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1 Journal of Exercise Physiologyonline 117 December 2017 Volume 20 Number 6 Editor-in-Chief Official Research Journal of Tommy the American Boone, PhD, Society MBA of Review Exercise Board Physiologists Todd Astorino, PhD Julien Baker, ISSN PhD Steve Brock, PhD Lance Dalleck, PhD Eric Goulet, PhD Robert Gotshall, PhD Alexander Hutchison, PhD M. Knight-Maloney, PhD Len Kravitz, PhD James Laskin, PhD Yit Aun Lim, PhD Lonnie Lowery, PhD Derek Marks, PhD Cristine Mermier, PhD Robert Robergs, PhD Chantal Vella, PhD Dale Wagner, PhD Frank Wyatt, PhD Ben Zhou, PhD Official Research Journal of the American Society of Exercise Physiologists ISSN JEPonline Chronic Effects of Resistance Training with Blood Flow Restriction on Maximal Dynamic Strength and Flexibility at Different Phases of the Menstrual Cycle Carolina Araujo 1, Gabriel R. Neto 1,2,3,4, Maria S. Cirilo- Sousa 2,3, Eduardo Chaves 1, Amanda Brown 1, Ingrid Dias 1,3,5, Marcos Sá 1, Jeferson Vianna 6, Jefferson S. Novaes 1,6 1 Department of Gymnastics, Federal University of Rio de Janeiro (UFRJ), Physical Education Graduate Program, Rio de Janeiro, RJ, Brazil, 2 Department of Physical Education, Associate Graduate Program in Physical Education UPE / UFPB, João Pessoa, Paraíba, Brazil, 3 Department of Physical Education, Kinanthropometry and Human Development Laboratory - UFPB, João Pessoa, Paraíba, Brazil, 4 Coordination of Physical Education, Nursing and Medical Schools, Nova Esperança (FAMENE/ FACENE), 5 Medical Clinic Postgraduate Program, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil, 6 Department of Physical Education, Federal University of Juiz de Fora, Physical Education Post Graduation Program, Juiz de Fora, Brazil ABSTRACT Araujo C, Neto, GR, Cirilo-Sousa MS, Chaves E, Brown A, Dias I, Sá M, Vianna J, Novaes JS. Chronic Effects of Resistance Training with Blood Flow Restriction on Maximal Dynamic Strength and Flexibility at Different Phases of the Menstrual Cycle. JEPonline 2017;20(6): The aim of the present study was to assess the chronic effects of resistance training (RT) with or without blood flow restriction (BFR) on maximal dynamic strength (MDS) and flexibility at different phases of the menstrual cycle (MC). Twenty-nine sedentary women were randomly divided into three groups: (a) HI = high-intensity resistance training at 80% of onerepetition maximum (1RM); (b) LL+BFR = low-load resistance training at 20% 1RM combined with BFR; and (c) CG =

