ACUTE EFFECTS OF LATERAL THIGH FOAM ROLLING ON ARTERIAL TISSUE PERFUSION DETERMINED BY SPECTRAL DOPPLER AND POWER DOPPLER ULTRASOUND THILO HOTFIEL,1 BERND SWOBODA,1 SEBASTIAN KRINNER,2 CASPER GRIM,3 MARTIN ENGELHARDT,3 MICHAEL UDER,4 AND RAFAEL U. HEISS4 1

Division of Orthopedic Rheumatology, Department of Orthopedic Surgery, Friedrich-Alexander-University of ErlangenNuremberg, Erlangen, Germany; 2Department of Orthopedic Trauma Surgery, University Hospital Erlangen, Erlangen, Germany; 3Department of Trauma and Orthopedic Surgery, Klinikum Osnabru¨ck, Osnabru¨ck, Germany; and 4Department of Radiology, University Hospital Erlangen, Erlangen, Germany ABSTRACT

Hotfiel, T, Swoboda, B, Krinner, S, Grim, C, Engelhardt, M, Uder, M, and Heiss, R. Acute effects of lateral thigh foam rolling on arterial tissue perfusion determined by spectral Doppler and power Doppler ultrasound. J Strength Cond Res 31(4): 893– 900, 2017—Foam rolling has been developed as a popular intervention in training and rehabilitation. However, evidence on its effects on the cellular and physiological level is lacking. The aim of this study was to assess the effect of foam rolling on arterial blood flow of the lateral thigh. Twenty-one healthy participants (age, 25 6 2 years; height, 177 6 9 cm; body weight, 74 6 9 kg) were recruited from the medical and sports faculty. Arterial tissue perfusion was determined by spectral Doppler and power Doppler ultrasound, represented as peak flow (Vmax), time average velocity maximum (TAMx), time average velocity mean (TAMn), and resistive index (RI), and with semiquantitative grading that was assessed by 4 blindfolded investigators. Measurement values were assessed under resting conditions and twice after foam rolling exercises of the lateral thigh (0 and 30 minutes after intervention). The trochanteric region, mid portion, and distal tibial insertion of the lateral thigh were representative for data analysis. Arterial blood flow of the lateral thigh increased significantly after foam rolling exercises compared with baseline (p # 0.05). We detected a relative increase in Vmax of 73.6% (0 minutes) and 52.7% (30 minutes) (p , 0.001), in TAMx of 53.2% (p , 0.001) and 38.3% (p = 0.002), and in TAMn of 84.4% (p , 0.001) and 68.2% (p , 0.001). Semiquantitative power Doppler scores at all portions revealed increased average grading of 1.96 after intervention and 2.04 after 30 minutes compared with 0.75 at Address correspondence to Dr. Rafael Heiß, [email protected]. 31(4)/893–900 Journal of Strength and Conditioning Research Ó 2016 National Strength and Conditioning Association

baseline. Our results may contribute to the understanding of local physiological reactions to self-myofascial release.

KEY WORDS myofascial release, black roll, training, regeneration

INTRODUCTION

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oam rolling has received increased attention from a wide spectrum of athletes in various sports disciplines, such as physical therapists and fitness professionals. Foam rolling, referred to as a method of self-myofascial release (SMR), has been developed into a popular intervention and has been established in training and rehabilitation. The commonly used tools for self-myofascial release include foam rollers and roller massagers, and they include a wide variety of different shapes, densities, and sizes (8). The technique is intended to enhance recovery and performance, although there is currently limited evidence to support this (6,27). There is still a lack of consensus regarding the optimal SMR program (6,27). Recent studies focusing on the influence on flexibility have reported an increase in the range of motion for the hip joint (2,23), knee joint (21), hamstring muscles (32), and ankle joint (30). Some studies observed the effects of foam rolling on muscle recovery and recommended foam rolling to enhance muscle performance after acute muscle soreness (13), delayed onset muscle soreness (25), and postexercise-induced muscle damage (20). Despite the growing application of foam rolling, studies observing the effects on a cellular and physiological level are lacking. A study focusing on the recovery effects reported foam rolling to be primarily accrued through neural responses and connective tissue (20). Okamoto et al. (24) investigated acute effects of selfmyofascial release on systemic hemodynamic parameters, such as brachial-ankle pulse wave velocity, blood pressure, heart rate, and plasma nitric oxide concentration, and indicated that SMR using a foam roller reduces arterial stiffness VOLUME 31 | NUMBER 4 | APRIL 2017 |

