Eur J Appl Physiol (2012) 112:3787–3795 DOI 10.1007/s00421-012-2361-5
ORIGINAL ARTICLE
The acute effects of aerobic exercise and modified rugby on inflammation and glucose homeostasis within Indigenous Australians Amy E. Mendham • Aaron J. Coutts Rob Duffield
•
Received: 30 November 2011 / Accepted: 17 February 2012 / Published online: 2 March 2012 Ó Springer-Verlag 2012
Abstract This study investigated the acute effects of two exercise modes, including cycle ergometry and modified rugby on inflammation and glucose regulation within an Indigenous Australian population. Ten sedentary, untrained Indigenous male participants volunteered to participate and were not clinically diagnosed with cardiovascular or metabolic disorders. Following baseline testing and in a randomized cross-over design participants completed two exercise protocols (cycle ergometry and modified rugby) of 40-min duration separated by 7 days’ recovery. Fasting venous blood was collected pre, post, 30, 60 and 240 min post exercise for analysis of glucose, insulin, cortisol and inflammatory markers of tumour necrosis factor (TNF)-a, interleukin (IL)-1b, IL-6, IL-1 receptor agonist (ra) and C-reactive protein (CRP). IL-6 and IL-1ra were significantly (P \ 0.05) increased within the 240 min post-exercise period, without significant differences between protocols (P [ 0.05). There were no significant changes within or between protocols for TNF-a, IL-1b and CRP (P [ 0.05). A comparison of insulin resistance: homeostasis model (HOMA) between resting and 240 min post exercise shows a change from a baseline value of 4.44 (3.71) to 1.76 (1.67) HOMA in cycle ergometry (P \ 0.05) and to 1.54 (1.33) HOMA in modified rugby (P \ 0.05), without differences between sessions (P [ 0.05). This study identified similar
acute inflammatory and glucose regulatory responses between cycle ergometry and modified rugby. Prescribing modified rugby as a mode of physical activity may provide Indigenous populations with a community-based approach to promote increased engagement in physical activity and assist in the acute regulation of glucose disposal and inflammatory cytokines. Keywords Aboriginal Australians Sedentary Cycling Interval Small-sided games Abbreviations CVD Cardiovascular disease CRP C-reactive protein GPS Global positioning satellite GXT Graded exercise test HR Heart rate HOMA Insulin resistance: homeostasis model IL Interleukin MHR Maximum heart rate VO2 Oxygen consumption Ra Receptor agonist TB-FM Total body fat mass TNF-a Tumor necrosis factor alpha T2DM Type 2 diabetes mellitus
Communicated by Michael Lindinger. A. E. Mendham (&) R. Duffield School of Human Movement Studies, Charles Sturt University, Panorama Avenue, Bathurst, NSW 2795, Australia e-mail:
[email protected] A. J. Coutts Sport and Exercise Discipline Group, UTS: Health, University of Technology Sydney (UTS), Sydney, NSW, Australia
Introduction In recent decades there has been a marked change in the lifestyle of many Indigenous groups around the world (Cleland and Sattar 2005). These lifestyle changes involve cultural isolation, psychological stress, physical inactivity and the incorporation of a westernized diet (Cleland and
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Sattar 2005; O’Dea 2005; Rowley et al. 1997). Such changes represent a serious health burden for Indigenous communities, evident through the increased incidence of obesity, type 2 diabetes mellitus (T2DM) and cardiovascular disease (CVD) (Cleland and Sattar 2005; O’Dea 2005; Zimmet et al. 2003). Additionally, the emerging morbidity and mortality rates associated with T2DM and CVD have significant implications for the development of health promotion strategies that specifically target disease prevention. As such, information derived from studies targeting physical activity strategies for specific ethnic groups may provide improved preventative interventions that are culturally appropriate, relevant and evidence-based (Cleland and Sattar 2005; Rowley et al. 1997, 2003; Wang and Hoy 2007). Recent studies examining the health status of Indigenous Australians highlights obesity, infection and/or smoking as the main causes of elevated inflammatory biomarkers and resultant chronic disease development (Rowley et al. 2003; Wang and Hoy 2007). Specifically, C-reactive protein (CRP) is predominately up-regulated in the hepatocytes under the control of interleukin (IL)-6, IL-1b and tumour necrosis factor-a (TNF-a) (Fischer 2006; Pedersen and Febbraio 2008). The prolonged presence of such inflammatory markers creates a heightened state of chronic inflammation that is regarded as a predictor and instigator of increased risk of future development of T2DM and CVD (Petersen and Pedersen 2005). Conversely, acute exercise-induced IL-6 release from skeletal muscle results in the subsequent secretion of IL-1 receptor agonist (ra) and cortisol; stimulating an antiinflammatory response (Fischer 2006). As a counter to disease development, research emphasizes primary prevention of T2DM and CVD through exercise-based health programs, particularly aimed at improving physical activity levels and reducing the inflammatory state (Brukner and Brown 2005; McDermott et al. 2000; Rowley et al. 2000a). Indeed, regular exercise training has been shown to decrease pro-inflammatory cytokines and delay the deterioration of glucose tolerance and insulin sensitivity (Eriksson and Lindga¨rde. 1991; Okita et al. 2004; Zimmet et al. 2003). However, despite literature supporting lifestyle and exercise interventions across different ethnic cohorts, there is no information relating to acute exercise-based research within Indigenous Australians (Pan et al. 1997; Unwin et al. 2002; Zimmet et al. 2003; Rowley et al. 2000b). As such, prior to providing specific exercise training recommendations (modality, intensity and duration), further research is required to report the acute exercise-induced inflammatory and glucose homeostasis responses within this Indigenous population. Engagement in physical activity as a preventative measure of chronic disease development contains specific ethnic
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bias relating to assumptions on equipment availability, facilities and social importance (Thompson and Gifford 2000; Zimmet et al. 2003). As such, traditional gym-based exercise modes (Mendham et al. 2011; Okita et al. 2004) as a sustainable intervention to reduce disease risk may not be optimal in Indigenous communities. Given cultural and social issues involved in developing an ethnicity-specific health intervention (Zimmet et al. 2003); the modification of physical activity will be more likely to succeed if reinforced through group participation as opposed to individualized exercise and lifestyle-based programmes (Thompson and Gifford 2000). Team sports such as rugby league are popular within Indigenous Australian communities and may reinforce group participation and cohesion (Andersen et al. 2010). Thus, modified team sport, such as rugby small-sided games may be an achievable option to reverse low physical activity levels within Indigenous populations (Thompson and Gifford 2000). Accordingly, the current study aimed to assess the acute effects of traditional gym-based (cycle ergometry) and modified rugby as small-sided games on the biochemistry relating to inflammation and glucose homeostasis within an Indigenous Australian population. It was hypothesized that when matched for intensity modified rugby would not differ in the post-exercise inflammatory response to cycle ergometry. Further, the acute inflammatory response in both modes would be indicative of an acute increase in anti-inflammatory markers IL-6 and IL-1ra following exercise.
Methods Participant recruitment Participants volunteered from a regional Indigenous Australian community, through the support of local Indigenous members. Participants comprised of ten sedentary Indigenous males, who were non-smokers and not clinically diagnosed with CVD or metabolic disorders. The study was approved by the Research in Human Ethics Committee of Charles Sturt University. Prior to testing procedures, all participants were familiarized with all testing procedures, provided verbal and written consent and completed a preexercise health questionnaire. Overview Testing procedures were conducted at standardized times from 0730 to 1300 h, following an overnight fast (10–12 h). On two separate occasions, participants completed two respective exercise protocols (cycle ergometry or modified rugby) in a randomized cross-over design, each separated by 7 days’ recovery. Participant’s physical
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activity and diet were standardized and recorded 24 h prior to testing and then replicated throughout the remaining testing procedures. During each protocol and 240 min after all testing sessions, participants remained fasted and consumed water ab libitum (*500 mL). Baseline testing On arrival at baseline testing, measures of height (stadiometer: Custom CSU, Bathurst, Australia), body mass on calibrated scales (HW 150 K; A&D, Bradford, MA, USA) and waist (measured just above the iliac crest) and hip girths (greatest posterior protuberance of the buttocks) (steel tape, EC P3 metric graduation, Sydney, Australia) were obtained (Hill et al. 2007). Manual blood pressure was obtained with an aneroid sphygmomanometer and cuff (Welch-Allyn, Arden, CA, USA) expressed as the mean of three measurements after being seated for 5 min. A supine whole body dual-energy X-ray absorptiometry (DXA) scan (XR800, Norland, Cooper Surgical Company, Trumbull, CT, USA) was conducted with scanning resolution set at 6.5 9 13.0 mm, and scanning speed was set at 130 mm s-1. Whole body scans were analysed (Illuminatus DXA, ver. 4.2.0, Trumbull, CT, USA) for total body fat mass (TB-FM) (Kim et al. 2002; Mendham et al. 2011). Aerobic fitness measures were obtained via a graded exercise test (GXT) to determine sub-maximal oxygen consumption (VO2). Pulmonary gas exchange was measured by determining O2 and CO2 concentrations and ventilation to calculate VO2 consumption using a metabolic gas analysis system (ParvoMedics, True2400, East Sandy, UT, USA). Prior to each session, the flow meter was calibrated using a 3-l syringe, while gas analysers were calibrated for fractional gas concentration with a gravimetric gas mixture of known concentrations [CO2, 4.1(0.1)%; O2, 15.7(0.2)%], in accordance with the manufacturer’s instructions. The GXT was performed on an electronically braked cycle ergometer (LODE Excalibur Sport, LODE BV, Groningen, The Netherlands), which started at 25 W and increased by 25 W every min. Heart rate (HR) (Vantage NV, Polar, Kempele, Finland) was recorded each min throughout the protocol, and subjects exercised until attainment of 80% age-predicted maximum heart rate (MHR). VO2 was measured continuously throughout the exercise protocol and reported as a VO2 at 80% predicted MHR. Exercise protocols Modified rugby The protocol consisted of interval sessions, with participants completing 40 min of six-a-side on a small pitch
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(width: 40 m; length: 60 m). The modified rugby session was played under touch football rules. The game required each team six ‘plays’ whilst in possession of the ball, each play requiring players to pass the ball backwards to an ‘on side’ team member. Defending players were required to touch their opponent with one hand. Following a successful touch, game play would restart with a ‘play the ball’, at this time requiring the line of defending players to be 5 m away from the position of each ‘play the ball’ (Kennett et al. 2011). The session comprised of 4 9 10 min bouts, interspersed by 2 min passive recoveries. A Global Positioning Satellite (GPS) device (SPIetite, GPSports, Canberra, Australia) was worn in a customised harness between the scapulae to quantify distance and mean speed (m min-1) of movement patterns during the session (Coutts and Duffield 2010). At the end of each 10-min period, HR and rating of perceived exertion (RPE; 6–20 scale) were recorded. Additionally, 30 min post-exercise exercise perception was recorded using the RPE scale (Hill-Haas et al. 2011) and rating the question as to how challenging did the participant find the exercise session on a scale of 1–10 (1 = Not at all, 10 = Very much). Using the intrinsic motivation inventory scale participants completed a question from the interest/enjoyment subscale the exercises are fun to do, ranging on a scale of 1–7 (1 = not at all true, 4 = somewhat true, 7 = very true) (McAuley 1989). Cycle ergometry The cycle ergometry session was conducted on Monark stationary cycle ergometers (Monark 828E, Monark Exercise AB, Varburg, Sweden) and comprised of 4 9 10 min bouts, at a target intensity of 80–85% MHR, interspersed by 2 min passive recoveries. During the session, cadence was maintained at 60–65 rpm and individual resistance adjusted to maintain target HR zones. At the end of each 10-min interval HR and RPE were recorded, with session RPE and the completion of exercise perception questions 30 min following exercise. Venous blood sampling and analysis Blood was collected during baseline testing for analysis of fasting total cholesterol (Enzymatic Method and Polychromatic Endpoint Technique), high-density lipoprotein (Accelerator Selective Detergent Methodology), low-density lipoprotein (Friedwald Equation), triglycerides (Enzymatic Method and Biochromatic Endpoint Technique) (Dimension Xpand Plus, Siemens Healthcare Diagnostics, Sydney, Australia), total leucocyte count (Cell Counter: Cell-Dyn 3200, Abbott Laboratories, Abbott Park, IL, USA) and glycosylated haemoglobin (HbA1c) (High-Performance Liquid Chromatography: Bio-Rad
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Variant, Bio-Rad Laboratories, Sydney, Australia). During the respective protocols, 20 mL was collected at each time point for analysis of glucose, lactate (ABL825 Flex Analyzer, Radiometer Medical ApS, Bronshoj, Denmark), insulin, cortisol (Solid-phase Chemiluminescent Enzyme Immunometric Assay: Immulite 2000, Siemens Healthcare Diagnostics, Los Angeles, CA, USA) and CRP (Particle Enhanced Turbidimetric Immunoassay: Dimension Xpand Plus, Siemens Healthcare Diagnostics, Sydney, Australia). Analysis of biochemistry variables glucose, lactate, insulin, cortisol and CRP showed intra and inter-assay coefficients of variation between 4.0 and 7.4%. IL-6, IL-1b, IL-1ra and TNF-a were measured at each time point using a monoclonal antibody, specific to the cytokine pre-coated onto the microplate (Sandwich Enzyme Immunoassay—ELISA: Quantikine, R & D Systems, Minneapolis, MN, USA), with intra and inter-assay coefficients of variation between 4.3 and 5.6% insulin resistance: homeostasis model assessment (HOMA) was calculated using the formula (fasting insulin 9 fasting glucose)/22.5 (Matthews et al. 1985; Wallace et al. 2004). Serum or plasma was collected following centrifugation at 3,500 rpm for 15 min at 4°C. Aliquots were frozen at -80 and -20°C for ethylene diamine tetraacetic acid (EDTA) and serum separator tubes (SST), respectively. For analysis of glucose, leucocytes and HbA1c, whole blood was refrigerated (4°C) until further analysis.
Statistical analysis All data are reported as mean (standard deviation). Within and between protocol and blood measure time-point differences were assessed using a two-way repeated measures ANOVA (condition 9 time). When significant differences were observed, Tukey’s pairwise comparisons were employed to assess the source of significance that was set at P B 0.05. All statistical analyses were performed using PASWTM for MS-Windows v17.0 (Statistical Package for the Social Sciences, Chicago, IL, USA).
Results All resting and descriptive measures of anthropometry, DXA (TB-FM %), blood pressure, sub-maximal VO2 (at 80% MHR) and resting venous blood values are presented in Table 1. Participants showed high levels of adiposity, CRP concentrations and insulin resistance, as evident through elevated fasting insulin concentrations and HOMA. Modified rugby and cycle ergometry demands Total distance covered during the modified rugby was 2,696 (398) m, at 67 (10) m min-1, involving 140 (78) m of high-speed running above 14 km h-1. The mean HR
Table 1 Baseline characteristics within the subject cohort (n = 10)
Resting values Age (years)
38.5 (10.23)
Sub-Maximal oxygen consumption (mL kg-1 min-1)
30.8 (5.30)
Body mass index (kg m2)
31.98 (6.41)
Desirable range – – \25
Systole blood pressure (mmHg)
131 (8.76)
\130
Diastole blood pressure (mmHg)
84 (7.47)
\85
103.62 (18.76)
\102
Waist to hip ratio
0.95 (0.08)
\0.90
Total body—fat mass (%)
27.8 (11.41)
\25
Waist circumference (cm)
-1
Total cholesterol (mmol L )
5.10 (0.88)
\5.5
High density lipoprotein (mmol L-1)
1.13 (0.29)
[1.0
Triglycerides (mmol L-1) Cholesterol hazard ratio
1.55 (0.72) 4.78 (1.52)
\2.0 \4.5
HbA1c (%A1c)
5.69 (0.61)
\7 \5.5
-1
Glucose (mmol L )
5.38 (0.66)
Insulin (ll U mL-1)
17.7 (12.40)
5–15
Insulin resistance (HOMA)
4.44 (3.71)
\4
Total leucocyte count (10-9 L-1)
6.85 (2.11)
4–10
Data provided as mean (SD)
CRP (mg L-1)
3.05 (2.06)