2 control group (no training performed). The biceps curl exercise was significantly increased between the follicular vs. ovulation phases in the HI and LL+BFR groups (P<0.05), between the follicular vs. luteal phases in the HI group (P<0.001), and between the ovulation vs. luteal phases in the LL+BFR group (P=0.009). The knee extension exercise was significantly increased between the follicular vs. ovulation, follicular vs. luteal, and ovulation vs. luteal phases in the HI and LL+BFR groups (all P<0.001). No differences occurred between the groups in either exercise (P>0.05). The flexibility analysis showed that no significant intraand inter-group differences occurred (P>0.05). Resistance training combined with BFR appears to progressively increase upper and lower limb MDS between phases of the MC, although it is not effective for increasing flexibility. Key Words: Kaatsu, Menstrual Cycle, Strength Training, Vascular Occlusion, Women 118 INTRODUCTION Resistance training (RT) is a method responsible for increasing muscle strength by promoting myofibrillar adaptations that result in hypertrophy and increased power and maximal strength (33) These increases are best demonstrated when the training intensity is equal to or higher than 70% of one-repetition maximum (1RM) (3). However, many individuals (e.g., elderly, injured) are unable to withstand high mechanical stress placed on the joints during highintensity RT. Furthermore, the performance of women may also be affected by hormonal changes that occur during the phases of the menstrual cycle (MC) (12). Thus, different healthcare professionals have sought alternatives using low-intensity (load) RT for such individuals that generate adaptations similar to traditional high-intensity resistance training. Some studies have shown that the same changes in strength (17,32,34,36) and muscle mass (17,36) may be achieved using low-load (LL) RT (20% to 30% 1RM) combined with blood flow restriction (BFR). This training method has also been used to increase local muscular endurance (13,15,34) and functional capacity (4) and has been demonstrated to be safe regarding hemodynamics (5,9,21-23,25,26,35,37). However, it does not appear to be very effective when using high loads (17,24). A review of the relevant literature indicates that one study assessed the effects of LL RT combined with BFR on strength and muscle mass (30), one on isometric muscle strength (9), and another study assessed the effects of LL RT and BFR on local muscular endurance and power (13) at different phases of the MC. However, no study has assessed the effects of LL RT combined with BFR on flexibility and maximal dynamic strength (MDS) in the upper and lower limbs during different phases of the MC. Thus, understanding the effects of LL RT combined with BFR on MDS and flexibility at different phases of the MC may help trainers and healthcare professionals create interventions because women go through different hormonal stages monthly, which may reduce performance in the proposed activities (12). Thus, the aim of the present study was to assess the chronic effects of RT with or without BFR on MDS and flexibility at different phases of the menstrual cycle (MC). This study s hypothesis states that LL RT performed in combination with BFR would significantly increase MDS and flexibility levels, which is similar to traditional training without BFR.

3 119 METHODS Subjects This study included a total of 29 women who were untrained in RT (19 to 39 yrs of age), with a normal MC ranging from 26 to 32 days (mean of 28 days). The women were randomly divided into three groups (Table 1). The following women were excluded from the study: (a) women using contraceptives for at least six months; (b) women undergoing hormone replacement therapy and ingesting supplements; (c) women with menstrual irregularities; (d) women who had some type of musculoskeletal injury in the upper or lower limbs; and (e) women who answered positively to any item of the Physical Activity Readiness Questionnaire (PAR-Q) (31). The subjects signed a free and informed consent form that was prepared in accordance with the Declaration of Helsinki after being explained the risks and benefits of this study. The research was approved by the Ethics Committee for Research Involving Human Subjects of the Federal University of Paraíba, Brazil, under protocol 0476/13. Table 1. Sample Characteristics of the Studjects. HI = 10 LL + BFR = 10 CG = 09 Age (yrs) 21.6 ± ± ± 6.0 Weight (kg) 53.7 ± ± ± 4.6 Height (m) 1.57 ± ± ± 0.07 BMI (kg m -2 ) 21.7 ± ± ± 1.6 Menarche 12.6 ± ± ± 1.5 Mean MC 27.3 ± ± ± 0.6 BMI = Body Mass Index; HI = High-Intensity Group; LL + BFR = Low Load + Blood Flow Restriction Group; CG = Control Group Study Design All subjects were familiarized with the procedures for at least two sessions before beginning the intervention. Anthropometry was evaluated during the first visit (1st day of the follicular phase), followed by determination of the BFR point 10 min later. Then, flexibility was evaluated using the sit-and-reach test (Wells bench), and 10 min later, MDS was evaluated using biceps curl and knee extension exercises with a 10-min interval between exercises. The flexibility and MDS tests were also performed during the ovulation (14th day of the MC) and luteal (26th 28th days of the MC) phases. Eight training sessions were performed between the follicular and luteal phases. The subjects were divided into three study groups that performed one of the following routines: (a) high-intensity resistance training performing the exercises at 80% 1RM (HI); (b) LL resistance training with exercises performed at 20% 1RM combined with partial BFR (LL+BFR); and the control group (CG), in which the subjects maintained their activities of daily living.

