SKINFOLD THICKNESS IS RELATED TO CARDIOVASCULAR AUTONOMIC CONTROL AS ASSESSED BY HEART RATE VARIABILITY AND HEART RATE RECOVERY

MICHAEL R. ESCO,1 HENRY N. WILLIFORD,

1

AND

MICHELE S. OLSON

Department of Physical Education and Exercise Science, Human Performance Laboratory, Auburn University Montgomery, Montgomery, Alabama

ABSTRACT
Esco, MR, Williford, HN, and Olson, MS. Skinfold thickness is related to cardiovascular autonomic control as assessed by heart rate variability and heart rate recovery. J Strength Cond Res 25(8): 23042310, 2011The purpose of this study was to determine if heart rate recovery (HRR) and heart rate variability (HRV) are related to maximal aerobic tness and selected body composition measurements. Fifty men (age = 21.9 6 3.0 years, height = 180.8 6 7.2 cm, weight = 80.4 6 9.1 kg, volunteered to participate in this study. For each subject, body mass index (BMI), waist circumference (WC), and the sum of skinfolds across the chest, abdomen, and thigh regions (SUMSF) were recorded. Heart rate variability (HRV) was assessed during a 5-minute period while the subjects rested in a supine position. The following frequency domain parameters of HRV were recorded: normalized highfrequency power (HFnu), and low-frequency to high-frequency power ratio (LF:HF). To determine maximal aerobic tness (i.e., _ O2max), each subject performed a maximal graded exercise V test on a treadmill. Heart rate recovery was recorded 1 (HRR1) and 2 (HRR2) minutes during a cool-down period. Mean _ O2max and BMI for all the subjects were 49.5 6 7.5 V mlkg21min21 and 24.7 6 2.2 kgm22, respectively. Although _ O2max, WC, and SUMSF was each signicantly correlated to V HRR and HRV, only SUMSF had a signicant independent correlation to HRR1, HRR2, HFnu, LF:HF (p , 0.01). The results of the regression procedure showed that SUMSF accounted for the greatest variance in HRR1, HRR2, HFnu, and LF:HF (p , 0.01). The results of this study suggest that cardiovascular autonomic modulation is signicantly related to maximal aerobic tness and body composition. However, SUMSF appears to have the strongest independent relationAddress correspondence to Michael R. Esco, mesco@aum.edu. 25(8)/23042310 Journal of Strength and Conditioning Research 2011 National Strength and Conditioning Association

ship with HRR and HRV, compared to other body composition _ O2max. parameters and V

KEY WORDS body composition, maximal oxygen consumption,

heart control, exercise

INTRODUCTION

ndurance-trained subjects tend to have lower heart rates at rest compared to nonathletic individuals (28). One reason for this discrepancy is because of differences in autonomic nervous control of the cardiovascular system (28). Most studies agree that exercise training enhances parasympathetic inuence of the heart (3,6,8,11,16). Regarding this context, heart rate recovery (HRR) after exercise and heart rate variability (HRV) under resting conditions have become widely used indicators of cardiovascular autonomic modulation (9,27,29). Heart rate recovery represents the fall in heart rate immediately after cessation of exercise and is primarily because of the return of parasympathetic, or vagal, nervous activity (9). Heart rate variability is described as the variation that occurs between successive heart beats (30). Spectral analysis of HRV has been shown to be capable of capturing sympathovagal balance during short-term recordings (30). The primary popularity of both HRR and HRV is because of their noninvasive prognostic value in predicting the occurrence of fatal ventricular arrhythmias and sudden cardiac death, even in apparently healthy subjects (14,17,21). Furthermore, autonomic dysfunction at young ages has been suggested to predict the early development of cardiovascular disease (12,23). Therefore, the 2 autonomic measures can play an important supplementary role in traditional health and tness screenings in determining high-risk subjects. There is substantial evidence to show that autonomic control of heart rate is related to body composition and aerobic tness. For example, poor HRR and HRV have been associated with higher body mass index (BMI) levels, larger waist circumference (WC) measurements, and higher body fat percentages (2,20,21). When

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_ O2max), were compared to (V HRR after maximal exercise TABLE 1. The abbreviations to the heart rate recovery and heart rate variability and to resting HRV. The aforeparameters used in the study. mentioned body composition variables were chosen because HRR Heart rate recoverythe fall in heart rate immediately afters exercise they are easy to administer and MHR Maximal heart rate are commonly used in clinical _ O2max HR1 The heart rate recorded at 1-min post-V (17) and eld settings (13). In _ O2max HR2 The heart rate recorded at 2-min post-V addition, they have been shown HRR1 1-min heart rate recovery, which was to have a strong relationship to the difference between MHR and HR1 HRR2 2-min heart rate recovery, which was overall health, performance the difference between MHR and HR2 and cardiovascular disease risks HRV Heart rate variabilitythe variation (13,17,22). After the body combetween successive heart beats position variables were meaHFnu Normalized high-frequency component sured, each subject rested of the HRV power spectrum (0.150.40 Hz), which was recorded to represent quietly in a supine position for parasympathetic modulation 10 minutes during which HRV LFnu Normalized low-frequency component was analyzed. Then, a maximal of the HRV power spectrum (0.040.14 Hz) treadmill test was performed to LF:HF The LFnu to HFnu ratio which was recorded _ O2max and HRR. determine V to represent sympathetic to parasympathetic balance Heart rate recovery was monitored for 2 minutes of a cooldown period during which the subjects walked at a speed of comparing different tness groups, most cross-sectional studies 2.5 mph at 1.5% grade. The independent variables were _ O2max and the selected body composition parameters (i.e., have shown faster HRR and higher HRV in t vs. unt individuals V (3,25). Longitudinal investigations have shown an improvement BMI, WC, and SUMSF). These were compared to HRR and in HRR and HRV after dietary weight loss interventions (2,10), HRV, which served as the dependent variables. Table 1 prolonged endurance-training programs (3,6,8,11,16), and combiprovides a summary of the HRR and HRV parameters used nations of both (5). Thus, HRV and HRR have also become in the study. popular tools to monitor the positive cardiovascular benets that Subjects occur with weight loss and with aerobic exercise training. Fifty apparently healthy young adult men (age = 21.9 6 3.0 The distinct inuences of aerobic tness and body composition years, height = 180.8 6 7.2 cm, weight = 80.4 6 9.1 kg) on cardiovascular autonomic control may be frequently volunteered to participate in this study. All data were confounded because aerobically t subjects generally have collected between 7:00 AM and 11:00 AM on any day of the a healthy body composition. Most studies have investigated the week (Monday through Friday). Before the testing proce_ O2max) relationship between maximal oxygen consumption (V dures began, each subject was asked not to eat or consume and HRVor HRR without regard for body composition and vice caffeinated beverages for 12 hours and not to consume versa. Furthermore, there are no studies that have attempted to alcohol 24 hours before the testing procedures. The subjects examine the relationship between cardiovascular autonomic were also asked to avoid strenuous exercise for 24 hours before modulation and the simple body composition eld measurement data collection. After receiving detailed instruction regarding the of skinfold thickness. Therefore, the purpose of this study was study purpose, methods, and risks, subjects provided appropriate twofold: (a) determine if cardiovascular autonomic modulation written informed consent and were told that they could was related to aerobic tness, BMI, WC, and sum of skinfold withdraw from the study at any time without any bias. The thickness across the chest, abdomen, and thigh regions subjects then completed health-history questionnaires. Those (SUMSF); and (b) to demonstrate which of the independent subjects who were apparently healthy; free from cardiopulmovariables was the strongest predictor of HRR and resting HRV. It nary, metabolic, and orthopedic disorders; and currently not was hypothesized that all of the studied variables would be taking any prescription or over-the-counter medications were related to HRR and HRV but that aerobic tness would be the included in the data collection process. This study was greatest predictor to both autonomic measures. approved by the Universitys Institutional Review Board for research involving human subjects. METHODS
Experimental Approach to the Problem Body Composition