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Relationship of Foam Rolling and Arterial Tissue Perfusion METHODS Experimental Approach to the Problem

This study consisted of an experimental approach to investigate arterial tissue perfusion in 21 healthy participants after a foam rolling intervention. Each participant received 3 spectral Doppler and PDS examinations, with each in 3 defined anatomical regions and 2 different probe positions. The first investigation was performed under resting condiFigure 1. A) Probe positions on the lateral thigh. B) Foam rolling of the lateral thigh. tions. Participants were reexamined directly after (1 minute) and 30 minutes after and improves vascular endothelial function. Some authors a prescribed foam rolling intervention. The aim of this study suggest that the most common outcome of SMR could be was to investigate the role of foam rolling on arterial tissue attributed to the increase in muscular blood flow (25). Blood perfusion. The dependent variables in the study were spectral circulation has been shown to have an essential role in tissue Doppler measurement parameters and absolute values of an healing (19) and has been reported to enable the delivery of established semiquantitative power Doppler grading score. proteins, nutrients, and oxygen (5). However, to date, no inSubjects vestigations have determined a local arterial perfusion Twenty-one healthy students (12 male students and 9 female response after performing SMR using a custom-made foam students; age (mean 6 SD), 25 6 2 years; age range, 23 – 31; roller. Thus, the aim of the present study was to assess the height, 177 6 9 cm; body weight, 74 6 9 kg) with no acute or impact of foam rolling on arterial blood flow and tissue peroveruse injuries of the lower extremity were recruited from fusion by the established means of spectral Doppler and the medical and sports faculty and asked to participate. Inclupower Doppler ultrasound (PDS). We hypothesized that sion criteria included having more than 3 months of experiSMR performed with a foam roller increases local arterial ence in foam rolling to ensure a proper exercise technique. blood flow directly after the intervention; however, we did not expect changes after 30 minutes. There was no malalignment of the lower limb in any participant, and all participants represented full ranges of motion for the hip joint, knee joint, and ankle joint (determined by Hotfiel, T, orthopedic surgeon). According to the inclusion criteria of the study of Okamoto et al. (24), all participants were normotensive, with no signs, symptoms, or history of chronic diseases. The participants were advised to renounce sports activities for 48 hours before the examination date. Average common training frequency of the participants was 4 6 2 sessions per week, resulting in 8 6 1.5 training hours per week, complying with grade 3 of the Valderrabano Sport Scale Figure 2. Semiquantitative scoring system for intramuscular power Doppler signal: grade 0 for none (A), grade I (high level of sports activity in for minor (B), grade II for moderate (C), and grade III for major (D) presence of hyperperfusion. leisure time) (37). Various sports

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TABLE 1. Absolute values of Vmax, TAMx, TAMn, and RI (6SD), corresponding p-values and relative increases to baseline for 21 participants for following settings: resting conditions (baseline), early postintervention phase (EPIP) and late postintervention phase (LPIP).*

Vmax (cm$s21) TAMx TAMn RI

LPIP (30 min)

p

Relative raise (baseline) (%)

Baseline

EPIP (1 min)

p

Relative increase (baseline) (%)

7.2 6 2.6

12.5 6 5.0

,0.001

73.6

11.0 6 4.1

,0.001

52.7

2.01 6 0.56 0.64 6 0.28 0.87 6 0.04

3.08 6 1.41 1.18 6 0.72 0.89 6 0.04

,0.001 ,0.001 0.016

53.2 84.4 2.3

2.78 6 1.11 1.07 6 0.66 0.88 6 0.04

0.002 ,0.001 0.337 (not significant)