4 Procedures Anthropometric Assessment The subjects height and body mass were measured to a 0.5 cm and 1.0 kg accuracy, respectively, using a stadiometer and a Filizola balance. The measurements were then used to calculate body mass index (BMI) expressed as kg m -2. Blood Flow Restriction Assessment Total BFR was assessed using a vascular doppler (MedPeg DV 2001, Ribeirão Preto, São Paulo (SP), Brazil). The probe was placed on the radial artery (arm) and tibial artery (legs) to assess the BFR pressure (mmhg; first day of menstruation follicular phase). The volunteers remained lying in the supine position, and a standard blood pressure sphygmomanometer (komprimeter pneumatic tourniquet for hemostasis in extremities Riester) for the biceps (60 mm width; 470 mm length) and knee extensors (100 mm width; 540 mm length) were attached to the axillary and inguinal folds, respectively, and inflated until the auscultatory pulse of the radial or tibial arteries were interrupted. The cuff pressure used during training was set at 80% of the pressure necessary for complete BFR at rest (17). Maximal Dynamic Strength Test (1RM) The training load prescription was evaluated using the 1RM test (2). The tests were performed during the 1st day (follicular phase), 14th day (ovulation phase) and 26th -28th days (luteal phase), adjusting the load immediately after each test. The exercises were performed bilaterally: right biceps curl (using a conventional barbell and disk weights) and knee extension (knee extension machine - Body fitness, Brazil). A 10-min rest interval was taken between the exercises. For warm-up, each individual performed 2 sets of 5 to 10 reps at 40 to 60% of the subject s self-perceived maximal strength (1 min interval between sets), respectively. After a 1 min interval, the 3rd set was concluded completing 3 to 5 reps at 60 to 80% perceived maximal strength. After another rest period (1 min), the strength assessment was started, in which up to 5 attempts could be performed, adjusting the load before each new attempt. The length of the rest period between attempts was 3 to 5 min. The test was interrupted when the subject failed to perform the movement correctly, with the fully completed repetition considered the maximal load. Sit-and-Reach Test The sit-and-reach test was used to measure flexibility (1). The subjects were positioned on an exercise mat on the floor with their feet placed on the platform of the Wells bench. Then, they performed two trunk flexion movements with their arms aloft and remained in that position for 2 sec. The best measurement of two attempts was used for the statistical analysis. Training Protocol Eight training sessions were performed during the MC between the follicular and luteal phases, and these sessions were conducted twice per week. The two bilateral resistance exercises were right biceps curl (using a conventional barbell and disk weights) and knee extension (knee extension machine). The subjects were randomly divided into 3 groups as follows: (a) HI = two high-intensity resistance exercises at 80% 1RM; (b) LL + BFR = two lowload resistance exercises at 20% 1RM combined with BFR; and (c) CG = control group. In the HI group, the subjects completed 4 sets of 8 reps at 80% 1RM with a 2 min interval 120

5 between all sets and a 1 min interval between exercises. In the LL + BFR group, the subjects completed 1 set of 30 reps followed by 3 sets of 15 reps, using 20% 1RM with a 30-sec interval between all sets and a 1 min interval between exercises, while using a standard blood pressure sphygmomanometer for BFR. The cuff pressure was maintained throughout the training session except during the 30-sec intervals between sets. Execution speed was set at 4 sec (2 sec for the concentric and 2 sec for the eccentric muscle action), which was controlled using the metronome Tagima Japan (WMT-30C, Metro-Tuner). Conversely, the subjects in the CG continued with their daily living activities. Statistical Analyses The statistical analysis was initially performed using the Shapiro-Wilk normality test and Levene s test of homogeneity of variance. The variables showed a normal distribution and homogeneity (P>0.05). Thus, the data are shown as the mean ± standard deviation. Repeated-measure two-way analysis of variance (ANOVA) (groups [HI vs. LL + BFR vs. CG] time [follicular phase vs. ovulation phase vs. luteal phase]) was used to compare the differences between the dependent variables of the study. Where appropriate, specific differences were determined using the Bonferroni s post hoc test. The effect size (ES) was used to assess the magnitude (trivial < 0.50, small = , moderate = , large > 2.0) of the changes between study protocol assessments (29). The significance level was set at P<0.05. All of the statistical analyses were performed using the statistical software Statistical Package for the Social Sciences (SPSS) version 20.0 (SPSS Inc., Chicago, IL, USA). RESULTS No significant differences were observed among the groups in the comparative analysis of age, anthropometric characteristics, age at first menarche, and mean MC (P>0.05) (Table 1). The following mean pressures were used throughout the arm (right = ± 11.0 mmhg; left = 128 ± 13.9 mmhg) and leg (right = ± 9.6 mmhg; left ± 12.6 mmhg) training protocols. Arm Curl (1RM) The comparative analysis of MDS in the biceps curl exercise using repeated-measures twoway ANOVA showed that there were no significant interactions between groups x time (F (2,6) = 1.798; ɳ 2 = 0.134; P = 0.112) and between groups (F (2,6) = 0.123; ɳ 2 = 0.010; P = 0.946). However, there was an interaction in the condition time (F (2,6) = ; ɳ 2 = 0.484; P<0.001). The intragroup analysis showed significant increases in the HI group between the follicular vs. ovulation phases and between the follicular vs. luteal phases (P = 0.002, ES = 0.40; P<0.001, ES = 0.63, respectively). In the LL + BFR group, significant increases were observed between the follicular vs. luteal phases and between the ovulation vs. luteal phases (P<0.001, ES = 0.89; P = 0.009, ES = 0.48, respectively). No significant differences were observed between the phases of the MC regarding the CG (P>0.05), as shown in Figure

