodthe women were wearing a new compressiongarment, not only during the control andintervention period but also at least onemonth prior to the start of the study. Thisprocedure was applied to assure that old,insufficient compression garments would notinfluence the arm volume results during thestudy. Results show that there were nosignificant changes in arm volume during thecontrol period in the lymphedema arm or inthe healthy arm, indicating that volumechanges were not influenced by insufficientgarments or normal fluctuations.

Images (MRI) of the upper arm wereobtained in order to determine whether anyincrease of arm volume during interventionmight be caused by increase in muscle massor fluid. As no significant increase in armvolume was found in the first ten patients nofurther examinations were performed due topractical reasons (Table 3).Upon analysis ofimages, a tendency towards reduction of fatin both arms was found, but there was nochange in body weight to support this finding.However, this discrepancy could possiblyhave been clarified by a RCT, adequatelypowered. Still, even more important seems to be the need for a test of validation andreliability in MRI measurements forlymphedema status, and responsiveness tolymphedema treatment outcome.

Both arms increased (not significantly)after the intervention; however, the healthyarm increased more than the edematous arm,resulting in a significant reduction of excessvolume (Table 2). It is hard to determinewhat made the arms increase, as MRI did notshow any increase of muscle mass or water,but a reduction of fat on both sides that mayhave reduced the arm volume. Though MRIis used for diagnosis of lymphedema, test ofvalidity for measurement of water/tissue fluidhas not been performed. However, in thisstudy it was possible to show a difference in

water content between the affected and non-affected arm (p=0.007). An intra-raterreliability test was also made within thisstudy. However, it only included 4 patients,and results from the test may therefore belimited. Nor has the responsiveness of MRI to detect changes in water/tissue fluid afterintervention been evaluated.

Whatever the cause of the increase, the lesser increase in the edematous armcompared to the healthy arm may have beendue to the compression sleeve, and the reduc-tion of excess volume may not have occurredif the sleeve had not been worn at least dailyand also during the exercise sessions.

The tendency towards less subcutaneousfat in the arms, but without body weightreduction, may indicate a local fat reduction.It has been discussed for many years whetherspecific exercises can reduce local adiposetissue depots, i.e., induce a “spot reduction”of adipose tissue, and thus modify fatdistribution (29,30). Olsen and Edelstein (30)found a decrease in skinfold thickness of thetrained arm compared to the untrained arm.The local fat reduction was supported inanother, more recent study (31) where malesubjects perform single-leg extensions withlight weight for 30 consecutive minutes. An increase in blood flow and lipolysis wereobserved in the exercising leg when comparedto the resting leg. The study suggested thatduring exercise, body fat is preferentiallyused from the area being trained (31). If“spot reduction” can be established, it couldmean a lot for the effort to try to reduceinduration of fat found in long-standinglymphedema, otherwise requiring surgicaltreatment (32). In that case a RCT examiningthe influence of weight-lifting on local fattissue in lymphedema patients could beperformed.

Upper Extremity Strength and Disability

The increase of strength in all musclegroups measured after intervention was aclear indication that the load of weights had

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been high enough. This was supported by the patient’s own experience of exertionassessed on the Borg scale as the mean valueat the end of the intervention was about 17,meaning the patients experienced the exertionas very hard. The experience of exertion andknowledge of the value assigned on a scale isinformative to patients, because it providesthem with evidence as to the size of the loadthat is attainable for them in daily life.However, it is essential for safety thatpatients start at an exertion level lower thantheir peak attainable level and then worktheir way up, which is the same advice givento inactive but otherwise healthy persons.

In a systematic review of exercise inpatients with lymphedema it was stated thatstrong evidence is available regarding thesafety of resistance exercise without risk ofdevelopment or exacerbation of breast cancer-related lymphedema (7). However, to ourknowledge, Schmitz et al (33) are the onlygroup that has published data on the load ofweights. Their protocol included a gradualincrease in weight on both arms by doingbench presses with a mean weight of 24 kp(53 lbs) during 6 months. This weight issimilar to our findings from correspondingweight-lifting for elbow extension in a supineposition. The lifting was one-handed, that isone dumbbell in each hand, and showed amean of 15 kp for each arm after 12 weeks of intervention. Both studies showed asignificant increase of strength without anydeterioration of the arm lymphedema.However, the study by Schmitz et al (33) was a large (n=141) randomized study whilethe present study was a pilot study. Still, the present pilot study provides data forrecommendations to the patients concerningweight resistance level. Compared to thestudy by Schmitz et al (33), the present studyalso shows that the same amount of weightscan be distributed at home without going to a special location, like a gym.

Another interesting finding is that gripstrength increased though the hand and wristmuscle were not the target for the special

exercises. However, dumbbells need to bestabilized by hand and wrist in particular bythe exercises with long lever arm, andgripping strength may have improved by thisneed of stabilization.

All patients chose to wear garments. Wedid not evaluate why they made this choicebut a former study found that many patientsreported that the sleeve gave support whenweight-lifting (11).

The DASH score was found to be verylow, with a mean of 11.4 and maximum range at 35 at the start of the intervention,compared to a group of breast cancer patients(n=50) also with axillary node dissection andarm lymphedema with a score of 36.6 (34).The difference may be explained by theexclusion criteria of the present study notaccepting e.g., patients with pain. Because ofthe low DASH score, the potential to improvethe DASH score was limited. However,several patients expressed spontaneously thatthey felt stronger in the shoulder and arm,and some used the expression “my arm feelsnormal again.”

In practice, it is likely that the mostimportant issue for the patients is to focus onthe 10RM system and to be well-informedabout increasing resistance when they areable to do more. This should automaticallylead to the experience of high exertion. Theamount of weights will then turn out to be ofless importance, but can provide stimulationand an individual challenge.

CONCLUSION

The findings of this pilot study show that a home-based weight-lifting program for patients with breast cancer-relatedlymphedema is feasible and relatively safe.The results of the program show increasedarm and shoulder strength, without anydeterioration of the lymphedema but a smallreduction of the excess volume and, in asmaller group, a tendency towards reductionof fat tissue in the upper arm. A regularfollow-up with control of lymphedema

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symptoms is recommended at least during the first weeks of the program.

The findings can be used to inform thedevelopment of RCT, adequately powered, toevaluate home-based compared to supervisedexercise programs with a range of outcomesincluding shoulder and arm strength, armlymphedema status and local subcutaneousfat distribution.

ACKNOWLEDGMENTS

This study was supported by grants from the Swedish Cancer Foundation. Manythanks to all the patients who volunteered toparticipate in the study.

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Karin Johansson, RPT, Assistant Professor, Lund UniversityLymphedema Unit, Dept. of OncologySkane University Hospital221 85 Lund, SwedenTel: +46 46 172281, +46 706167593Fax: +46 46 171548E-mail: [email protected]

Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY.