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Muscle pain and blood pressure responses during isometric handgrip exercise in healthy African American and non-Hispanic White adults
Physiology & Behavior 138 (2015) 242–246
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Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Muscle pain and blood pressure responses during isometric handgrip exercise in healthy African American and non-Hispanic White adults Masataka Umeda ⁎, Jon P. Williams, Courtney A. Marino, Shelby C. Hilliard Department of Health, Exercise, and Sport Sciences, Texas Tech University, Lubbock, TX, USA
H I G H L I G H T S • African Americans experience more pain during exercise than non-Hispanic Whites. • Muscle pain increases more rapidly during exercise in African Americans. • Blood pressure responses during exercise are similar in the two groups.
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Article history: Received 8 April 2014 Accepted 29 September 2014 Available online 24 October 2014 Keywords: Pain sensitivity Exercise Blood pressure Race and ethnicity
a b s t r a c t It has been shown that African Americans (AAs) are more sensitive to experimental pain stimuli compared to non-Hispanic Whites (NHWs). A single bout of exercise results in naturally-occurring muscle pain and elevation in blood pressure (BP); however, it is currently unclear whether AAs and NHWs differ in muscle pain and BP responses during exercise. Therefore, we examined the differences in muscle pain and blood pressure (BP) during isometric handgrip exercise in African Americans (AAs) and non-Hispanic Whites (NHWs). Fourteen AAs and 14 NHWs completed isometric exercise consisting of squeezing a hand dynamometer at 25% of maximal strength for 3 min. During exercise, muscle pain ratings (MPRs) were assessed every 30 s, whereas systolic and diastolic BP (SBP and DBP) were recorded every minute. During exercise, AAs generally reported greater MPR than NHWs (p b 0.001), and MPR increased more rapidly during exercise in AAs than NHWs (p b 0.05). In contrast, SBP and DBP continued to increase similarly during exercise in both AAs and NHWs (p N 0.05). The results suggest that AAs generally experienced a greater intensity of muscle pain than NHWs during isometric handgrip exercise, but both groups exhibited similar elevations in BP during exercise. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Growing evidence from experimental studies indicates that African Americans are generally more sensitive to experimental pain stimuli than other races. For example, previous research indicates that African Americans exhibited lower tolerances to heat, cold, and ischemic pain stimuli [1–6], and rated heat pain stimuli higher [1,4,7] in comparison to non-Hispanic Whites. In addition, a physiological study demonstrates that the nociceptive flexion reflex, a spinal reflex induced by noxious stimulation that is modulated by spinal and supraspinal pain mechanisms (e.g., cerebral cortex, cerebellum, brainstem) [8,9], was elicited with lower intensity electrical stimulation in African Americans compared to non-Hispanic Whites [10]. Furthermore, Campbell et al. [11] examined a conditioned pain modulation consisting of assessing the ⁎ Corresponding author at: Department of Health, Exercise, and Sport Sciences, Texas Tech University, Box 43011, Lubbock, TX 79409, USA. Tel.: +1 806 834 3475; fax: +1 806 742 1688. E-mail address: [email protected] (M. Umeda).
http://dx.doi.org/10.1016/j.physbeh.2014.09.013 0031-9384/© 2014 Elsevier Inc. All rights reserved.
reductions in electrical pain ratings during concurrent application of ischemic pain, and reported that non-Hispanic Whites exhibited greater reductions in electrical pain ratings during concurrent application of ischemic pain compared to African Americans. Conditioned pain modulation has been found to be mediated by a specific region in the medulla, the subnucleus reticularis dorsalis; therefore, it has also been used to assess the function of central pain modulation [12,13]. Together, these observations collectively suggest that African Americans have higher sensitivity to experimental pain stimuli compared to non-Hispanic Whites, and that this is partly due to an impairment of pain modulatory systems within the central nervous system. Central pain modulation can also be assessed using other psychophysiological techniques. For example, numerous studies have been conducted examining the association between pain sensitivity and resting blood pressure (BP) in humans and animals, and results indicate an inverse association between pain sensitivity and resting BP [14–16]. Furthermore, previous research indicates that acute elevations in BP, caused by pharmacological or behavioral interventions (e.g., exercise), are also accompanied by reduced sensitivity to experimental pain
M. Umeda et al. / Physiology & Behavior 138 (2015) 242–246
stimuli [17]. Animal research demonstrates that several brain sites (e.g., rostral ventromedial medulla, nucleus tractus solirarius) are involved in the control of both BP and pain, and it has been suggested that elevated BP may initiate descending pain modulation via activation in these brain sites, resulting in decreased pain sensitivity [14,15]. Mechlin et al. examined the relationship between subjective responses to experimental pain stimuli and BP responses in African Americans and non-Hispanic Whites, and found that African Americans did not have an inverse association between pain sensitivity and BP, whereas the inverse association was confirmed in non-Hispanic Whites [4]. Therefore, the results suggest an impaired central pain modulation associated with BP elevations in African Americans. Exercise is a potent behavioral stimulus that acutely elevates BP [18, 19], and produces naturally-occurring pain in exercising muscles [20, 21]. A previous study demonstrates that even low intensity, short duration isometric handgrip exercise produces significant elevations in BP and a moderate intensity of muscle pain in the exercising forearm in healthy young adults [27]. These observations suggest that submaximal isometric handgrip exercise may be an optimal behavioral stimulus that can be used to examine the racial/ethnic differences in muscle pain and BP responses; however, no study has been conducted to compare muscle pain and BP responses during exercise in African Americans and non-Hispanic Whites. Therefore, the purpose of the present study was to examine whether African Americans and non-Hispanic Whites differ in muscle pain and BP responses during submaximal isometric exercise. 2. Materials and methods 2.1. Participants Healthy adults who identified themselves as African American or non-Hispanic Whites were recruited to participate in this study using an advertisement that was circulated via the campus-wide electronic mailing system and study flyers that were posted on designated places for public announcement on campus. The inclusion criteria for this study were 1) 18 to 30 years of age, 2) self-identification as African American or non-Hispanic White, 3) no medical conditions diagnosed by their physician, and 4) no medication use. Subjects were excluded from the study if 1) they indicated medical contraindications for exercise, 2) they were pregnant or breastfeeding at the time of screening, or 3) they were unable to understand instructions in English. The two groups were matched based on age (±3 years) and gender. The study protocol was fully approved by an institutional review board, and all participants signed a consent form before participating in the study. Power analysis was performed to estimate a sample size necessary to detect significant group differences in muscle pain during exercise in African Americans and non-Hispanic Whites. To perform the analysis, effect size (Cohen's d) was first calculated based on our pilot data, and the calculated effect size (d = 1.2), an α = 0.05, and a power = 0.80 were then used for the analysis [22]. The power analysis indicated that approximately 12 African Americans and 12 non-Hispanic Whites would be needed for the study. 2.2. Procedures The participants were asked to visit our laboratory once to complete a study session examining muscle pain and BP responses during isometric handgrip exercise. All study sessions were conducted by trained staff between 0900 and 1800 h, and the participants were asked to refrain from 1) strenuous exercise for 12 h, 2) alcohol consumption for 12 h, 3) caffeine intake for 3 h, and 4) smoking for 2 h before the study to accurately assess resting BP [23,24]. Upon arrival at the lab, the participants were first asked to sign a consent form, and then to complete questionnaires regarding demographics and general health, and regular physical activity (PA) levels using the Baecke Physical Activity Questionnaire (BPAQ) [25]. The
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BPAQ is a validated self-report questionnaire to quantify PA levels, and it consists of three subscales to estimate work-, sport-, and leisurerelated PA [25,26]. The work-related PA subscale assesses the type of occupation and the activity levels associated with their occupation. The sport-related PA subscale quantifies the amount of PA the participants are recreationally engaging in, whereas the leisure-related PA subscale quantifies the amount of PA except for recreational PA. Therefore, the leisure-related PA includes, for example, activities associated with the participants' daily commuting and TV-viewing. Each subscale quantifies the specific domain of PA, and total scores from the three subscales represent the participants' total PA levels. The investigator then prepared the participants for assessment of their resting BP by placing three electrodes on their chest and attaching a BP cuff around their non-dominant upper arm. Both electrodes and the BP cuff were connected to a small ECG device (Tango +, SunTech Medical, NC) that allowed the investigator to monitor BP periodically during the session. The participants were asked to remain seated in a comfortable chair for several minutes, and the investigator then assessed the participants' resting BP. Next, the investigator explained the exercise protocol to the participants, and then instructed them how to use the muscle pain rating (MPR) scale [20]. After the participants demonstrated understanding of the MPR scale with no further questions, they were informed that they would be rating muscle pain every 30 s during the exercise protocol. The participants were specifically instructed to rate the intensity of painful sensation in their forearm during exercise using the MPR scale. The MPR scale is constructed in a vertical alignment with 12 numbers (MPR 0, ½, 1–10), and has the corresponding verbiage next to nine numbers. The MPR scale ranges from no pain at all (MPR = 0) to extremely intense pain (MPR = 10), and also includes an unbearable pain option after the 10 rating if the participant experiences pain that exceeds the rating of extremely intense pain. The participants were then asked to squeeze a hand dynamometer (Model 78010, Lafayette Instrument, IN) with their dominant hand as hard as possible to assess their maximal voluntary contraction (MVC). The MVC assessment was conducted twice with sufficient rest between the trials, and the average of the two trials was used to compute 25% MVC for the subsequent exercise session. The participants were then asked to squeeze the hand dynamometer at 25% MVC and hold it at the target intensity as well as possible for 3 min. During this exercise, the investigator assessed MPR every 30 s, and BP every min. This exercise protocol was used because a previous study demonstrated that isometric handgrip exercise at 25% MVC for 3 min produces a moderate intensity of muscle pain in the forearm and significant elevations in BP in healthy adults [27]. The entire session took approximately 40 min to complete. 2.3. Data analyses The BPAQ was scored based on the published scoring method [25], and body mass index (BMI) was calculated using the following formula: BMI = weight (kg) / (height (m))2. Age, BMI, MVC, the BPAQ scores, and resting BP were compared between African Americans and nonHispanic Whites using an independent sample t-test to examine group differences in these variables. To test our primary hypotheses regarding whether African Americans would differ from non-Hispanic Whites in muscle pain and BP responses during isometric handgrip exercise, the MPR data were analyzed using a 2 (group: African American and non-Hispanic White) × 6 (time: every 30 s during 3 min of exercise) mixed model of repeated measures ANOVA, whereas the BP data were analyzed using a 2 (group: African American and non-Hispanic White) × 3 (time: every min during 3 min of exercise) mixed model of repeated measures ANOVA. Effect size was calculated using Cohen's d to assist in accurate interpretation of significant interaction effects where appropriate. Effect size was interpreted based on the following guideline: small effect = 0.2, medium effect = 0.5, and large effect = 0.80 [22].
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Correlational analyses were also performed to examine whether MPR was associated with BP using Pearson's correlation. For these analyses, MPR, SBP, and DBP during exercise were averaged over time, and resting SBP and DBP were included for the correlational analyses. The significance level was set at α = 0.05 for all statistical analyses. 3. Results 3.1. Participants Fourteen African American and 14 non-Hispanic White adults were recruited from the campus and completed this study. Each group consisted of nine men and five women, and all participants reported engaging in recreational exercise. Results from the analyses indicated that there were no significant differences between the two groups in age, BMI, MVC, resting BP, or BPAQ scores (t = − 1.36–1.61, p N 0.05). These characteristics are presented in Table 1.
10 Extremely Intense Pain 9 7 Very Strong Pain 6 5 Strong Pain 4 3 2 1 0
3.2. Muscle pain ratings during exercise Results from the MPR data analyses indicated a significant effect of time (F5, 22 = 28.46, p b 0.001), a significant effect of group (F1, 26 = 19.24, p b 0.001), and a significant time × group interaction (F5, 22 = 3.09, p b 0.05). Closer inspection of the data using effect size indicated that African Americans consistently reported a greater intensity of muscle pain than non-Hispanic Whites from the beginning of exercise, and this difference in the MPR scores became progressively larger as exercise progressed (d = 0.74–1.74). These data suggest that African Americans generally experienced greater MPR during exercise compared to non-Hispanic Whites, and that MPR increased more rapidly in African Americans compared to non-Hispanic Whites. These changes in the MPR scores during exercise are illustrated in Fig. 1, and effect sizes for each time point are summarized in Table 2.
African Americans Non-Hispanic Whites
8 MPR Scores
244
30
60
90 120 Time (sec)
150
180
Fig. 1. The MPR responses during isometric handgrip exercise. African Americans reported a greater intensity of MPR compared to non-Hispanic Whites (p b 0.001), and MPR increased during exercise more rapidly in African Americans compared to non-Hispanic Whites (p b 0.05). The data indicate group means ± SE at each time point.
3.4. The association of MPR with BP Results from the correlational analyses indicated that averaged MPR during exercise was not associated with BP measures in African Americans or in non-Hispanic Whites (p N 0.05). The results for the association between MPR and BP are summarized in Table 3.
4. Discussion 3.3. Blood pressure responses during exercise The SBP and DBP responses during exercise were similar for African Americans and non-Hispanic Whites. There was a significant effect of time (SBP: F2, 25 = 23.41, p b 0.001 & DBP: F2, 25 = 29.14, p b 0.001); however, neither a group effect (SBP: F 1, 26 = 0.01, p N 0.05 & DBP: F1, 26 = 0.16, p N 0.05) nor a time × group interaction (SBP: F2, 25 = 2.21, p N 0.05 & DBP: F2, 25 = 3.15, p N 0.05) was significant. These results suggest that SBP and DBP continued to increase during exercise at a similar rate in both African Americans and non-Hispanic Whites. The SBP and DBP responses during exercise are illustrated in Fig. 2a and b, respectively.
Table 1 Characteristics of study participants.
Age (years) BMI (kg/m2) Resting SBP (mmHg) Resting DBP (mmHg) MVC (kg) BPAQ-Total BPAQ-Work BPAQ-Sport BPAQ-Leisure
African Americans
Non-Hispanic White
22.14 (2.88) 26.02 (3.08) 116.36 (13.13) 65.36 (12.54) 44.86 (15.49) 9.07 (1.48) 2.54 (0.59) 3.57 (0.95) 2.96 (0.91)
21.86 (2.98) 24.06 (3.38) 121.5 (12.27) 70.71 (7.81) 38.54 (11.86) 8.81 (1.48) 2.58 (0.83) 3.39 (1.22) 2.84 (0.53)
Numbers are means, and numbers in parentheses are standard deviations. BMI; body mass index. SBP; Systolic Blood Pressure. DBP; Diastolic Blood Pressure. MVC; maximal voluntary contraction. BPAQ; Baecke Physical Activity Questionnaire.
The present study examined possible racial/ethnic differences in muscle pain and BP responses during isometric handgrip exercise in healthy African American and non-Hispanic White adults. Results for muscle pain indicated that African Americans generally experience a greater intensity of muscle pain during exercise compared to age- and gender-matched non-Hispanic Whites, and that muscle pain intensity increases more rapidly during exercise in African Americans in comparison to non-Hispanic Whites. With regard to BP, both SBP and DBP continued to increase during exercise in a similar rate in both groups. Together, these findings extend the literature in this area by suggesting that African Americans experience a greater intensity of naturallyoccurring muscle pain during exercise compared to non-Hispanic Whites, whereas both African Americans and non-Hispanic Whites have similar changes in BP during exercise.
Table 2 Effect size analyses for MPR during exercise in African Americans and non-Hispanic Whites.
MPR-30 MPR-60 MPR-90 MPR-120 MPR-150 MPR-180
African Americans
Non-Hispanic Whites
Effect size (d)
1.18 (0.99) 1.79 (0.98) 2.86 (1.03) 3.71 (1.20) 4.86 (1.35) 5.93 (1.59)
0.57 (0.62) 1.11 (0.66) 1.64 (0.91) 2.25 (1.05) 2.71 (1.20) 3.21 (1.53)
0.74 0.82 1.26 1.29 1.68 1.74
Numbers are means, and numbers in parentheses are standard deviations. MPR; Muscle pain ratings at each time point (sec) during 3 min of exercise. Guidelines for effect size interpretation; Small for d = 0.20, Medium for d = 0.50, Large for d = 0.80.
M. Umeda et al. / Physiology & Behavior 138 (2015) 242–246
(a)
245
(b)
150
90
African Americans
African Americans
145 85
SBP (mmHg)
140
DBP (mmHg)
Non-Hispanic Whites
135
130
Non-Hispanic Whites 80
75
125 70 120
115
1
2
65
3
Time (minutes)
1
2
3
Time (minutes)
Fig. 2. a. The SBP responses during isometric handgrip exercise. SBP increased comparably during exercise in African Americans and non-Hispanic Whites (p N 0.05). The data indicate group means ± SE at each time point. b. The DBP responses during isometric handgrip exercise. DBP increased comparably during exercise similarly in African Americans and non-Hispanic Whites (p N 0.05). The data indicate group means ± SE at each time point.
The augmented muscle pain during exercise in African Americans is consistent with previous research documenting that African Americans are more sensitive to a variety of experimental pain stimuli compared to non-Hispanic Whites, including heat, cold, ischemic, and electrical stimuli [1–7]. The underlying physiological mechanisms for the racial/ethnic differences are currently unclear; however, an impairment of central pain modulation has been suggested to explain the racial/ethnic differences in pain responses. For example, it has been demonstrated that African Americans have a lower threshold to elicit a nociceptive flexion reflex [10], and a smaller magnitude of reduction in pain ratings during concurrent application of noxious stimulation [11] compared to nonHispanic Whites. Furthermore, an inverse association between pain sensitivity and BP has been found in previous research, and it has been suggested that descending pain modulation might be initiated by elevated BP, resulting in decreased pain sensitivity through activation in brain sites that are involved in both BP and pain control [14,15]. However, an experimental study by Mechlin et al. indicate that the inverse association between pain sensitivity and BP is not found in African Americans [4], suggesting altered pain modulation associated with BP elevation in African Americans. In the present study, we found that submaximal isometric handgrip exercise elevated BP comparably in African Americans and non-Hispanic Whites, and that African Americans experienced a greater intensity of muscle pain during exercise compared to non-Hispanic Whites. Therefore, the present results further suggest that augmented muscle pain during exercise may be due to differential central pain modulation associated with BP elevation in African Americans and non-Hispanic Whites.
Table 3 Correlations between MPR and BP measures. African Americans
Non-Hispanic Whites
Resting Average Resting Average Resting Average Resting Average SBP SBP DBP DBP SBP SBP DBP DBP MPRs −0.37
−0.41
MPRs; muscle pain ratings. SBP; Systolic Blood Pressure. DBP; Diastolic Blood Pressure.
−0.28
−0.09
0.13
0.20
0.24
0.11
Our findings, however, are not consistent with results from the studies reporting an inverse association between pain sensitivity and BP in non-Hispanic Whites [4]. It is currently unclear why we failed to replicate the inverse association between pain and BP in non-Hispanic Whites in this study; however, one likely possibility is that different pain induction techniques were used. We used naturally-occurring muscle pain during exercise as the experimental pain stimulus, whereas Mechlin et al. used experimentally-evoked pain with ischemia, cold, and heat [4]. Although an inverse association between pain sensitivity and BP is supported by ample empirical evidence from numerous experimental studies [14–17], only limited data currently exist regarding a possible relationship between muscle pain during exercise and BP, and previous research in this area appears to provide mixed results. For example, it has been demonstrated that muscle pain during submaximal dynamic handgrip exercise is not associated with BP in healthy adults, whereas a strong inverse correlation between muscle pain during exercise and BP is found at peak exercise intensity [28]. In contrast, Ray and Carter reported no association between muscle pain during isometric fatiguing handgrip exercise and BP in healthy adults [29]. Furthermore, Cook et al. found that muscle pain during a maximal exercise test is not associated with BP in African American women [30]. Together, it appears that the relationship between muscle pain during exercise and BP is still unclear, suggesting a need for more research in this area. Alternatively, the similar BP responses during exercise and the absent correlations between muscle pain and BP in both groups could suggest that BP elevation may not explain the augmented muscle pain in African Americans. Although exercise was used to produce pain in this study, there is a growing literature documenting that exercise can also reduce sensitivity to a variety of experimental pain stimuli in healthy adults [31,32]. This hypoalgesic phenomenon has been termed as exercise-induced hypoalgesia, and previous research demonstrates that exercise-induced hypoalgesia can be successfully elicited with submaximal isometric handgrip exercise in healthy adults [23,27,33,34]. Furthermore, exercise-induced hypoalgesia occurs in body regions distant from the exercised muscles (e.g., contralateral and bilateral alterations in pain sensitivity) [31,32], suggesting the involvement of central pain mechanisms in exercise-induced hypoalgesia. Our findings indicate that African Americans experience greater muscle pain during
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submaximal isometric handgrip exercise compared to non-Hispanic Whites, potentially suggesting that exercise does not successfully elicit centrally-mediated hypoalgesic mechanisms in African Americans to the same extent as in non-Hispanic Whites. Therefore, these observations support the conclusion that central pain modulation differs between these two races/ethnic groups. More research is needed to better understand these differences. There are several limitations in this study. First, our study sample primarily consisted of men (9/14 in each group); therefore, possible gender differences in muscle pain during exercise cannot be ascertained. However, there is an established literature documenting that women are generally more sensitive to experimental pain stimuli compared to men [35–37]; therefore, future research is needed to confirm whether the gender differences in pain sensitivity are evident in muscle pain during exercise. Also, our study sample was homogeneous in terms of regular physical activity levels, as all participants reported engaging in recreational exercise. There is some evidence suggesting that regular physical activity levels are inversely associated with pain sensitivity in healthy adults [38–41], and it is currently unclear whether regular physical activity levels play a role in determining muscle pain intensity during exercise. The small sample size in the present study might have been partially responsible for these study limitations; however, the sample size was adequately estimated to detect the group differences in our primary variable of interest (muscle pain) using power analysis. Therefore, the small sample size did not limit our primary findings from this study. 5. Conclusions In conclusion, the present study is the first to report that African Americans experienced a greater intensity of muscle pain during low intensity, short duration isometric handgrip exercise than non-Hispanic Whites. These findings are consistent with previous research showing the augmented pain sensitivity among African Americans in comparison to non-Hispanic Whites. In contrast, both African Americans and nonHispanic Whites had similar elevations in BP during exercise. Together, these results suggest racial/ethnic difference in central pain modulation associated with BP elevation between African Americans and nonHispanic Whites. Conflict of interest There is no conflict of interest among authors. Acknowledgments We thank Amritpaul Chatrath for his assistance with data collection, and Ramona Harwell for her administrative support for the present study. This study was supported by the Institutional Research Fund awarded to the PI (MU). References [1] Campbell CM, Edwards RR, Fillingim RB. Ethnic differences in responses to multiple experimental pain stimuli. Pain 2005;113:20–6. [2] Edwards RR, Doleys DM, Fillingim RB, Lowery D. Ethnic differences in pain tolerance: clinical implications in a chronic pain population. Psychosom Med 2001;63:316–23. [3] Edwards RR, Fillingim RB. Ethnic differences in thermal pain responses. Psychosom Med 1999;61:346–54. [4] Mechlin B, Heymen S, Edwards CL, Girdler SS. Ethnic differences in cardiovascularsomatosensory interactions and in the central processing of noxious stimuli. Psychophysiology 2011;48:762–73. [5] Forsythe LP, Thorn B, Day M, Shelby G. Race and sex differences in primary appraisals, catastrophizing, and experimental pain outcomes. J Pain 2011;12:563–72.
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Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Muscle pain and blood pressure responses during isometric handgrip exercise in healthy African American and non-Hispanic White adults Masataka Umeda ⁎, Jon P. Williams, Courtney A. Marino, Shelby C. Hilliard Department of Health, Exercise, and Sport Sciences, Texas Tech University, Lubbock, TX, USA
H I G H L I G H T S • African Americans experience more pain during exercise than non-Hispanic Whites. • Muscle pain increases more rapidly during exercise in African Americans. • Blood pressure responses during exercise are similar in the two groups.
a r t i c l e
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Article history: Received 8 April 2014 Accepted 29 September 2014 Available online 24 October 2014 Keywords: Pain sensitivity Exercise Blood pressure Race and ethnicity
a b s t r a c t It has been shown that African Americans (AAs) are more sensitive to experimental pain stimuli compared to non-Hispanic Whites (NHWs). A single bout of exercise results in naturally-occurring muscle pain and elevation in blood pressure (BP); however, it is currently unclear whether AAs and NHWs differ in muscle pain and BP responses during exercise. Therefore, we examined the differences in muscle pain and blood pressure (BP) during isometric handgrip exercise in African Americans (AAs) and non-Hispanic Whites (NHWs). Fourteen AAs and 14 NHWs completed isometric exercise consisting of squeezing a hand dynamometer at 25% of maximal strength for 3 min. During exercise, muscle pain ratings (MPRs) were assessed every 30 s, whereas systolic and diastolic BP (SBP and DBP) were recorded every minute. During exercise, AAs generally reported greater MPR than NHWs (p b 0.001), and MPR increased more rapidly during exercise in AAs than NHWs (p b 0.05). In contrast, SBP and DBP continued to increase similarly during exercise in both AAs and NHWs (p N 0.05). The results suggest that AAs generally experienced a greater intensity of muscle pain than NHWs during isometric handgrip exercise, but both groups exhibited similar elevations in BP during exercise. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Growing evidence from experimental studies indicates that African Americans are generally more sensitive to experimental pain stimuli than other races. For example, previous research indicates that African Americans exhibited lower tolerances to heat, cold, and ischemic pain stimuli [1–6], and rated heat pain stimuli higher [1,4,7] in comparison to non-Hispanic Whites. In addition, a physiological study demonstrates that the nociceptive flexion reflex, a spinal reflex induced by noxious stimulation that is modulated by spinal and supraspinal pain mechanisms (e.g., cerebral cortex, cerebellum, brainstem) [8,9], was elicited with lower intensity electrical stimulation in African Americans compared to non-Hispanic Whites [10]. Furthermore, Campbell et al. [11] examined a conditioned pain modulation consisting of assessing the ⁎ Corresponding author at: Department of Health, Exercise, and Sport Sciences, Texas Tech University, Box 43011, Lubbock, TX 79409, USA. Tel.: +1 806 834 3475; fax: +1 806 742 1688. E-mail address: [email protected] (M. Umeda).
http://dx.doi.org/10.1016/j.physbeh.2014.09.013 0031-9384/© 2014 Elsevier Inc. All rights reserved.
reductions in electrical pain ratings during concurrent application of ischemic pain, and reported that non-Hispanic Whites exhibited greater reductions in electrical pain ratings during concurrent application of ischemic pain compared to African Americans. Conditioned pain modulation has been found to be mediated by a specific region in the medulla, the subnucleus reticularis dorsalis; therefore, it has also been used to assess the function of central pain modulation [12,13]. Together, these observations collectively suggest that African Americans have higher sensitivity to experimental pain stimuli compared to non-Hispanic Whites, and that this is partly due to an impairment of pain modulatory systems within the central nervous system. Central pain modulation can also be assessed using other psychophysiological techniques. For example, numerous studies have been conducted examining the association between pain sensitivity and resting blood pressure (BP) in humans and animals, and results indicate an inverse association between pain sensitivity and resting BP [14–16]. Furthermore, previous research indicates that acute elevations in BP, caused by pharmacological or behavioral interventions (e.g., exercise), are also accompanied by reduced sensitivity to experimental pain
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stimuli [17]. Animal research demonstrates that several brain sites (e.g., rostral ventromedial medulla, nucleus tractus solirarius) are involved in the control of both BP and pain, and it has been suggested that elevated BP may initiate descending pain modulation via activation in these brain sites, resulting in decreased pain sensitivity [14,15]. Mechlin et al. examined the relationship between subjective responses to experimental pain stimuli and BP responses in African Americans and non-Hispanic Whites, and found that African Americans did not have an inverse association between pain sensitivity and BP, whereas the inverse association was confirmed in non-Hispanic Whites [4]. Therefore, the results suggest an impaired central pain modulation associated with BP elevations in African Americans. Exercise is a potent behavioral stimulus that acutely elevates BP [18, 19], and produces naturally-occurring pain in exercising muscles [20, 21]. A previous study demonstrates that even low intensity, short duration isometric handgrip exercise produces significant elevations in BP and a moderate intensity of muscle pain in the exercising forearm in healthy young adults [27]. These observations suggest that submaximal isometric handgrip exercise may be an optimal behavioral stimulus that can be used to examine the racial/ethnic differences in muscle pain and BP responses; however, no study has been conducted to compare muscle pain and BP responses during exercise in African Americans and non-Hispanic Whites. Therefore, the purpose of the present study was to examine whether African Americans and non-Hispanic Whites differ in muscle pain and BP responses during submaximal isometric exercise. 2. Materials and methods 2.1. Participants Healthy adults who identified themselves as African American or non-Hispanic Whites were recruited to participate in this study using an advertisement that was circulated via the campus-wide electronic mailing system and study flyers that were posted on designated places for public announcement on campus. The inclusion criteria for this study were 1) 18 to 30 years of age, 2) self-identification as African American or non-Hispanic White, 3) no medical conditions diagnosed by their physician, and 4) no medication use. Subjects were excluded from the study if 1) they indicated medical contraindications for exercise, 2) they were pregnant or breastfeeding at the time of screening, or 3) they were unable to understand instructions in English. The two groups were matched based on age (±3 years) and gender. The study protocol was fully approved by an institutional review board, and all participants signed a consent form before participating in the study. Power analysis was performed to estimate a sample size necessary to detect significant group differences in muscle pain during exercise in African Americans and non-Hispanic Whites. To perform the analysis, effect size (Cohen's d) was first calculated based on our pilot data, and the calculated effect size (d = 1.2), an α = 0.05, and a power = 0.80 were then used for the analysis [22]. The power analysis indicated that approximately 12 African Americans and 12 non-Hispanic Whites would be needed for the study. 2.2. Procedures The participants were asked to visit our laboratory once to complete a study session examining muscle pain and BP responses during isometric handgrip exercise. All study sessions were conducted by trained staff between 0900 and 1800 h, and the participants were asked to refrain from 1) strenuous exercise for 12 h, 2) alcohol consumption for 12 h, 3) caffeine intake for 3 h, and 4) smoking for 2 h before the study to accurately assess resting BP [23,24]. Upon arrival at the lab, the participants were first asked to sign a consent form, and then to complete questionnaires regarding demographics and general health, and regular physical activity (PA) levels using the Baecke Physical Activity Questionnaire (BPAQ) [25]. The
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BPAQ is a validated self-report questionnaire to quantify PA levels, and it consists of three subscales to estimate work-, sport-, and leisurerelated PA [25,26]. The work-related PA subscale assesses the type of occupation and the activity levels associated with their occupation. The sport-related PA subscale quantifies the amount of PA the participants are recreationally engaging in, whereas the leisure-related PA subscale quantifies the amount of PA except for recreational PA. Therefore, the leisure-related PA includes, for example, activities associated with the participants' daily commuting and TV-viewing. Each subscale quantifies the specific domain of PA, and total scores from the three subscales represent the participants' total PA levels. The investigator then prepared the participants for assessment of their resting BP by placing three electrodes on their chest and attaching a BP cuff around their non-dominant upper arm. Both electrodes and the BP cuff were connected to a small ECG device (Tango +, SunTech Medical, NC) that allowed the investigator to monitor BP periodically during the session. The participants were asked to remain seated in a comfortable chair for several minutes, and the investigator then assessed the participants' resting BP. Next, the investigator explained the exercise protocol to the participants, and then instructed them how to use the muscle pain rating (MPR) scale [20]. After the participants demonstrated understanding of the MPR scale with no further questions, they were informed that they would be rating muscle pain every 30 s during the exercise protocol. The participants were specifically instructed to rate the intensity of painful sensation in their forearm during exercise using the MPR scale. The MPR scale is constructed in a vertical alignment with 12 numbers (MPR 0, ½, 1–10), and has the corresponding verbiage next to nine numbers. The MPR scale ranges from no pain at all (MPR = 0) to extremely intense pain (MPR = 10), and also includes an unbearable pain option after the 10 rating if the participant experiences pain that exceeds the rating of extremely intense pain. The participants were then asked to squeeze a hand dynamometer (Model 78010, Lafayette Instrument, IN) with their dominant hand as hard as possible to assess their maximal voluntary contraction (MVC). The MVC assessment was conducted twice with sufficient rest between the trials, and the average of the two trials was used to compute 25% MVC for the subsequent exercise session. The participants were then asked to squeeze the hand dynamometer at 25% MVC and hold it at the target intensity as well as possible for 3 min. During this exercise, the investigator assessed MPR every 30 s, and BP every min. This exercise protocol was used because a previous study demonstrated that isometric handgrip exercise at 25% MVC for 3 min produces a moderate intensity of muscle pain in the forearm and significant elevations in BP in healthy adults [27]. The entire session took approximately 40 min to complete. 2.3. Data analyses The BPAQ was scored based on the published scoring method [25], and body mass index (BMI) was calculated using the following formula: BMI = weight (kg) / (height (m))2. Age, BMI, MVC, the BPAQ scores, and resting BP were compared between African Americans and nonHispanic Whites using an independent sample t-test to examine group differences in these variables. To test our primary hypotheses regarding whether African Americans would differ from non-Hispanic Whites in muscle pain and BP responses during isometric handgrip exercise, the MPR data were analyzed using a 2 (group: African American and non-Hispanic White) × 6 (time: every 30 s during 3 min of exercise) mixed model of repeated measures ANOVA, whereas the BP data were analyzed using a 2 (group: African American and non-Hispanic White) × 3 (time: every min during 3 min of exercise) mixed model of repeated measures ANOVA. Effect size was calculated using Cohen's d to assist in accurate interpretation of significant interaction effects where appropriate. Effect size was interpreted based on the following guideline: small effect = 0.2, medium effect = 0.5, and large effect = 0.80 [22].
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Correlational analyses were also performed to examine whether MPR was associated with BP using Pearson's correlation. For these analyses, MPR, SBP, and DBP during exercise were averaged over time, and resting SBP and DBP were included for the correlational analyses. The significance level was set at α = 0.05 for all statistical analyses. 3. Results 3.1. Participants Fourteen African American and 14 non-Hispanic White adults were recruited from the campus and completed this study. Each group consisted of nine men and five women, and all participants reported engaging in recreational exercise. Results from the analyses indicated that there were no significant differences between the two groups in age, BMI, MVC, resting BP, or BPAQ scores (t = − 1.36–1.61, p N 0.05). These characteristics are presented in Table 1.
10 Extremely Intense Pain 9 7 Very Strong Pain 6 5 Strong Pain 4 3 2 1 0
3.2. Muscle pain ratings during exercise Results from the MPR data analyses indicated a significant effect of time (F5, 22 = 28.46, p b 0.001), a significant effect of group (F1, 26 = 19.24, p b 0.001), and a significant time × group interaction (F5, 22 = 3.09, p b 0.05). Closer inspection of the data using effect size indicated that African Americans consistently reported a greater intensity of muscle pain than non-Hispanic Whites from the beginning of exercise, and this difference in the MPR scores became progressively larger as exercise progressed (d = 0.74–1.74). These data suggest that African Americans generally experienced greater MPR during exercise compared to non-Hispanic Whites, and that MPR increased more rapidly in African Americans compared to non-Hispanic Whites. These changes in the MPR scores during exercise are illustrated in Fig. 1, and effect sizes for each time point are summarized in Table 2.
African Americans Non-Hispanic Whites
8 MPR Scores
244
30
60
90 120 Time (sec)
150
180
Fig. 1. The MPR responses during isometric handgrip exercise. African Americans reported a greater intensity of MPR compared to non-Hispanic Whites (p b 0.001), and MPR increased during exercise more rapidly in African Americans compared to non-Hispanic Whites (p b 0.05). The data indicate group means ± SE at each time point.
3.4. The association of MPR with BP Results from the correlational analyses indicated that averaged MPR during exercise was not associated with BP measures in African Americans or in non-Hispanic Whites (p N 0.05). The results for the association between MPR and BP are summarized in Table 3.
4. Discussion 3.3. Blood pressure responses during exercise The SBP and DBP responses during exercise were similar for African Americans and non-Hispanic Whites. There was a significant effect of time (SBP: F2, 25 = 23.41, p b 0.001 & DBP: F2, 25 = 29.14, p b 0.001); however, neither a group effect (SBP: F 1, 26 = 0.01, p N 0.05 & DBP: F1, 26 = 0.16, p N 0.05) nor a time × group interaction (SBP: F2, 25 = 2.21, p N 0.05 & DBP: F2, 25 = 3.15, p N 0.05) was significant. These results suggest that SBP and DBP continued to increase during exercise at a similar rate in both African Americans and non-Hispanic Whites. The SBP and DBP responses during exercise are illustrated in Fig. 2a and b, respectively.
Table 1 Characteristics of study participants.
Age (years) BMI (kg/m2) Resting SBP (mmHg) Resting DBP (mmHg) MVC (kg) BPAQ-Total BPAQ-Work BPAQ-Sport BPAQ-Leisure
African Americans
Non-Hispanic White
22.14 (2.88) 26.02 (3.08) 116.36 (13.13) 65.36 (12.54) 44.86 (15.49) 9.07 (1.48) 2.54 (0.59) 3.57 (0.95) 2.96 (0.91)
21.86 (2.98) 24.06 (3.38) 121.5 (12.27) 70.71 (7.81) 38.54 (11.86) 8.81 (1.48) 2.58 (0.83) 3.39 (1.22) 2.84 (0.53)
Numbers are means, and numbers in parentheses are standard deviations. BMI; body mass index. SBP; Systolic Blood Pressure. DBP; Diastolic Blood Pressure. MVC; maximal voluntary contraction. BPAQ; Baecke Physical Activity Questionnaire.
The present study examined possible racial/ethnic differences in muscle pain and BP responses during isometric handgrip exercise in healthy African American and non-Hispanic White adults. Results for muscle pain indicated that African Americans generally experience a greater intensity of muscle pain during exercise compared to age- and gender-matched non-Hispanic Whites, and that muscle pain intensity increases more rapidly during exercise in African Americans in comparison to non-Hispanic Whites. With regard to BP, both SBP and DBP continued to increase during exercise in a similar rate in both groups. Together, these findings extend the literature in this area by suggesting that African Americans experience a greater intensity of naturallyoccurring muscle pain during exercise compared to non-Hispanic Whites, whereas both African Americans and non-Hispanic Whites have similar changes in BP during exercise.
Table 2 Effect size analyses for MPR during exercise in African Americans and non-Hispanic Whites.
MPR-30 MPR-60 MPR-90 MPR-120 MPR-150 MPR-180
African Americans
Non-Hispanic Whites
Effect size (d)
1.18 (0.99) 1.79 (0.98) 2.86 (1.03) 3.71 (1.20) 4.86 (1.35) 5.93 (1.59)
0.57 (0.62) 1.11 (0.66) 1.64 (0.91) 2.25 (1.05) 2.71 (1.20) 3.21 (1.53)
0.74 0.82 1.26 1.29 1.68 1.74
Numbers are means, and numbers in parentheses are standard deviations. MPR; Muscle pain ratings at each time point (sec) during 3 min of exercise. Guidelines for effect size interpretation; Small for d = 0.20, Medium for d = 0.50, Large for d = 0.80.
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(a)
245
(b)
150
90
African Americans
African Americans
145 85
SBP (mmHg)
140
DBP (mmHg)
Non-Hispanic Whites
135
130
Non-Hispanic Whites 80
75
125 70 120
115
1
2
65
3
Time (minutes)
1
2
3
Time (minutes)
Fig. 2. a. The SBP responses during isometric handgrip exercise. SBP increased comparably during exercise in African Americans and non-Hispanic Whites (p N 0.05). The data indicate group means ± SE at each time point. b. The DBP responses during isometric handgrip exercise. DBP increased comparably during exercise similarly in African Americans and non-Hispanic Whites (p N 0.05). The data indicate group means ± SE at each time point.
The augmented muscle pain during exercise in African Americans is consistent with previous research documenting that African Americans are more sensitive to a variety of experimental pain stimuli compared to non-Hispanic Whites, including heat, cold, ischemic, and electrical stimuli [1–7]. The underlying physiological mechanisms for the racial/ethnic differences are currently unclear; however, an impairment of central pain modulation has been suggested to explain the racial/ethnic differences in pain responses. For example, it has been demonstrated that African Americans have a lower threshold to elicit a nociceptive flexion reflex [10], and a smaller magnitude of reduction in pain ratings during concurrent application of noxious stimulation [11] compared to nonHispanic Whites. Furthermore, an inverse association between pain sensitivity and BP has been found in previous research, and it has been suggested that descending pain modulation might be initiated by elevated BP, resulting in decreased pain sensitivity through activation in brain sites that are involved in both BP and pain control [14,15]. However, an experimental study by Mechlin et al. indicate that the inverse association between pain sensitivity and BP is not found in African Americans [4], suggesting altered pain modulation associated with BP elevation in African Americans. In the present study, we found that submaximal isometric handgrip exercise elevated BP comparably in African Americans and non-Hispanic Whites, and that African Americans experienced a greater intensity of muscle pain during exercise compared to non-Hispanic Whites. Therefore, the present results further suggest that augmented muscle pain during exercise may be due to differential central pain modulation associated with BP elevation in African Americans and non-Hispanic Whites.
Table 3 Correlations between MPR and BP measures. African Americans
Non-Hispanic Whites
Resting Average Resting Average Resting Average Resting Average SBP SBP DBP DBP SBP SBP DBP DBP MPRs −0.37
−0.41
MPRs; muscle pain ratings. SBP; Systolic Blood Pressure. DBP; Diastolic Blood Pressure.
−0.28
−0.09
0.13
0.20
0.24
0.11
Our findings, however, are not consistent with results from the studies reporting an inverse association between pain sensitivity and BP in non-Hispanic Whites [4]. It is currently unclear why we failed to replicate the inverse association between pain and BP in non-Hispanic Whites in this study; however, one likely possibility is that different pain induction techniques were used. We used naturally-occurring muscle pain during exercise as the experimental pain stimulus, whereas Mechlin et al. used experimentally-evoked pain with ischemia, cold, and heat [4]. Although an inverse association between pain sensitivity and BP is supported by ample empirical evidence from numerous experimental studies [14–17], only limited data currently exist regarding a possible relationship between muscle pain during exercise and BP, and previous research in this area appears to provide mixed results. For example, it has been demonstrated that muscle pain during submaximal dynamic handgrip exercise is not associated with BP in healthy adults, whereas a strong inverse correlation between muscle pain during exercise and BP is found at peak exercise intensity [28]. In contrast, Ray and Carter reported no association between muscle pain during isometric fatiguing handgrip exercise and BP in healthy adults [29]. Furthermore, Cook et al. found that muscle pain during a maximal exercise test is not associated with BP in African American women [30]. Together, it appears that the relationship between muscle pain during exercise and BP is still unclear, suggesting a need for more research in this area. Alternatively, the similar BP responses during exercise and the absent correlations between muscle pain and BP in both groups could suggest that BP elevation may not explain the augmented muscle pain in African Americans. Although exercise was used to produce pain in this study, there is a growing literature documenting that exercise can also reduce sensitivity to a variety of experimental pain stimuli in healthy adults [31,32]. This hypoalgesic phenomenon has been termed as exercise-induced hypoalgesia, and previous research demonstrates that exercise-induced hypoalgesia can be successfully elicited with submaximal isometric handgrip exercise in healthy adults [23,27,33,34]. Furthermore, exercise-induced hypoalgesia occurs in body regions distant from the exercised muscles (e.g., contralateral and bilateral alterations in pain sensitivity) [31,32], suggesting the involvement of central pain mechanisms in exercise-induced hypoalgesia. Our findings indicate that African Americans experience greater muscle pain during
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submaximal isometric handgrip exercise compared to non-Hispanic Whites, potentially suggesting that exercise does not successfully elicit centrally-mediated hypoalgesic mechanisms in African Americans to the same extent as in non-Hispanic Whites. Therefore, these observations support the conclusion that central pain modulation differs between these two races/ethnic groups. More research is needed to better understand these differences. There are several limitations in this study. First, our study sample primarily consisted of men (9/14 in each group); therefore, possible gender differences in muscle pain during exercise cannot be ascertained. However, there is an established literature documenting that women are generally more sensitive to experimental pain stimuli compared to men [35–37]; therefore, future research is needed to confirm whether the gender differences in pain sensitivity are evident in muscle pain during exercise. Also, our study sample was homogeneous in terms of regular physical activity levels, as all participants reported engaging in recreational exercise. There is some evidence suggesting that regular physical activity levels are inversely associated with pain sensitivity in healthy adults [38–41], and it is currently unclear whether regular physical activity levels play a role in determining muscle pain intensity during exercise. The small sample size in the present study might have been partially responsible for these study limitations; however, the sample size was adequately estimated to detect the group differences in our primary variable of interest (muscle pain) using power analysis. Therefore, the small sample size did not limit our primary findings from this study. 5. Conclusions In conclusion, the present study is the first to report that African Americans experienced a greater intensity of muscle pain during low intensity, short duration isometric handgrip exercise than non-Hispanic Whites. These findings are consistent with previous research showing the augmented pain sensitivity among African Americans in comparison to non-Hispanic Whites. In contrast, both African Americans and nonHispanic Whites had similar elevations in BP during exercise. Together, these results suggest racial/ethnic difference in central pain modulation associated with BP elevation between African Americans and nonHispanic Whites. Conflict of interest There is no conflict of interest among authors. Acknowledgments We thank Amritpaul Chatrath for his assistance with data collection, and Ramona Harwell for her administrative support for the present study. This study was supported by the Institutional Research Fund awarded to the PI (MU). References [1] Campbell CM, Edwards RR, Fillingim RB. Ethnic differences in responses to multiple experimental pain stimuli. Pain 2005;113:20–6. [2] Edwards RR, Doleys DM, Fillingim RB, Lowery D. Ethnic differences in pain tolerance: clinical implications in a chronic pain population. Psychosom Med 2001;63:316–23. [3] Edwards RR, Fillingim RB. Ethnic differences in thermal pain responses. Psychosom Med 1999;61:346–54. [4] Mechlin B, Heymen S, Edwards CL, Girdler SS. Ethnic differences in cardiovascularsomatosensory interactions and in the central processing of noxious stimuli. Psychophysiology 2011;48:762–73. [5] Forsythe LP, Thorn B, Day M, Shelby G. Race and sex differences in primary appraisals, catastrophizing, and experimental pain outcomes. J Pain 2011;12:563–72.
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