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ARTICLE The effects of a 6-month resistance training and dried plum consumption intervention on strength, body composition, blood markers of bone turnover, and inflammation in breast cancer survivors1 Emily Simonavice, Pei-Yang Liu, Jasminka Z. Ilich, Jeong-Su Kim, Bahram Arjmandi, and Lynn B. Panton

Abstract: The purpose of this study was to examine the effects of resistance training (RT) and dried plum (DP) consumption on strength, body composition, blood markers of bone, and inflammation in breast cancer survivors (BCS). Twenty-three BCS (RT, n = 12; RT+DP, n = 11), aged 64 ± 7 years, were evaluated at baseline and after 6 months of intervention on the following: muscular strength (chest press and leg extension) via 1-repetition maximums (1RMs); body composition, specifically bone mineral density (BMD) by dual energy X-ray absorptiometry; biochemical markers of bone turnover (bone-specific alkaline phosphatase (BAP), tartrate resistant acid phosphatase (TRAP-5b)); and inflammation (C-reactive protein (CRP)). Target RT prescription was 2 days/ week of 10 exercises, including 2 sets of 8–12 repetitions at ⬃60%–80% of 1RM. RT+DP also consumed 90 g of DP daily. There were no baseline differences between groups or any group-by-time interactions for any of the variables. BCS increased upper (p < 0.05) (RT: 64 ± 14 to 80 ± 17 kg; RT+DP: 72 ± 23 to 91 ± 20 kg) and lower (p < 0.05) (RT: 69 ± 20 to 87 ± 28 kg; RT+DP: 78 ± 19 to 100 ± 21 kg) body strength. Body composition and BMD improvements were not observed. TRAP-5b decreased in the RT group (p < 0.05) (4.55 ± 1.57 to 4.04 ± 1.63 U/L) and the RT+DP group (p = 0.07) (5.10 ± 2.75 to 4.27 ± 2.03 U/L). Changes in BAP and CRP were not observed. RT was effective for improving biochemical markers of bone turnover and muscular strength in BCS. A longer and higher intensity intervention may be needed to reveal the true effects of RT and DP on body composition and biochemical markers of inflammation. Key words: resistance training, bone health, inflammation. Résumé : Cette étude se propose d’examiner les effets de l’entraînement contre résistance (« RT ») et de la consommation de pruneaux (« DP ») sur la force musculaire, la composition corporelle, les marqueurs sanguins du tissu osseux et l’inflammation chez les survivants du cancer du sein (« BCS »). Vingt-trois BCS (RT, n = 12; RT+DP, n = 11) âgées de 64 ± 7 ans participent a` une évaluation des variables suivantes au début et après le programme d’intervention d’une durée de 6 mois : force musculaire (« 1RM », développé pectoral et extension des jambes), composition corporelle et plus spécifiquement la densité minérale osseuse (« BMD ») par absorptiométrie a` rayons X en double énergie, marqueurs biochimiques du renouvellement du tissu osseux (phosphatase alcaline spécifique aux os (« BAP »), phosphatase acide résistant aux tartrates (« TRAP-5b »)) et l’inflammation (protéine C-réactive (« CRP »)). Le programme RT consiste principalement en 10 exercices comprenant deux séries de 8–12 répétitions a` ⬃60–80 % 1RM, et ce, a` raison de 2 fois par semaine. Le groupe RT+DP consomme en plus 90 g de DP tous les jours. Toutes les variables ne présentent ni différences entre les groupes au début du programme, ni d’interaction groupe-temps. On observe chez les BCS une augmentation de la force du haut du corps (p < 0,05) (RT : de 64 ± 14 a` 80 ± 17 kg; RT+DP : de 72 ± 23 a` 91 ± 20 kg) et du bas du corps (p < 0,05) (RT : de 69 ± 20 a` 87 ± 28 kg; RT+DP : de 78 ± 19 a` 100 ± 21 kg). On n’observe aucune amélioration de la composition corporelle et de la BMD. On observe une diminution de TRAP-5b dans le groupe RT (p < 0,05) (de 4,55 ± 1,57 a` 4,04 ± 1,63 U/L) et dans le groupe RT+DP (p = 0,07) (de 5,10 ± 2,75 a` 4,27 ± 2,03 U/L). On n’observe aussi aucune modification de BAP et de CRP. Le programme RT est efficace pour améliorer les marqueurs biochimiques du renouvellement du tissu osseux et la force musculaire chez les BCS. Il faut peut-être prolonger et intensifier le programme d’intervention pour révéler les effets réels de RT et de DP sur la composition corporelle et les marqueurs biochimiques de l’inflammation. [Traduit par la Rédaction] Mots-clés : entraînement contre résistance, santé osseuse, inflammation.

Introduction Over 1.6 million new cases of cancer were projected to be diagnosed in the United States in 2013, and of these diagnoses, it was estimated that 234 580 would be breast cancer (Siegel et al. 2013). While the prognosis of breast cancer is improving, breast cancer

survivors (BCS) are often left to deal with the numerous adverse side effects caused by the cancer itself and the treatments of the cancer. Among the long list of unfavorable side effects of cancer treatments are body composition changes, specifically decreased bone mineral density (BMD), decreased lean body mass, and increased fat mass. A loss of BMD can lead to osteopenia and (or)

Received 25 June 2013. Accepted 4 September 2013. E. Simonavice. School of Health and Human Performance, Georgia College and State University, Campus Box 112, Milledgeville, GA 31061, USA. P.-Y. Liu. School of Nutrition and Dietetics, University of Akron, Schrank Hall South 210M, Akron, OH 44325, USA. J.Z. Ilich, J.-S. Kim, B. Arjmandi, and L.B. Panton. Department of Nutrition, Food and Exercise Sciences, Florida State University, Tallahassee, FL 32306, USA. Corresponding author: Emily Simonavice (e-mail: [email protected]). 1This paper is a part of a Special Issue entitled The role of diet, body composition, and physical activity on cancer prevention, treatment, and survivorship. Appl. Physiol. Nutr. Metab. 39: 730–739 (2014) dx.doi.org/10.1139/apnm-2013-0281

Published at www.nrcresearchpress.com/apnm on 23 September 2013.

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osteoporosis, ultimately increasing the susceptibility to fractures. This is of notable concern as a previous report showed significant increases in mortality following vertebral and hip fractures (Cauley et al. 2000). BCS are vulnerable to BMD loss because of the direct and indirect effects of chemotherapy and a common sex-hormone suppressant therapy known as aromatase inhibitors (AIs). Chemotherapy is reported to directly affect the number and thickness of osteoblasts (Friedlaender et al. 1984); whereas both chemotherapy and AIs are reported to indirectly affect BMD possibly by lowering the amount of estrogen produced in the body (Pfeilschifter and Diel 2000; Ramaswamy and Shapiro 2003). Specifically, during a 12-month chemotherapy regimen, women experienced a loss of approximately 7% in lumbar spine BMD (Shapiro et al. 2001). Similar detrimental effects can occur from 1 to 5 years with the use of AIs, with a reported loss of BMD up to 7.2% during the treatment period (Brufsky 2007). Other body composition changes that BCS experience are decreases in lean body mass and increases in fat mass, which may be a result of decreased levels in physical activity reported during and after cancer-related treatment (Demark-Wahnefried et al. 2001; Irwin et al. 2004). These unfavorable body composition changes, particularly the increases in fat mass, may influence the prognosis of BCS by promoting a state of chronic inflammation, as seen in obese individuals (Alokail et al. 2009). Elevated inflammation markers in BCS have been associated with an increased risk of developing cardiovascular disease and (or) metabolic disease as well as a reduced survival time (Pierce et al. 2009; Thomson et al. 2009). These findings suggest that cancer-related treatments may directly and indirectly account for the undesirable body composition changes that are seen in BCS and ultimately may affect their prognosis and survival. Nonpharmaceutical approaches play a vital therapeutic role in the success of the cancer recovery process. Proper diet and exercise are often stressed by health and wellness professionals for the treatment and prevention of detrimental changes in body composition that occur in middle-aged and older adults. Specifically, in healthy populations, resistance exercise training (RT) and dried plum (DP) consumption have shown to be promising therapies to attenuate many of the previously mentioned BMD changes that BCS encounter (Arjmandi et al. 2002; Hooshmand et al. 2011; Simkin et al. 1987; Vincent and Braith 2002). The efficacy of these nonpharmaceutical therapies to modulate body composition, specifically BMD, in BCS has not been well researched. However, the positive effects of RT on bone health in healthy postmenopausal women have been noted by improvements in biochemical indices of bone formation, decreases in biochemical indices of bone resorption (Bemben et al. 2000; Humphries et al. 1999; Klentrou et al. 2007), as well as improvements in total and regional BMD (Simkin et al. 1987; Vincent and Braith 2002). These improvements in BMD have been shown to occur in a little as 6 months of RT (Bemben et al. 2000; Simkin et al. 1987). Similarly, DP has been shown to improve biochemical markers of bone turnover and may be an effective means for improving BMD in postmenopausal women (Arjmandi et al. 2002; Hooshmand et al. 2011). Specifically, Arjmandi and colleagues found that DP consumption dose-dependently elevated circulation levels of IGF-I (Arjmandi et al. 2001). IGF-I is produced by bone cells at the local level, and acts to stimulate osteoblasts, increase collagen synthesis, and enhance matrix apposition (Pfeilschifter et al. 1990; Radcliff et al. 2005). Therefore, the mechanism of action for decreasing bone loss through DP consumption can be attributed to an increased bone formation as opposed to the suppression of bone resorption. In addition to the bone health benefits, RT has been shown to reduce systemic inflammation levels in obese postmenopausal women in as little as 12 weeks (Phillips et al 2012). Although the efficacy of RT and DP to improve the bone health and inflammation markers of BCS has not been thoroughly

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investigated, studies have shown that both cancer patients and cancer survivors can experience improvements in lean mass and fat mass as a result of RT (Cheema and Gaul 2006; Courneya et al. 2007). Because of the scant research that has been conducted with BCS examining the effectiveness of RT to improve BMD, and the complete lack of research investigating the effectiveness of DP to improve BMD and inflammation levels in BCS, an investigation of these 2 nonpharmacological interventions to improve the body composition and inflammation levels of BCS is warranted. Therefore, the primary aims of the current investigation were to determine and compare the efficacy of a 6-month intervention with RT and a combination of RT and DP on improving body composition (BMD, lean mass, and fat mass) and muscular strength in postmenopausal BCS and examine the effects of RT and a combination of RT and DP on biochemical indices of bone turnover (markers of resorption and formation) and inflammation. Based upon the reviewed literature conducted in healthy postmenopausal women it was hypothesized that both groups would improve total and regional (lumbar spine, femur, and forearm) BMD, experience increases in lean body mass and decreases in fat body mass, and demonstrate increases in skeletal muscular strength. Additionally, it was hypothesized that the biochemical analyses for both groups would reveal increased levels of bone formation markers, decreased levels of bone resorption markers, and decreased levels of inflammation markers, with the RT+DP group having the most improvements in these areas.

Materials and methods Participants Postmenopausal female BCS (stages 0–III), having completed treatments at least 6 months prior to beginning the study were recruited. Participants currently taking or who had completed hormone suppressant therapies were eligible to participate in this study. Participants still receiving hormone suppressant therapies were eligible for the study because after initial treatments are completed, hormone suppressant therapies are typically prescribed for an additional period of 3 to 5 years. Excluding women still taking hormone suppressant therapies would have significantly decreased the number of women eligible for the study. Participants already participating in vigorous exercise programs at baseline of the study and (or) those with uncontrolled hypertension (≥160/100 mm Hg), uncontrolled diabetes, or uncontrolled heart disease were excluded. Procedures Prior to baseline testing all participants attended an informational orientation during which time the study coordinator reviewed the time commitment of the study, explained the study protocol, and gave out a physician consent form for participants to take to their primary health care providers to be evaluated for participation in the study. Demographic and medical history questionnaires were also administered for participants to complete and bring to their first visit. Written informed consent was obtained from all participants prior to testing. This study was approved by the Institutional Review Board at Florida State University. Baseline testing for all participants occurred over the course of 2 separate visits to the laboratory, each visit occurring between 0700 and 1100 hours. During the first laboratory visit, fasted blood draws were taken in the amount of 20 mL under sterile conditions for the purposes of measuring serum biochemical markers of bone formation (bone-specific alkaline phosphatase (BAP)), bone resorption (tartrate-resistant acid phosphate (TRAP-5b)), and inflammation (C-reactive protein (CRP)). Serum was separated from whole blood by centrifugation (4 °C for 15 min at 1000g) and aliquots were kept frozen at –80 °C. Biochemical assays and procePublished by NRC Research Press

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dures included duplicate analysis of each sample; when test results did not meet the manufacturers’ standards (or better) for control variables, samples were re-run. Bone resorption, bone formation, and inflammation assays included high and low controls, as well as standards that were run with each assay. Inter-assay coefficients of variation (CVs) were determined from the individual sets of duplicates. Samples having a CV higher than >20% were deemed unacceptable and were not analyzed (Kivlighan et al. 2004; Reed et al. 2002). All blood samples were analyzed at the conclusion of the 6-month intervention. Height and weight were measured via the use of a wall-mounted stadiometer and a digital scale, respectively (Seca Corporation, Hanover, Md., USA) and body mass index (BMI) was calculated. Body composition and BMD of the total body and regional areas of the lumbar spine, femur, and forearm were measured noninvasively via dual energy X-ray absorptiometry (DXA) with the use of the iDXA scanner (GE Healthcare Inc., Madison, Wis., USA). A total of 4 scans were performed on each participant: (i) anteroposterior (AP) view of the total body with the participant lying supine; (ii) AP view of the lumbar (L1–L4) spine with the participant lying supine with hips and knees supported at a 90° angle; (iii) AP view of the right and left femur with the participant lying supine with thigh internally rotated (femur neck and total femur were analyzed); and (iv) posteroanterior view of the right and left forearm (including ulna, radius, and both ultradistal and 33% sites) with the participant lying supine. Testing was completed according to the manufacturer’s instructions and specifications by a certified X-ray technician. Following the body composition analyses, both upper and lower body strength were assessed using the chest press and leg extension exercises, respectively (MedX; MedX Holdings Inc., Ocala, Fla., USA). After a warm-up, participants were progressed towards the maximum weight that they could lift 1 time through a full range of motion to achieve a 1-repetition maximum (1RM). The 1RM tests for both upper and lower body were obtained within a 10- to 15-min time frame after the initial warm-up set and were performed according the guidelines for strength testing as outlined by the American College of Sports Medicine (ACSM) (Thompson et al. 2010). On the second baseline visit, which occurred 1 week later, participants had their hip and waist circumferences assessed and had their muscular strength measures repeated. Waist circumference measures were taken at the narrowest part of the torso superior to the hip and inferior to the most distal rib. Hip circumference measures were taken at the greatest gluteal protuberance while the participant stood upright with feet together. Circumference measures were taken at least twice at both anatomical sites using a Gulick fiberglass measuring tape with a tension handle (Creative Health Products Inc., Ann Arbor, Mich., USA). If the readings were not within 5 mm of each other, an additional measure was taken until the 2 readings were equal to or less than 5 mm of difference (Armstrong et al. 2009). Maximal strength tests were verified by repeating the 1RM as outlined in day 1 of baseline testing. The highest measurement for the upper and lower body from the 2 days of testing was considered to be the 1RM and was used for calculating the resistance training exercise prescription. At baseline, both groups were given a pedometer to log their step counts. For 1 randomly assigned week for each month of the 6 months, all participants were asked to record their steps daily. This was done to try to account for activity levels outside of the laboratory that may have influenced the outcome variables. All baseline measurements were repeated at 3 and 6 months with the exception of DXA measurements, which were only repeated at the 6-month time point in attempt to limit radiation exposure to the participants. Muscular strength assessments via 1RM were repeated monthly to assure the most appropriate exercise prescription throughout the intervention.

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Intervention After the completion of baseline testing, each participant was stratified into 1 of 2 treatment groups: (i) resistance exercise training (RT) or (ii) RT and DP consumption (RT+DP). Stratification occurred using the following variables: breast cancer stage, cancer treatment received, race, age, weight, baseline forearm BMD, and baseline chest press 1RM. Each participant, regardless of treatment, was instructed to consume twice daily a provided daily vitamin/mineral supplement containing 450 mg calcium and 800 IU of vitamin D. Each month participants were rationed the appropriate number of calcium/vitamin D pills to last for 1 month. At the end of each month, remaining pills were collected to calculate adherence for calcium/vitamin D use. Participants were requested to replace their current supplements with the ones that were provided. Additionally, for the duration of the investigation, participants were asked to avoid any major dietary and physical activity changes outside of the requested changes necessary for completion of the study. For the length of the study, both groups completed 6 months of supervised resistance exercise training. On 2 nonconsecutive days each week, the participants performed 2 sets of 8–12 repetitions of 10 resistance exercises for the upper and lower body. Exercise machines included the MedX (MedX Holdings Inc.) chest press, leg press, leg extension, biceps curl, triceps press down, overhead press, seated row, leg curl, abdominal crunch, and lower back hyperextensions. Exercise intensities for the chest press and leg extension were calculated as a representation of upper body and lower body intensity, respectively. When assessing the intensity (percentage of 1RM) for a particular 4-week period, the 1RM test just prior to the 4-week period was used for calculating percentage of 1RM lifted. For example, baseline 1RM values were used when calculating the intensity at which the participants exercised during weeks 1–4. Training sessions began at approximately 60% of each participant’s 1RM and intensity was slowly progressed to an intensity not exceeding 80% 1RM throughout the 6 months. Once 12 repetitions could be completed with proper form, the weight was increased by approximately 10%. The resistance exercise program followed the recommendations of the ACSM (Feigenbaum and Pollock 1999). During each resistance exercise session, participants performed a warm-up by walking for approximately 5 min, and concluded their session by performing stretches that targeted all the major muscle groups. For the duration of the study, the RT+DP group was instructed to consume 3 packets (30 g each) of DPs, for a total of 90 ± 6 g of DPs daily (equating to approximately 9–12 DPs). The participants in the RT+DP group were advised to cut 300 kcal from their “normal” diet to account for the additional kilocalories consumed from the DPs. Each month the participants were rationed the appropriate number of DP packets to last for 1 month. At the end of each month, remaining packets of DPs were collected to calculate adherence for DP consumption. Statistical analysis A group-by-time interaction effect, with an effect size of 0.49, maintaining ␣ = 0.05 and 1-␤ = 0.80, indicated that a sample size of 14 participants per experimental group was required to detect changes in spinal BMD based on a previous finding by Khort et al. (1997). All analyses were performed using the SPSS statistical package (version 18; SPSS Inc., Chicago., Ill., USA). Descriptive statistics (means, standard deviations) were calculated for all variables. An independent t test was used to analyze baseline measures between the 2 groups. Dependent variables of body composition (bone, muscle, fat), strength, and blood markers, were analyzed by a 2-way (group × time) repeated measures ANOVA with repeated measures performed on the time factor. When interactions were significant, independent t tests were used to compare between group values. All significance was accepted at p ≤ 0.05. In cases of sphericity violations, Greenhouse–Geisser adjustment Published by NRC Research Press

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was used to test the effects of experimental condition and time interactions on the dependent variables. All data are presented as means ± standard deviations.

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Results Participant characteristics A total of 51 BCS potential participants inquired about the study; 10 declined participation after initial screening and 9 did not meet qualifying criteria. Thirty-two participants completed baseline testing; however, 5 women did not return after initial testing. Thus, 27 participants were stratified into the 2 groups. Fourteen women were assigned to the RT group and only 12 women were able to complete the intervention. One participant developed uncontrolled hypertension during the eighteenth week of the study and her physician would not grant clearance to remain in the study. The second participant, during the eighth week of the study was diagnosed with a reoccurrence of cancer that metastasized into her bones and was not allowed to continue with the study. Thus, 12 participants from the RT group were included in data analysis. Thirteen women were assigned and completed the RT+DP group; however, over the course of the study, 2 women had less than 80% compliance to the DPs because of gastrointestinal distress and were excluded from analyses, thus 11 women were used for data analysis. See Fig. 1 for progression of participants through study. Participants in the 2 treatment groups shared similar baseline characteristics in terms of age (RT: 64 ± 5 years; RT+DP: 64 ± 7 years), height (RT: 162.8 ± 5.6 cm; RT+DP: 163.8 ± 7.5 cm), weight (RT: 71.3 ± 14.0 kg; RT+DP: 71.9 ± 10.4 kg), and BMI (RT: 26.8 ± 5.0 kg/m2; RT+DP: 26.9 ± 3.7 kg/m2). The majority of the participants, 87% (n = 20), were Caucasian, while the remaining 13% (n = 3) were African American. The African-American women were dispersed between the RT (n = 2) and RT+DP (n = 1) groups. Participants in the 2 treatment groups also shared similar characteristics in terms of breast cancer diagnosis history and treatment strategies. Table 1 provides a detailed listing of the cancer diagnosis and treatment histories of the participants. Compliance to intervention Adherence to vitamin and mineral supplements in the RT and RT+DP groups were 89% ± 13% and 95% ± 4%, respectively. There were no differences in the level of adherence to resistance exercise attendance, as well as DP consumption (RT+DP group). The RT group attended 95% ± 9% of exercise sessions, while the RT+DP group attended 98% ± 4% of exercise sessions. In the RT+DP group, adherence to DP consumption was 94% ± 5%. There was no statistically significant difference for step count at baseline (RT: 6715 ± 3307 steps/day; RT+DP: 6525 ± 3841 steps/day, p = 0.90) or at 6 months (RT: 5720 ± 2769 steps/day; RT+DP: 6350 ± 3266 steps/day, p = 0.62), and there were no significant changes in step counts within groups throughout the study. Intervention Both intervention groups displayed similar progression for upper and lower body exercises throughout the 6-month intervention. No group-by-time interactions were observed for weight lifted for any of the resistance training exercises. There were no significant differences between groups, at any time point, for weight lifted for any of the upper body exercises (chest press, seated row, triceps press down, biceps curl, and overhead press). For weeks 1–4, both groups exercised at intensity less than the target intensity (60%–80% 1RM); with the RT group achieving an intensity of 53% ± 12% 1RM and the RT+DP group achieving 52% ± 5% 1RM. Beginning in weeks 5–8, both groups achieved an exercise intensity of ≥60% 1RM and continued to maintain compliance to the study design of 60%–80% 1RM for the remaining weeks of the intervention. Although the target repetition range

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for the study was 8–12, both groups executed 11–12 repetitions for all upper body exercises throughout the 6 months. With the exception of weeks 17–20 and weeks 21–24 for weight lifted on hamstrings curl, there were no significant differences between groups, at any time point, for any of the lower body exercises (leg extension, hamstrings curl, leg press, abdominal crunch, back extension). At the 2 significant time points (17–20 weeks and 21–24 weeks) for weight lifted on the hamstrings curl exercise, the RT+DP group lifted significantly heavier weights than did the RT group. Within group analyses showed that both groups exhibited a significant steady progression of weight lifted throughout the 24 weeks on the remaining lower body exercises, with the exception of back extension. For the back extension exercise, both groups began using only their body weight, with no extra weight being added. The RT group did not significantly increase weight lifted for the back extension exercise at any time point throughout the intervention. Only at weeks 21–24 did the RT+DP group significantly increase weight lifted on the back extension exercise compared with baseline, concluding with 2 ± 2 kg. For weeks 1–4, both groups exercised at an intensity less than the target intensity (60%–80% 1RM); with the RT group achieving an intensity of 52% ± 7% 1RM and the RT+DP group achieving 50% ± 2% 1RM. Beginning in weeks 5–8, the RT group achieved an exercise intensity of 61% ± 6% 1RM and continued compliance to the study design of 60%–80% 1RM for the remaining weeks of the intervention. The RT+DP group did not achieve an exercise intensity of >60% 1RM until weeks 9–12, but thereafter maintained compliance to the study design of 60%–80% 1RM for the remaining weeks of the intervention. The target repetition range for the study was 8–12 repetitions; both groups performed 11–12 repetitions throughout the 6 months for leg extension, hamstrings curl, and leg press. Both groups performed a range of 13–24 repetitions and 12–15 for the abdominal crunch and back extension, respectively. At no point in the study did the participants exercise over 69% of their previous 4-week 1RM for upper or lower body. Muscular strength Participants from both the RT and the RT+DP groups demonstrated similar baseline strength values for chest press and leg extension strength measurements. Group-by-time interactions were not observed for the upper body (p = 0.72) or lower body (p = 0.49) muscular strength variables. Similar to baseline values, there were no significant differences between groups at the 3- or 6-month time points. There was a significant time effect observed for chest press (F[2,21] = 40.62, p ≤ 0.01, effect size (ES) = 0.659) and leg extension (F[1.246,23] = 51.919, p ≤ 0.01, ES = 0.722). RT and RT+DP groups both exhibited significant increases in the chest press and the leg extension over the course of the study. The RT group experienced a significant (p = 0.03) 16% increase in chest press strength from baseline to the 3-month time point, and a further significant (p = 0.01) 13% increase from month 3 to month 6. Overall, the RT group significantly (p < 0.01) improved their chest press strength by 24% from baseline to month 6. Similarly the RT+DP groups exhibited a significant (p < 0.01) 16% increase in chest press strength from baseline to the 3-month time point, as well as a further significant (p = 0.05) 9% increase from month 3 to month 6. Overall, the RT+DP group significantly (p < 0.01) improved their chest press strength by 26% from baseline to month 6. The RT group experienced a significant (p = 0.01) 16% increase in leg extension strength from baseline to the 3-month time point, and a further significant (p < 0.01) 9% increase from month 3 to month 6. Overall, the RT group significantly (p < 0.01) improved their leg extension strength by 25% from baseline to month 6. The RT+DP group experienced a significant (p = 0.01) 14% increase in leg extension strength from baseline to the 3-month time point, and a further significant (p < 0.01) 12% increase from month 3 to month 6. Overall, the RT group significantly (p < 0.01) improved their leg extension strength by 28% from baseline to month 6. Published by NRC Research Press

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Fig. 1. Flow chart of participants’ progression through study.

Table 1. Frequencies of breast cancer diagnosis/treatment specifics (N = 23). (Frequency of diagnosis and treatment occurrences)

RT group (n = 12)

RT+DP group (n = 11)

Stage 1 Stage 2 Stage 3 Affected breast — left Affected breast — right Currently taking osteoporosis medication Currently taking hormone suppressant therapy Time since diagnosis (months) Time since hormone therapy completed (months) Time since primary* treatment completed (months) Number of lymph nodes removed

5 6 1 3 9 2

5 5 1 4 7 3

5

4

94.0±75.6 57.0±8.5

96.5±67.5 65.6±53.6

75.4±69.3

89.7±68.3

8±13

9±12

Note: Data are presented as means ± standard deviation. RT, resistance training; RT+DP, resistance training + dried plum consumption. *Surgery, radiation, and (or) chemotherapy.

A detailed description of muscular strength changes over the course of the study can be found in Table 2. Body composition and BMD Both the RT and the RT+DP group showed similar baseline characteristics in terms of body composition variables obtained via

circumference measures and DXA. There were no group-by-time interactions for any of the body composition variables. Similarly, there were no significant differences calculated between groups between baseline and the 6-month time point, and there were no significant differences found between time points within groups. A complete description of body composition variables can be found in Table 3. Both the RT and the RT+DP group showed similar baseline characteristics in BMD variables obtained via DXA. There were no group time interactions observed for any of the BMD variables, and there were no significant differences between groups at the 6-month time point. There were significant time effects observed for right total radius (F[1,21] = 9.909, p = 0.01, ES = 0.321), right total ulna (F[1,21] = 5.803, p = 0.03, ES = 0.217), right total forearm (F[1,21] = 10.789, p ≤ 0.01, ES = 0.339), and left total femur (F[1,21] = 5.33, p = 0.03, ES = 0.210). Further analysis indicated that the time effects associated with the right forearm occurred within the RT+DP group and the time effect for the left total femur occurred in the RT group. Over the course of the study, the RT+DP group exhibited a significant (p = 0.04) 2% decrease in the right total radius (baseline: 0.483 ± 0.059; 6 months: 0.473 ± 0.053 g/cm2), a significant (p < 0.01) 2% decrease in the right total ulna (baseline: 0.436 ± 0.051; 6 months: 0.429 ± 0.050 g/cm2), and a significant (p = 0.01) 2% decrease in the right total forearm (baseline: 0.463 ± 0.054; 6 months: 0.454 ± 0.051 g/cm2). The RT group experienced a significant (p = 0.02) 1% increase in left total femur BMD (baseline: 0.918 ± 0.121; 6 months: 0.928 ± 0.127 g/cm2). A complete description of BMD variables can be found in Table 4. Published by NRC Research Press

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Table 2. Comparison of muscular strength (N = 23). RT group (n = 12) Baseline

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1RM chest press (kg) 1RM leg extension (kg)

RT+DP group (n = 11)

3 mo

6 mo a

64±14 69±20

74±14 80±25a

Baseline a,b

80±17 87±28a,b

72±23 78±19

3 mo

6 mo a

84±20 89±21a

91±20a,b 100±21a,b

Note: Data are presented as means ± standard deviation. RT, resistance training; RT+DP, resistance training + dried plum consumption; 1RM, 1-repetition maximum. aSignificantly different from baseline assessment within same group, p ≤ 0.05. bSignificantly different from 3-month assessment within same group, p ≤ 0.05.

Table 3. Comparison of body composition variables (N = 23).

Weight (kg) BMI (kg/m2) Waist girth (cm) Hip girth (cm) Lean mass (kg) Fat mass (kg) Lean/fat mass ratio Android fat (%) Gynoid fat (%) Total body fat (%)

RT group (n = 12)

RT+DP group (n = 11)

ically significant. Please refer to Table 5 for a complete description of the biochemical markers of inflammation.

Baseline

6 mo

Baseline

6 mo

Discussion

71.3±14.0 26.8±5.0 84.5±11.7 108.1±9.5 38.9±6.8 30.4±10.2 1.36±0.34 46.5±7.4 48.7±4.9 43.8±4.9

71.3±14.0 26.8±5.0 83.1±10.0 107.0±9.5 39.2±6.8 30.2±10.1 1.38±0.34 45.7±8.3 48.8±4.5 43.4±5.1

71.9±10.4 26.9±3.7 83.3±11.2 108.1±7.0 40.2±5.5 28.9±5.9 1.43±0.27 43.5±7.6 46.5±3.6 41.6±4.2

73.0±10.2 27.2±3.7 84.1±11.3 108.4±6.7 40.8±5.0 29.5±5.8 1.41±0.24 44.0±7.6 46.6±3.3 41.7±3.9

Following participation in a 6-month RT or RT+DP intervention, the results of the present study support the hypotheses that BCS participants would demonstrate improvements in skeletal muscular strength, improve left total femur BMD, and experience decreased levels of bone resorption. The intervention elicited no other significant body composition changes, except for the significant decline in the right forearm BMD components, and there were no statistically significant changes in bone turnover makers or inflammation markers. With the exception of the increases in left total femur BMD in the RT group, the present study did not show any improvements in total body or any of the other regional sites of BMD assessed for either intervention group. The present study was the first to implement a combination treatment group of RT+DP for examining the effects of this nonpharmalogical treatment on BMD. It was hypothesized that both the RT and the RT+DP group would experience positive BMD changes, but it was unknown as to whether the RT+DP group would experience additive benefits of DP compared with the RT group alone. Results revealed that the addition of DP to RT did not provide additional benefits in BMD improvements. A recent study implementing DP in a group of healthy postmenopausal women showed significant improvements in lumbar spine and ulna BMD over the course of 12 months (Hooshmand et al. 2011). Perhaps if the duration of the present study was longer changes may have been seen. It may also be possible that because of the effects of the cancer treatment BCS may not get the same benefits as healthy postmenopausal women. The significant time effects observed over the course of the study indicated that the RT+DP group demonstrated a significant decrease in BMD of several sites of the right forearm. These results are not easily understood or explained. One possible explanation for the decreases in right forearm BMD may be that the women were unintentionally taking more precautions with their right arms when exercising. Nearly 70% of the women in the study were diagnosed with breast cancer on the right side of their body. This equates to all the surgeries and treatments being targeted toward the right arm area. Common procedures for breast cancer involve removing the sentinel lymph node for biopsy purposes. Even with a sentinel lymph node biopsy, there is an approximate 17% risk for the development of lymphedema (Francis et al. 2006). Despite the precautions taken to avoid the development of lymphedema, some of the women may have avoided full exertion with their affected arms, and thus account for the declines seen in right forearm BMD. Though this explanation may serve as a possible explanation as to why negative time effects were observed in the RT+DP group, the rationale does not account for the maintenance of forearm BMD seen in the RT group. The BMD results of the present study contradict the results found from studies conducted with healthy postmenopausal women, but coincide with the few existing studies that have implemented RT with BCS. Schwartz and colleagues found BCS partaking in RT for 6 months in conjunction with chemotherapy significantly

Note: Data are presented as means ± standard deviation. RT, resistance training; RT+DP, resistance training + dried plum consumption, BMI, body mass index.

Biochemical markers of bone turnover and inflammation Participants from the RT and the RT+DP groups demonstrated similar baseline values for both of the biochemical markers of bone turnover (BAP and TRAP-5b), as well as biochemical markers of inflammation (CRP). There were no significant group-by-time interactions observed for any of the biochemical markers. Inter-assay CVs were determined from the individual sets of duplicates and ranged from 0% to 26% for the BAP assay, 0% to 33% for the TRAP-5b assay, and 0% to 16% for the CRP assay. Because of the pre-established criterion for biochemical markers, 2 samples were ineligible for the BAP assay and 4 of the samples were ineligible for analysis of the TRAP-5b assay. The total sample sizes for each of the biochemical assays can be found in Table 5. No interaction effects were found for either marker of bone turnover, and there was no significant time effect for BAP. Though statistically nonsignificant, the overall changes for BAP within the RT and the RT+DP groups were –3% and –19%, respectively. There was a significant time effect (F[1.317,17] = 8.728, p = 0.01, ES = 0.339) observed for TRAP-5b. Analyses of the main effects showed that the RT group demonstrated a significant (p = 0.04) 11% decline in TRAP-5b from baseline to 3 months, while the RT+DP group showed a similar decline of 16% from baseline to 3 months (p = 0.07). Though statistically nonsignificant, the overall change of TRAP-5b, from baseline to 6 months was –12% (p = 0.42) for the RT group and –26% (p = 0.13) for the RT+DP group. While these overall changes for BAP and TRAP were deemed statistically nonsignificant, these changes may be clinically significant. Refer to Table 5 for a complete description of the biochemical markers of bone turnover. Participants from the RT and the RT+DP groups demonstrated similar baseline values for CRP. There was no significant groupby-time interaction observed for CRP. Though statistically nonsignificant, the overall change of CRP, from baseline to 6 months, was –44% (p = 0.29) for the RT group and –49% (p = 0.13) for the RT+DP group. While these overall changes for CRP were deemed statistically nonsignificant, these changes may be clin-

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Appl. Physiol. Nutr. Metab. Vol. 39, 2014

Table 4. Comparison of bone mineral density (N = 23).

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RT group (n = 12)

RT+DP group (n = 11)

Bone mineral density (g/cm2)

Baseline

6 mo

Baseline

6 mo

Total body Lumbar spine (L1–L4) Left femur neck Left total femur Right femur neck Right total femur Left radius 33% Left total radius Left total ulna Left total forearm Right radius 33% Right total radius Right total ulna Right total forearm

1.144±0.115 1.129±0.154 0.871±0.115 0.918±0.121 0.890±0.111 0.935±0.121 0.661±0.058 0.515±0.063 0.460±0.060 0.492±0.060 0.675±0.052 0.515±0.057 0.470±0.062 0.496±0.058

1.139±0.111 1.110±0.170 0.871±0.134 0.928±0.127a 0.888±0.111 0.938±0.123 0.657±0.058 0.510±0.060 0.460±0.063 0.489±0.059 0.670±0.046 0.509±0.053 0.468±0.058 0.492±0.054

1.131±0.145 1.094±0.162 0.879±0.146 0.914±0.123 0.891±0.152 0.942±0.116 0.622±0.077 0.476±0.059 0.433±0.054 0.458±0.055 0.637±0.078 0.483±0.059 0.436±0.051 0.463±0.054

1.130±0.148 1.092±0.164 0.885±0.141 0.920±0.126 0.892±0.148 0.942±0.115 0.619±0.062 0.475±0.053 0.429±0.048 0.455±0.049 0.629±0.071 0.473±0.053a 0.429±0.050a 0.454±0.051a

Note: Data are presented as means ± standard deviation. RT, resistance training; RT+DP, resistance training + dried plum consumption. aSignificantly different from baseline, within same group, p ≤ 0.05.

Table 5. Comparison of biochemical markers. Biochemical markers of bone formation (N = 21) RT group (n = 11)

BAP (U/L)

RT+DP group (n = 10)

Baseline

3 mo

6 mo

Baseline

3 mo

6 mo

44.00±14.00

45.79±18.49

42.68±17.08

45.10±17.68

41.29±13.98

36.53±12.71

Biochemical markers of bone resorption (N = 19) RT Group (n = 11) Baseline TRAP-5b (U/L)

RT+DP Group (n = 8)

3 mo

6 mo a

4.55±1.57

4.04±1.63

4.03±1.81

Baseline 5.10±2.75

3 mo

6 mo b

4.27±2.03

3.77±1.80

Biochemical markers of inflammation (N = 23) RT group (n = 12)

CRP (U/L)

RT+DP group (n = 11)

Baseline

3 mo

6 mo

Baseline

3 mo

6 mo

4.13±6.77

3.00±3.66

2.30±2.55

3.20±4.40

2.32±2.72

1.64±1.48

Note: Data are presented as means ± standard deviation. RT, resistance training; RT+DP, resistance training + dried plum consumption; BAP, bone-specific alkaline phosphatase; TRAP-5b, tartrate resistant acid phosphatase; CRP, C-reactive protein. aSignificantly different from baseline assessment, within same group, p ≤ 0.05. bSignificantly different from baseline assessment within same group, p ≤ 0.07.

decreased (–4.92%) lumbar spine over the course of the study (Schwartz et al. 2007). Likewise, Waltman and colleagues reported a significant 2.6% loss in forearm BMD of BCS after engaging in a 12-month multi-component intervention featuring RT and bisphosphonate therapies (Waltman et al. 2003). These results closely mimic the 3% forearm BMD loss reported in the RT+DP group of the present study. Even though the women from the present study showed no significant improvements in BMD, it is noteworthy that all sites except the right forearm were maintained over the course of the 6 months, and the total left femur was improved by 1% in the RT group. Maintaining BMD should be considered a desirable outcome for postmenopausal women, and even more so for BCS, given the vulnerability of their bone health. A limitation of the present study is the lack of a true control group, though it can be expected that without the interventions, the women in the study may have experienced a significant decline in 1 or more BMD sites over the course of the 6 months. Pruitt and colleagues reported that while the women in the RT group of their study maintained BMD over the course of the 9-month study, their control group lost a significant 3.6% in the lumbar spine (Pruitt et al. 1992). Similarly, Jessup and colleagues reported significant losses of the femur neck in their control group over the course of their 32-week intervention (Jessup et al. 2003). Simonavice and colleagues fol-

lowed a group of BCS and healthy controls over the course of 15 months and noted that both groups lost a significant 2% for the lumbar spine, total femur, and total forearm (Simonavice et al. 2011b). Thus, the results from several previous studies indicate that it is likely that the women from the present study would have experienced a significant decrease in BMD had they not been participating in the intervention. The success in maintaining BMD, with the exception of the right forearm, seen in the present study is reflective of the positive changes demonstrated in the biomarkers representing bone turnover. Though there were no group-by-time interactions observed for either of the biochemical markers of bone metabolism, there was, however, a significant time effect observed for the biomarker of bone resorption over the course of the study. Results showed that bone resorption, as expressed by TRAP-5b, was significantly decreased; 11% for the RT group and 16% for the RT+DP group. These findings are especially encouraging given the fact that BCS that have been treated with hormone suppressant therapies (aromatase inhibitors) and have significantly higher levels of bone resorption as compared with healthy postmenopausal women (Heshmati et al. 2002). Eastell and colleagues reported that 2 years of aromatase inhibitor treatment elicited a 15% increase in bone resorption indices. This increase in bone turnover was associated with a loss of BMD ranging from 1%–4%, depending upon the site Published by NRC Research Press

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Simonavice et al.

measured (Eastell et al. 2006). Given the increase in bone turnover elicited by hormone suppressant therapies, the ability of the present study to decrease bone resorption and maintain bone formation provides a viable option for BCS to decrease bone turnover. The results of the present study indicated that DP consumption does not provide added benefit to bone turnover in addition to RT. However, the design of the present study does not allow for clear distinction of the benefit of DP consumption on BCS. Similar to the results of bone formation markers, CRP levels did not statistically decrease over the course of the study. Despite the lack of statistical significance, the 44% and 49% decline in CRP levels for the RT and RT+DP groups, respectively, may certainly be of clinical significance. According to clinical cut points for CRP in relation to prediction of cardiovascular disease, both the RT and the RT+DP groups were in the high-risk group, having levels >3 mg/L. The declines of CRP experienced over the course of the study lowered the risk of both groups to that of moderate risk, with levels between 1–3 mg/L (Ridker et al. 2002). The declines in CRP are also of clinical significance because CRP has been deemed as having the highest association with breast cancer risk and risk of cancer death compared with any of the other inflammatory markers (Il’yasova et al. 2005). Similar to the BMD results of the study, the women participating in the present study exhibited no changes in body composition over the course of the 6 months. While these results contradict the lean mass and fat mass improvements that previous RT studies have reported with BCS (Cheema and Gaul 2006; Schmitz et al. 2005), Winters-Stone and colleagues recently implemented a 12-month RT intervention with BCS and reported similar lean mass and fat mass results as the present study (Winters-Stone et al. 2011). Although improving lean mass and fat mass is most desirable, maintaining lean mass, fat mass, and body fat percent should be given some merit considering that the normal aging process yields unfavorable body composition changes. In a longitudinal study following a sample of BCS and healthy postmenopausal women, results showed that over the course of approximately 15 months, all women in the study exhibited a significant 3% increase in body fat percent as well as a significant 7% decline in their lean to fat mass ratio (Simonavice et al. 2011b). Since the present study implemented only a RT exercise intervention 2 days per week, it is possible that body composition improvements could have occurred if the intervention consisted of RT 3 days per week, had participants exercising at greater intensities (70%–85% of 1RM), and (or) added an aerobic exercise component. The lack of improvement in lean mass did not hinder the women’s ability to make significant strength gains in both upper and lower body muscular groups. These results coincide with the strong support of previous literature that indicated the ability for BCS to make improvements in skeletal muscle strength. Courneya and colleagues showed that even while breast cancer patients were in the course of their chemotherapy regimen, a RT program elicited a 31% increase in upper body strength and a 32% increase in lower body strength (Courneya et al. 2007). Other studies implementing a RT program after the completion of cancer treatments (as did the present study) have reported gains of 33% for upper body strength and 48% increase in lower body strength (Cheema and Gaul 2006). The ability for BCS to gain skeletal muscular strength is especially encouraging given the fact that typically after cancer treatments, BCS are significantly weaker compared with healthy agematched controls (HC). Simonavice and colleagues found that BCS were significantly weaker for upper body (BCS: 61 ± 13; HC: 77 ± 20 kg) and lower body (BCS: 70 ± 13; HC: 91 ± 18 kg) strength compared with healthy postmenopausal women (Simonavice et al. 2011a). Comparing the 6-month strength values for upper body (RT: 80 ± 5; RT+DP: 91 ± 6 kg) and lower body (RT: 87 ± 8; RT+DP: 100 ± 7 kg) from the present study to the baseline values of the healthy controls in Simonavice et al. (2011a) indicates that the RT intervention increased strength up the levels of healthy post-

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menopausal women. The results from the present study in combination with the reviewed studies confirm the idea that BCS are very capable of making both upper and lower body strength gains. Limitations of the present study include a lack of formal monitoring of diet and physical activity throughout the course of the study. Though participants were asked to refrain from making any major dietary or physical activity changes while participating in the study, it is possible that the participants could have altered 1 or both of these components of their lifestyle. However, body weights were taken weekly and pedometer data were collected monthly to assess physical activity. Neither of these measurements changed significantly over the course of the study. Similarly, it is possible that some of the women in the RT group, though asked not to, could have incorporated DPs into their diets. These alterations could be deemed as potential confounding variables for the outcomes assessed. Second, a limitation of the present study was the short duration of the intervention. A longer duration (≥12 months) may have provided a more complete assessment on how bone turnover and BMD were affected by the interventions. Another limitation is that the BCS in both intervention groups did not begin training in the prescribed 60%–80% 1RM range until approximately 4 weeks into the study. It is possible that had the women been able to achieve the prescribed intensity sooner or progress to the upper limit of the prescribed intensity, body composition changes may have occurred. Finally, the small sample size (n = 23) of the present study lowers the external validity of the study and could have hindered obtaining statistical significance on the variables assessed.

Conclusions Our findings indicate that an RT or combination RT+DP intervention was well tolerated among BCS. All women displayed high levels of adherence to the attendance of exercise sessions as well as to the calcium/vitamin D supplements. With the exception of 2 women from the RT+DP group, adherence to DP consumption was also very good. One of the research questions of the study was to determine whether the addition of DP to a RT intervention would elicit added BMD, biochemical markers of bone turnover, and (or) biochemical markers of inflammation benefits. The results showed that there was no additive effect of DP to RT observed over the course of the study for any of the variables assessed. Further research is needed to assess whether DP consumption alone would have similar BMD and biochemical marker changes of bone turnover and inflammation in BCS as was reported in healthy postmenopausal women. It was further concluded that the majority of the results showing the maintenance of all BMD sites, except for the right forearm, was the physical manifestation of the observed changes of bone turnover markers. These biochemical changes indicated maintenance of bone formation, with a decline in bone resorption. Though statistically nonsignificant, the intervention lowered inflammation to the point of moving both groups from a high cardiovascular disease risk to a moderate cardiovascular disease risk. The intervention maintained all body composition variables assessed (lean mass, fat mass, body fat percent, and girth measurements). Although this outcome was not what was hoped for when designing this study, it is possible that had the women not been participating in the study, they may have experienced unfavorable age- and disease-related body composition changes. Finally, it should be concluded that the BCS exhibited large capabilities for improving both upper and lower body muscular strength over the course of the study. Future studies among BCS may benefit from implementing a RT intervention of longer duration and higher intensities or volumes in hopes of seeing more favorable biochemical bone turnover and body composition changes. Additionally, the role of DP consumption in affecting bone health in BCS remains unclear, thus future Published by NRC Research Press

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research would benefit from designing a study that would more clearly reveal the role of DP in modulating biochemical markers of inflammation, bone turnover, and BMD.

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Acknowledgements The authors thank the California Dried Plum Board for supplying the dried plums and Florida State University for funding to conduct the study. The authors would also like to extend a sincere thank you to all the women who dedicated their time and efforts to make this project possible.

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The effects of a 6-month resistance training and dried plum consumption intervention on strength, body composition, blood markers of bone turnover, and inflammation in breast cancer survivors.

The purpose of this study was to examine the effects of resistance training (RT) and dried plum (DP) consumption on strength, body composition, blood ...
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