38.31 68.2 1.1

*Vmax = mean peak flow; TAMx = time average velocity maximum; TAMn = time average velocity mean; RI = resistive index.

disciplines were performed by the participants, including running, swimming, soccer, crossfit, and gymnastics. The participants performed SMR 2–3 times per week. The local ethics committee approved the conduct of the study with no requirements (University of ErlangenNuremberg, Erlangen, Germany). All participants were informed of the benefits and risks of the investigation before signing an institutionally approved informed consent document to participate in the study. Procedures

Ultrasound Examination and Data Collection. Data were collected at our department of radiology at a room temperature of 218C. All measurements were conducted by senior author Heiß, R. (radiologist with expert knowledge in ultrasound examination) and were obtained using the Siemens ACUSON Antares Premium Edition ultrasound system (Siemens, Erlangen, Germany) using a linear multifrequency probe (VFX13-5; Siemens). Baseline B-mode ultrasound with a frequency of 10 MHz was performed before PDS for anatomical orientation. The following anatomical sections were defined for data analysis (Figure 1): Proximal portion (PP) (distal trochanter major), mid portion (MP) (0–50% length between proximal and distal portion), and distal portion (DP) (distal insertion of the iliotibial band; Gerdy’s tubercle was chosen as the landmark). The power Doppler settings were as follows: a sample volume with a size of 1.5 3 2.5 cm (placed from the epifascial subcutaneous tissue to the subfascial muscle tissue), frequency of 6.2 MHz, pulse repetition frequency of 488 Hz, color gain at a constant level for all measurements at which no noise artifacts appear. For each section, data were assessed in a longitudinal and transversal scan. In total, 3 trials were performed. First, ultrasound data were assessed under resting conditions (after 20 minutes of rest at horizontal lying position) to define baseline values. The second and third trials were performed

immediately after and 30 minutes after the foam rolling intervention (early postintervention phase [EPIP]; late postintervention phase [LPIP]). Probe positions were marked during the first trial using a permanent marker to ensure identical probe position for the following postintervention trials (Figure 1). Quantitative blood flow parameters represented as mean peak flow (Vmax), time average velocity maximum (TAMx), time average velocity mean (TAMn), and resistive index (RI) ([peak systolic velocity 2 end diastolic velocity]/peak systolic velocity) were obtained from 5 measurement repetitions each for the distal portion, as it was the only section that represented a sufficient amount of blood vessels that allowed a reliable pulsed waved Doppler analysis. The gate was chosen with a diameter of 1 mm. For evaluating semiquantitative blood flow, ultrasound images were digitized as uncompressed TIFF files and were evaluated by 4 independent and blindfolded observers (1 radiologist, 1 orthopedic surgeon, 1 cardiologist, each with experience in Doppler ultrasound, and 1 medical student in their final clinical year). A subjective semiquantitative scoring system was used in accordance to prior published protocols to assess hyperperfusion (16,17,33,39). The following graduations were determined: grade 0 for none, grade I for minor, grade II for moderate, and grade III for major presence of intramuscular hyperperfusion (Figure 2). Exercise Intervention. The exercise protocol consisted of 3 sets, each with 45 seconds foam rolling on the lateral thigh in the sagittal plane (20 seconds of rest between sets). All foam rolling exercises were performed using a custommade foam roller (Blackroll AG, Bottighofen, Switzerland). It consists of expanded polypropylene and had an outer diameter of 15 cm, a length of 30 cm and at a thickness of 6 cm. One week in advance of the study, a physical therapist VOLUME 31 | NUMBER 4 | APRIL 2017 |

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instructed the participants regarding performing foam rolling exercises of the lateral thigh to ensure a proper execution on the measurement day. The participants were instructed to start in a side lying position, placing the upper leg on the surface. They rolled from the lateral tibia condyle upward to a position superior to the greater trochanter and back to the starting position (Figure 1). Both hands were allowed to guide the movement. Participants were instructed for all repetitions to place as much body mass as tolerable on the foam roller (25). Movement execution and velocity was kept constant as much as possible (1 rolling per 2 seconds) and controlled by a physical therapist. Statistical Analyses

Absolute values of peak flow (Vmax), TAMx, TAMn, RI, and mean grades of semiquantitative perfusion assessment were transferred to GraphPad Prism 6 software (GraphPad Software, Inc., San Diego, CA, USA). Values were checked for normality with the D’Agostino-Pearson test. In cases of normality, the paired t-test was applied; otherwise, the Wilcoxon matched-pair signed rank test was used. The paired t-test and the Wilcoxon matched-pair signed rank test were used to compare data from the EPIP and LPIP to resting conditions (baseline). p values of ,0.05 were regarded as statistically significant. The intraclass correlation coefficient (ICC) was used to assess the test-restest reliability using the statistical software package SPPS Version 21 (SPSS, Inc., Chicago, IL, USA). The interobserver reliability was determined by calculating Kendall’s w using the statistical software package SPPS Version 21 and the overall agreement (defined as the percentage of observed exact agreements, including all 4 raters) using Microsoft Excel 2010 (Microsoft Corporation, Redmond, WA, USA).

*The number of 168 assessments corresponds to 21 subjects, 2 probe orientations, and 4 blinded observers.

n = 168 (100) n = 168 n = 168 n = 168 n = 168 n = 168 n = 168 n = 168 n = 168 76 (45.2) 0 0 52 (31.0) 0 0 16 (9.5) 0 0 90 (53.6) 61 (36.3) 59 (35.1) 112 (66.7) 23 (13.7) 10 (6.0) 140 (83.3) 16 (9.5) 9 (5.4) 2 (1.2) 102 (60.7) 98 (58.3) 4 (2.4) 113 (67.3) 122 (72.6) 12 (7.1) 110 (65.5) 104 (61.9) 0 5 (3.0) 11 (6.6) 0 32 (19.1) 36 (21.4) 0 42 (25.0) 55 (32.7) 0.56 1.67 1.71 0.71 2.05 2.15 0.98 2.15 2.27 Total Grade 0 Grade I Grade II Grade III Average

EPIP Baseline EPIP EPIP Baseline Semiquantitative perfusion (grade 0–III)

Proximal portion (%)

TABLE 2. An overview of the semiquantitative scoring.*

LPIP

Baseline

Mid portion (%)

LPIP

Distal portion (%)

LPIP

Relationship of Foam Rolling and Arterial Tissue Perfusion

RESULTS All results are listed in detail in Tables 1 and 2 and Figure 3. For the calculated Doppler data and semiquantitative scores, a number of significant differences were recorded. When the 21 participants completed the study, we calculated the SD of the before-after difference of Vmax, TAMx, and TAMn for each of the trials. We are able to describe a difference of 20% between means (referred to baseline results) with a power of more than 90%. According to the semiquantitative grading, our results increased in the EPIP and in the LPIP, compared with baseline, clearly over all portions (Figure 4). The interobserver reliability showed an excellent correlation (Kendall’s w, 0.94) and a high overall agreement (81%). The test-retest reliability was evaluated before the examination date, according to the described investigation settings. Blood flow parameters were measured at the distal portion of 1 participant under resting conditions 4 times, each after 30 minutes. The ICC were between 0.77 and 0.92 (ICC, Vmax = 0.92; TAMx = 0.84; TM

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Figure 3. Mean peak flow (Vmax), time average velocity maximum (TAMx), time average velocity mean (TAMn), and resistive index (RI) (absolute value 6 SD) for 21 subjects for the following settings: resting conditions (baseline), early postintervention phase (EPIP), and late postintervention phase (LPIP).

TAMn = 0.77; RI = 0.83) and indicate a good (ICC . 0.75) and partly even excellent (ICC . 0.9) reliability (15). Detailed results for defined baseline and postintervention conditions are listed below.

Resting Conditions (Baseline Values)

Peak flow, TAMx, and TAMx values obtained from resting conditions were 7.2 6 2.6, 2.01 6 0.56, and 0.46 6 0.28 cm$s21, respectively. The Resistive index was 0.87 6 0.04. Semiquantitative assessment of hyperperfusion revealed an average grade of 0.56 (PP), 0.71 (MP), and 0.98 (DP). Early Postintervention Phase

Directly after foam rolling intervention, we observed peak flow values of 12.5 6 5.0 cm$s21 (DP) (p , 0.001). TAMx and TAMx values were 3.08 6 1.41 (p , 0.001) and 1.18 6 0.72 (p , 0.001), respectively. The resistive index was 0.89 6 0.04 (p = 0.016). The average of the corresponding semiquantitative grades was 1.67 for PP, 2.05 for MP, and 2.15 for DP. Late Postintervention Phase

Figure 4. Lateral longitudinal scan in power Doppler ultrasound modus of the mid section. Hyperperfusion scored by power Doppler ultrasound: grade 0 (A), grade II (B), and grade II (C). D) Spectral Doppler measurement at the distal section.

After 30 minutes after the intervention, blood flow values were 11.0 6 4.1 (p , 0.001) for Vmax, 2.78 6 1.11 (p = 0.002) for TAMx, and 1.07 6 0.66 VOLUME 31 | NUMBER 4 | APRIL 2017 |

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Relationship of Foam Rolling and Arterial Tissue Perfusion (p , 0.001) for TAMn. We detected a resistive index of 0.88 (p = 0.337, not significant). The average grades of the semiquantitative assessment were 1.71 for PP, 2.15 for MP, and 2.27 for DP.

DISCUSSION Foam rolling is commonly performed to improve performance and recovery and is recommended by many physical therapists and fitness professionals. Despite the extensive use and growing popularity of foam rolling in clinical use and research, only little data exist on the physiological outcomes. Changes in functional parameters, such as increased range of motion, are hypothesized to be based on altered viscoelastic and thixotropic property of the fascia, and increases in intramuscular temperature and blood flow are evoked by mechanical friction of the foam roller (1,6,21,23). However, currently, no study addresses such physiological parameters. Our results indicate that arterial blood flow of the lateral thigh obtained as Vmax, TAMx, and TAMn and a semiquantitative assessment increase directly after and 30 minutes after foam rolling exercises in comparison to resting conditions (p # 0.05). Given the current study design, blood flow improvement assessed directly after foam rolling corresponds to a relative increase of 73.6% (Vmax), 53.2% (TAMx), and 84.4% (TAMn) from baseline (p , 0.001). Even after 30 minutes, a statistically significant increase in tissue circulation can be detected and corresponds to relative increases of 52.7% (Vmax), 38.2% (TAMx), and 68.2% (TAMn) (p # 0.05). In addition, semiquantitative power Doppler scores at all portions revealed an increased average grading of 1.96 at EPIP and 2.04 at LPIP compared with 0.75 for baseline. Power Doppler ultrasound is a capable tool for the acquisition of perfusion in musculoskeletal assessment because of a high sensitivity to low-volume and lowvelocity blood flow at the microvascular level (38). The reliability and the simple application of a 4-staged perfusion grading system in PDS has been established by many authors (17,33,39) and confirmed by the excellent interrater correlation in this study (Kendall’s w, 0.94). Changes in tissue perfusion after foam rolling could be explained by vasoactive substances, such as nitric oxide (NO). Vasoactive substances are produced by vascular endothelial cells, which are intended to have an important role in the regulation of vascular constriction and dilatation (22,31). It is generally accepted that mechanical stress adapted on endothelial cells leads to the release of NO. Okamoto et al (24). observed a statistical significant increase in plasma NO concentration after self-myofascial release and concluded that foam rolling reduced arterial stiffness and improved vascular endothelial function. It could be argued that blood vessel compression evoked by foam rolling might distort the vascular endothelium, which could trigger the release of NO (24). Another pathway of this enhancement in blood flow could be based on changes in parasympathetic and sympathetic activation followed by the actions of