Body mass index, WC, and SUMSF across 3 sites were analyzed in male participants and, along with aerobic tness

Height was measured with a wall-mounted stadiometer (SECA; Seca Instruments Ltd, Hamburg, Germany) to the nearest
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Skinfold Thickness and Cardiac Autonomic Control

TABLE 2. Descriptive statistics of the studied variables.* Variable _ O2max (mlkg min V BMI (kgm22) WC (cm) SUMSF (mm) HRR1 (bmin21) HRR2 (bmin21) HFnu (ms2) LF:HF
21 21

TABLE 4. Partial correlation coefcients (r) showing the independent relationship between the variables.* Max 66.3 29.8 97.8 64.5 34.0 65.0 64.5 2.0 HRR1 HRR2 HFnu LF:HF _ O2max V 0.07 0.29 0.11 0.07 BMI 0.04 0.09 20.20 20.15 WC 0.10 20.03 20.01 20.17 SUMSF 20.42 20.47 20.44 0.53

Mean 6 SD Min ) 49.5 24.7 83.0 45.9 20.3 42.7 45.9 1.0 6 7.5 6 2.2 6 6.6 6 8.2 6 6.1 6 9.7 6 8.2 6 0.3 35.9 19.3 71.1 28.4 10.0 24.0 28.4 0.4

*BMI = body mass index; WC = waist circumference; SUMSF = sum of skinfold thickness; HRR1 = 1-minute heart rate recovery; HRR2 = 2-minute heart rate recovery; HFnu = normalized high frequency of heart rate variability; LF:HF = low-frequency to high-frequency ratio.

*BMI = body mass index; WC = waist circumference; SUMSF = sum of skinfold thickness; HRR1 = 1-minute heart rate recovery; HRR2 = 2-minute heart rate recovery; HFnu = Normalized high frequency of heart rate variability; LF:HF = low frequency to high frequency ratio. Signicantly related, p , 0.01.

0.5 cm. The subjects stood erect, without shoes, and with their hands on their sides. Body weight was measured with a digital scale (Tanita BWB-800A, Tanita Corp, Tokyo, Japan) to the nearest 0.5 kg. Body mass index was calculated as weight (kg), divided by height (m2), and rounded to the nearest 0.1 kgm22. Waist circumference was measured at the level of the umbilicus with a retractable tape measure (Mabis, Tokyo, Japan) to the nearest 0.5 cm while the subjects stood erect. Skinfold measurements were obtained for each subject by the same trained technician with the use of calibrated skinfold calipers (Harpenden; Baty International, West Sussex, United Kingdom). For this individual, intraclass correlation coefcient within each skinfold measurement was r = 0.99. Skinfolds were measured from 3 sites on the right side of the body as follows: a chest skinfold measurement was obtained from a diagonal skinfold on the chest half way between the nipple and the

anterior axiallary line; an abdominal skinfold measurement was obtained from a vertical fold on the abdomen 2 cm to the right of the umbilicus; and a thigh skinfold measurement was obtained with a vertical fold on the anterior midline of the thigh half way between the proximal border of the patella and the inguinal crease (1). All of the sites were measured in rotating order. At least 3 measurements were taken at each site, and the average was calculated. All of the measurements were rounded to the nearest 0.5 mm and were within 2 mm of each other. The values of the 3 sites were totaled and recorded as SUMSF.
Heart Rate Variability

TABLE 3. Zero-order correlation coefcients (r) showing the relationship between the variables.* _ O2max V HRR1 HRR2 HFnu LF:HF 0.17 0.47 0.14 20.17 BMI 20.01 0.17 20.01 0.08 WC 20.07 20.39 20.16 0.10 SUMSF 20.37 20.61 20.40 20.44

*BMI = body mass index; WC = waist circumference; SUMSF = sum of skinfold thickness; HRR1 = 1-minute heart rate recovery; HRR2 = 2-minute heart rate recovery; HFnu = normalized high-frequency of heart rate variability; LF:HF = low-frequency to high-frequency ratio. Signicantly related, p , 0.05. Signicantly related, p , 0.01.

After the body composition variables were measured and recorded, each subject was instructed to lay supine on an athletic training table in a dimly lit climate controlled laboratory for a 10-minute period. During this time, the subjects heart rate was assessed by electrocardiography (ECG). Electrodes were placed across the subjects chest in a Lead II conguration. The electrodes were interfaced with a Biopac MP100 data acquisition system (Goletta, CA, USA), and all data were stored in a Dell PC for analysis. The ECG recordings were visually inspected and any ectopic beats were removed and replaced by the adjacent normal RR interval. If 3 or more ectopic beats were found within any ECG segment, the reading was excluded from analysis. The last 5-minute period of the ECG recording was used for HRV analysis. The frequency domain analysis of HRV was used because of its ability to accurately assess HRV during short-term recordings (30). This procedure involved transforming the ECG into a power spectrum via fast Fourier transformation with the use of specialized HRV software (Nevrokard version 11.0.2, Izola, Slovenia). The area under the highfrequency component of the power spectrum (0.150.40 Hz) was normalized (HFnu) and recorded to represent parasympathetic modulation. The low-frequency

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Figure 1. Scatter plots displaying the signicant independent relationships between SUMSF (y-axis) and the cardiovascular autonomic parameters (x-axis). SUMSF = the sum of skinfolds across the chest, abdomen, and thigh; HRR1 = 1-minute heart rate recovery; HRR2 = 2-minute heart rate recovery; HFnu = normalized high frequency component of the heart rate variability power spectrum (0.150.40 Hz), a marker of parasympathetic modulation; LF:HF = low frequency to high frequency ration, a heart rate variability marker that represents parasympathetic to sympathetic balance.

component of the power spectrum (0.040.14 also normalized (LFnu) and recorded but included in data analyses. However, the LFnu ratio (LF:HF) was recorded and included in

Hz) was was not to HFnu the data

analysis because it provides an acceptable assessment of sympathetic to parasympathetic balance (31). All HRV analyses were carried out in accordance with written guidelines for HRV assessment (30).
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Maximal Oxygen Consumption

After the resting measures were complete, each subject performed a maximal graded exercise test on a treadmill (Parker Co., Opelika, AL, USA). The Bruce protocol was employed during each exercise test, which incorporated a series of 3-minute stages with progressively increased _ O2max. During the workloads until the subjects achieved V test, an Applied Electrochemistry (Ametek, Pittsburg, PA, USA) metabolic analyzer was used to determine the concentration of expired gases (oxygen and carbon dioxide) via a continuous manner at the mouth with a pneumotach. All data were recorded every 30-seconds using Turbot 5.06 software (Vacumed, Ventura, CA, USA) and stored on a personal computer for analysis. Maximal oxygen consumption was reached if 2 of the following criteria occurred: _ O2 with increasing work rate; RER $ 1.15; a plateau in V heart rate within 10 beats of age-predicted maximum (220 _ O2max, age); or volitional fatigue. Once the subject achieved V a 3-minute cool-down period was allowed. During this time, the speed was decreased to 2.5 mph at a 1.5% grade.
Heart Rate Recovery

Table 4 represents the partial correlation coefcients between the independent and dependent variables. The signicant partial correlations between SUMSF and all the dependent variables remained. The partial correlation coefcient for the relationship between SUMSF and the dependent variables (Figure 1) was as follows: r = 20.42, p , 0.01 for HRR1, r = 20.63, p , 0.01 for HRR2, r = 20.44, p , 0.01 for HFnu, r = 20.53, p , 0.01 for LF:HF. However, no other independent variable showed a signicant partial correlation with the HRR or HRV parameters. The results of the stepwise regression procedures showed that SUMSF accounted for the greatest variance in HRR1 (R2 = 0.14, p , 0.01) and HRR2 (R2 = 0.43, p , 0.01). For the HRV parameters, the SUMSF accounted for the greatest variance in HFnu (R2 = 0.16, p , 0.01), and LF:HF (R2 = 0.20, p , 0.01). No other variable added statistical signicance (p . 0.05) to the regression models, above and beyond that of SUMSF, and therefore was removed from the models.

DISCUSSION
This investigation sought to determine if cardiovascular autonomic regulation was related to cardiorespiratory tness and the simple anthropometric measures of BMI, WC, and the sum of skinfolds from the chest, abdomen, and thigh regions (i.e., SUMSF) in a sample of apparently healthy young adult men. We chose 2 parameters, HRV and HRR, which appear to be independently linked to cardiovascular autonomic control (15). The results of this study found that cardiovascular autonomic modulation (i.e., HRR and HRV) was signicantly associated with aerobic tness and body composition. For example, SUMSF held signicant negative correlations with HRR1 and HRR2. Furthermore, there were _ O2max and HRR2 signicant positive correlations between V and signicant negative correlations between WC and HRR2. Only SUMSF had a signicant inverse relationship with HFnu and a signicant positive relationship to LF:HF. These ndings would indicate that HRR is faster at higher _ O2max levels and lower for WC and SUMSF measureV ments. Moreover, HFnu and LF:HF ratio appear to be higher and lower, respectively, in subjects with lower SUMSF values. Body mass index, however, did not signicantly correlate with any of the HRR or HRV variables, which is in contrast to previous ndings (7,22). The results of the partial correlation procedures revealed a signicant correlation between SUMSF and the HRR and HRV parameters. No other independent variable showed a signicant partial correlation with the autonomic markers. Therefore, SUMSF was the only variable to have a signicant independent relationship with HRR and HRV. These results were supported by the stepwise regression procedures, which revealed the interesting nding that SUMSF was the strongest predictor of HRR1, HRR2, HFnu, and LF:HF ratio. Specically, SUMSF accounted for a signicant 14% of the variation in HRR1, 43% of the variation in HRR2, 16% of

_ O2max was The heart rate value that corresponded to V recorded as maximal heart rate (MHR). Heart rate was also recorded at 1 (HR1) and 2 (HR2) minutes during the cooldown period, which were subtracted from MHR and recorded as HRR 1-minute (HRR1) and HRR 2 minutes (HRR2), respectively.
Statistical Analyses

All statistical analyses were completed using SPSS version 16.0. Means (6SD) were determined for all of the recorded variables. Zero-order correlations were used to determine the relationship between the independent variables (i.e., the selected body _ O2max) and the markers of composition parameters and V cardiovascular autonomic modulation (i.e., HRR1, HRR2, HFnu, and LF:HF). Partial correlations were also performed to determine the specic correlation between the independent and dependent variables when controlling for the potential confounders. Stepwise regression procedures were carried out to determine which of the independent variables could account for the greatest variation in each of the autonomic measures. A priori statistical signicance for all tests was set at p # 0.05.

RESULTS
Table 2 shows the means (6SD) of all the recorded variables, and Table 3 represents the zero-order correlation coefcients between the independent and dependent variables. The sum of skinfolds was the only variable to have a signicant correlation with HRR1 (r = 0.37, p , 0.05). For HRR2, there were _ O2max (r = 0.47, p , 0.01), signicant correlations found for V WC (r = 0.39, p , 0.01), and SUMSF (r = 20.61, p , 0.01). The only variable to have a signicant relationship with HFnu and LF:HF was SUMSF (r = 20.40, p , 0.01, r = 0.44, p , 0.01, respectively). No other variable signicantly correlated with either HFnu or LF:HF (p . 0.05).

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the variation in HFnu, and 20% of the variation in the LF:HF _ O2max was excluded from all of the ratio. To our surprise, V _ O2max would regression models. Thus, our hypothesis that V have the strongest relationship with HRR and HRV was _ O2max), BMI, rejected. Maximal oxygen consumption (i.e., V and WC did not add statistical signicance, above and beyond that of SUMSF, to the stepwise regression procedures and were removed from the models. Therefore, the signicant relationships between the variables confounded each other. It appears that being aerobically t, having low BMI, and having low WC provide no additional benet to having low subcutaneous skinfold thicknesses on improved cardiovascular autonomic function in young adult men. Although the results of a number of cross-sectional and longitudinal studies show a greater HRR and HRV in trained individuals (4,8,16,25), others do not show an association between aerobic tness and autonomic modulation (7) or have reported no signicant HRV improvements after endurance training (31). Furthermore, there appears to be no signicant difference in either HRR (25) or HRV (4) between aerobically trained and anaerobically trained athletes. Therefore, the exercise-induced improvements in cardiovascularautonomic regulation that occur with prolonged exercise could perhaps be linked to the improvement of other trainable characteristics rather than to just endurance tness. Previous investigations have shown that cardiovascular autonomic regulation is signicantly related to body composition. For example, Lin et al. (20) showed that WC has the strongest relationship with HRR compared to any other marker of the metabolic syndrome (e.g., C-reactive protein, blood pressure, etc.). Miller et al. (21) found signicant correlations between HRV and body fat percentage, but not BMI, which support our ndings. We did not directly assess body fat percentage in this study. However, the SUMSF is commonly used to estimate body fat percentage and had the strongest relationship with the autonomic markers compared to any other variable. Furthermore, although weight loss from caloric reduction has been shown to improve autonomic regulation (2), there appears to be an even greater effect with the addition of exercise (5,10). Aerobically trained individuals typically display healthier body composition values compared to their sedentary counterparts. Thus, the difference in cardiovascularautonomic control between those with higher vs. lower aerobic tness levels could predominately be linked to the tter subjects having a healthier body composition prole (e.g., lower body fat percentages). If this were the case, HRR and HRV could possibly be improved to a greater extent with exercise training that induces an enhanced body composition instead of only an improvement in aerobic tness. Obviously, further investigation is warranted that would involve longitudinal investigation on the effects of exercise training with and without weight loss on HRR and HRV.

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There are a few limitations and delimitations concerning the present investigation: First, we were limited to only apparently healthy, young adult men. There are sex- and agerelated differences in the cardiovascular parameters that were studied (8). We cannot generalize our ndings to other populations, such as women and older-aged subjects. Second, we did not assess overall physical activity, which can inuence cardiovascular autonomic modulation independent of the level of tness (3,16).

PRACTICAL APPLICATIONS
Exercise physiologists, strength and conditioning professionals, coaches, nurses, physical therapists, and sports medicine physicians should become aware of the importance of HRR and HRV. Heart rate recovery is a cardiovascular marker with important implications that can be easily assessed within a eld situation. All that is required with HRR is an accurate measurement of heart rate at the cessation of exercise and at a certain time point during recovery, usually 1 or 2 minutes postexercise. The measurement of HRV has primarily been performed in laboratory and clinical conditions as an accurate, yet noninvasive representation of cardiac-autonomic function. However, there are a number of portable ECG systems and heart rate monitors that have the ability to assess HRV, which have allowed sports practitioners to use this technique in eld settings (4,19,24,32). Heart rate variability has been shown to be a benecial guide for prescribing exercise and a valuable tool to prevent overtraining (19,24). When combined with traditional cardiovascular evaluations, these measures can each provide a further insight into the physiological responses to an exercise training program. Both measures are also strong predictors of sudden cardiac death and the future development of premature cardiovascular disease in young subjects (18,23,26). Thus, they can offer important information that would otherwise not be obtained with simple health-history questionnaires or via regular tness appraisals. This study showed the importance of aerobic tness, and simple body composition measures in relation to cardiovascular autonomic control. We found that HRR and HRV were _ O2max, WC, and SUMSF. Thus, our signicantly related to V ndings strengthen the usefulness of aerobic tness and simple body composition measures in predicting cardiovascular disease risks. Of the variables analyzed in this study, SUMSF had the strongest independent relationship with HRR and HRV. Therefore, it appears that body fat percentage, which is commonly estimated with the use of the skinfold technique, is related to cardiovascular autonomic modulation more than aerobic tness, BMI, or WC.

ACKNOWLEDGMENTS
This study was partially funded by an internal grant provided by Auburn University Montgomerys Sponsored Programs. The authors would like to thank Ms. Angela Russell and Ms. Kelly Gaston for their assistance with the data collection process.
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