6 122 Figure 1. Comparative Analysis of Maximal Strength (1RM) of the Biceps Curl Exercise between Study Groups. *Significant difference between the follicular vs. ovulation phases and the follicular vs. luteal phases; Significant difference between the ovulation and luteal phases; HI = High-Intensity Group; LL + BFR = Low Load + Blood Flow Restriction Group; CG = Control Group Leg Extension (1RM) The comparative analysis of maximal strength in the knee extension exercise showed significant interactions between group x time (F (2,6) = 7.086; ɳ 2 = 0.378; P<0.001) and time (F (2,6) = ; ɳ 2 = 0.745; P<0.001). However, there were no significant interactions between groups (F (2,6) = 0.484; ɳ 2 = 0.040; P = 0.695). The intragroup analysis showed significant increases in the HI group between the follicular vs. ovulation phases, the follicular vs. luteal phases, and the ovulation vs. luteal phases (P<0.001, ES = 0.53; P<0.001, ES = 1.06; P<0.001, ES = 0.49, respectively). In the LL + BFR group, significant increases were observed between the follicular vs. ovulation phases, the follicular vs. luteal phases, and the ovulation vs. luteal phases (P<0.001, ES = 0.63; P<0.001, ES = 1.20; P<0.001, ES = 0.51, respectively). No significant differences were observed between phases of the MC regarding the CG (P>0.05), as shown in Figure 2. Flexibility The comparative analysis of flexibility showed no significant interactions between groups x time (F (2,6) = 1.684; ɳ 2 = 0.126; P = 0.160) and between groups (F (2,6) = 0.587; ɳ 2 = 0.048; P = 0.627), although there was a significant interaction in the condition time (F (2,6) = 5.410; ɳ 2 = 0.134; P = 0.013), as shown in Figure 3.

7 123 Figure 2. Comparative Analysis of Maximal Strength (1RM) of the Knee Extension Exercise between Study Groups. *Significant difference between the follicular vs. ovulation phases and the follicular vs. luteal phases; Significant difference between the ovulation and luteal phases; HI = High- Intensity Group; LL + BFR = Low Load + Blood Flow Restriction Group; CG = Control Group Figure 3. Comparative Analysis of Flexibility in the Wells Bench (cm) between Study Groups. HI = High-Intensity Group; LL + BFR = Low Load + Blood Flow Restriction Group; CG = Control Group