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stretch-activated mechanoreceptive muscle afferent fibers (9). However, the exact mechanisms responsible for the increase in blood flow remain unclear. Nevertheless, our findings may be significant for the practical use of foam rolling. The advantages of enhanced blood flow are relevant for warm-up and recovery, and our data support the implementation of foam rolling if tissue circulation is required. Otherwise, foam rolling should be renounced in cases of acute inflammatory processes in regard of adverse effects like reinforced inflammatory responses. This could be relevant for the management of traumatic injuries or for cases of bursitis or arthritis, whereas a cold application leading to vasoconstriction is generally recommended (7,35). Although circulation has been described as an essential role in tissue healing (19), numerous recent studies focused on comparing different interventions regarding their effectiveness on tissue circulation and blood flow. Massage, a widely used physiotherapeutic technique including soft tissue manipulation, is generally recommended to enhance local blood flow. However, there is a wide variety of massage techniques and a lack of homogenous data representing its effects on tissue circulation. Some studies reported that massage therapy improves blood circulation (4,10,28), whereas other studies suggest that it does not (12,29,36,40). A study comparing acute effects of matrix rhythm therapy and massage on the peripheral blood circulation assessed with PDS (popliteal and posterior tibial artery) reported an increase of up to 34% Vmax after rhythm therapy and 18% Vmax after massage therapy (34). Other studies investigating different mechanical vibratory devices also reported an increase in blood flow, revealing a relative increase between 20 and 46% (3,42). A study dealing with the acute effects of ThermaCare HeatWraps (Pfizer Consumer Healthcare, Madison, NJ, USA) on tissue perfusion by means of laser flowmetry observed an increase in blood flow of the skin and muscle of 109 and 149%, respectively (26). Comparing our data to the above-mentioned effects of massage and warming therapy on local blood flow, the obtained increase in blood flow after SMR can be considered between both techniques and blood flow changes until 30 minutes after SMR. The limitations of our study are recognized. First, our data are representative of the applied study setting and have to be considered cautiously if a different setting is chosen. The study consists of healthy participants with experiences in foam rolling. The participants’ experience, participants’ body weight (changes of local compression), the volume of foam rolling exercises, the type of foam roller, and the interaction with additional training exercises have to be seen as influencing parameters on tissue perfusion. Second, our data represent only short-term effects on arterial tissue perfusion up to 30 minutes after foam rolling. Long-term observation of changes in tissue perfusion (i.e., a question of neovascularization) in experienced and nonexperienced participants could be a prospect for future research. Third, Vmax, TAMx, TAMn, and the semiquantitative grading score were defined

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Taken together, our results indicate that blood flow of the lateral thigh increases significantly after foam rolling exercises in healthy participants. The advantages of enhanced blood flow are relevant for warm-up and recovery, and our data support the implementation of foam rolling if tissue circulation is required. It is remarkable that changes in local blood after foam rolling can be detected until 30 minutes after performing foam rolling, following multiple pathways leading to an increase in local blood flow. Our data may contribute to the understanding of local physiological reactions of self-myofascial release, and this study opens the possibility for further investigations of changes in local blood flow in the context of SMR.

PRACTICAL APPLICATIONS To our knowledge, our study is the first to investigate the role of foam rolling on arterial tissue perfusion. Increases in arterial blood flow suggest a role for the acute phase after foam rolling. Our data may contribute to the ongoing discussion and understanding of local physiological reactions of self-myofascial release. The advantages of enhanced blood flow might be important for warm-up and recovery, and our data support the implementation of foam rolling in sports if tissue circulation is required. Otherwise, foam rolling should be renounced in the case of acute inflammatory reactions, such as adverse effects like reinforced inflammatory responses.

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Journal of Strength and Conditioning Research

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Acute Effects of Lateral Thigh Foam Rolling on Arterial Tissue Perfusion Determined by Spectral Doppler and Power Doppler Ultrasound.

Hotfiel, T, Swoboda, B, Krinner, S, Grim, C, Engelhardt, M, Uder, M, and Heiss, R. Acute effects of lateral thigh foam rolling on arterial tissue perf...
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