8 124 DISCUSSION The present study assessed the effects of RT with or without BFR on MDS and flexibility during the different phases of the MC in untrained women. To our knowledge, this was the first study conducted on women untrained in RT that compared the chronic effects of RT combined with BFR on upper and lower limb MDS and flexibility between the follicular, ovulation, and luteal phases. The main findings of the present study were: (a) the occurrence of a significant increase in MDS between phases of the MC in the biceps curl and knee extension exercises in the HI and LL + BFR groups, without significant differences between them; and (b) no significant increase in flexibility occurred in the study groups. Some studies have previously compared the MDS (1RM) levels between HI RT without BFR and LL RT combined with BFR (16,18). The results found corroborate our findings. Lixandrão et al. (18) demonstrated that both HI RT without BFR and LL RT (20% and 40% 1RM) combined with BFR showed MDS increases in untrained men in the (unilateral) knee extension exercise after 12 wks of training. Karabulut et al. (16) suggested that the MDS of untrained elderly men increased significantly after 6 wks of LL RT (20% 1RM) combined with BFR. An analysis of the results from the aforementioned studies (16,18) compared to the results from the present study shows that LL RT combined with BFR apparently promotes significant increases in muscle strength, regardless of age (young adults, elderly), gender (male or female), body part (upper or lower limbs), exercise performance method (unilateral or bilateral), load percentages (20% to 40% 1RM), BFR method (continuous or intermittent), and training duration (6, 8, and 12 wks). These benefits are apparently related to high metabolic stress, which has been indicated as the main factor responsible for the activation of several other mechanisms that apparently induce muscle growth through autocrine or paracrine actions. Metabolic stress has been indicated because it signals several mechanisms that induce muscle growth, including the increased recruitment of fast-twitch muscle fibers, mechanotransduction, systemic and localized hormone production, cell swelling, and the production of reactive oxygen species and their variants, including nitric oxide and heat shock proteins. These mechanisms have been linked to the increase in muscle strength (27,28). However, no study has been conducted to assess the effects of LL RT combined with BFR on flexibility and upper and lower limb (bilateral execution) MDS during the phases of the MC. One study assessed the effects of LL RT combined with BFR on muscle strength and mass (30), and another study assessed the effects of LL RT and BFR on local muscle endurance and power (13) at different phases of the MC. Sakamaki et al. (30) found that the increase in isometric strength was higher in the luteal phase than in the follicular phase. Gil et al. (13) concluded that BFR apparently fails to increase upper and lower limb power, although it appears to improve local muscle endurance, particularly during the ovulation and luteal phases of the MC. These results indicate that healthcare professionals and trainers should pay more attention to women during the phases of the MC, focusing on the luteal phase. No studies assessing the effects of LL RT combined with BFR on flexibility were found when reviewing the available literature. However, studies were identified that assessed the effects of conventional RT on flexibility measured using goniometry (10,20) or the sit-and-reach test

9 (7). The results from the three studies differ from our results because the authors found increased flexibility after training. Furthermore, there appears to be a relationship between intensity and flexibility, that is, percentages higher than 60% 1RM were found to be more effective in producing increased flexibility levels (10). Moreover, RT combined with BFR was able to generate small increases in flexibility levels, albeit without significant differences. This most likely resulted from the low load percentage (20% 1RM), the number of exercises, and the small volume of training sessions conducted during one MC. Thus, training intensity and volume were apparently insufficient to achieve significant increases in range of motion because the BFR method inherently uses low load percentages and low training volumes. Furthermore, although the literature still does not adequately explain the mechanisms of flexibility gains resulting from RT, some hypotheses have been suggested. The first is related to neuromuscular responses and possible variations in myotendinous characteristics. The second possibility is linked to the immediate, albeit transient, increase of the reflex activity of Golgi tendon organs and muscle spindles (11). A third hypothesis is resistance training causes increased tension in tendons and ligaments, thereby improving muscle contractility that leads to an increased range of motion (6). Limitations of this Study A possible limitation that may have affected our results was the failure to perform hormonal tests in our subjects. However, evidence suggests that variations in MC have no effect on strength (14) and flexibility (8,19). Another possible limitation is the test specificity regarding the exercises used in training. CONCLUSIONS The present study suggests that RT combined with BFR progressively increases MDS in upper and lower limbs between phases of the MC, although it does not appear to be effective in increasing flexibility. Thus, further experiments analyzing MDS and flexibility must be conducted in women with different fitness levels, particularly involving multi-joint exercises, specific flexibility tests (goniometry), different load intensities, and different BFR pressures. 125 Address for correspondence: Dr. Gabriel Rodrigues Neto, Coordination of Physical Education - Nursing and Medical Schools, Nova Esperança (FAMENE / FACENE). Avenida Frei Galvão, 12 - Gramame, PB, , João Pessoa, Brazil. gabrielrodrigues_1988@hotmail.com REFERENCES 1. ACSM'S Manual for Evaluation of Health-Related Physical Fitness. (3rd Edition). Rio de Janeiro: Guanabara Koogan, American College of Sports Medicine. ACSM s Guidelines for Exercise Testing and Prescription. (6th Edition). Baltimore, MD: Williams & Wilkins, 2000.

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