At rest and during exercise, free fatty acids (FFAs) are liberated from adipocytes (i.e., lipolysis). These FFAs may then be transported to muscle tissue for oxidation, a process potentially limited by adipose tissue blood flow (Frayn & Karpe, 2014). Subcutaneous abdominal adipose tissue (SCAAT) is the predominate supplier of FFAs to the circulation during exercise (Horowitz, 2003). Thus, the lipolytic rate of SCAAT may influence whole-body fat oxidation and metabolic rate. Previous research reported increased SCAAT lipolysis and blood flow during endurance exercise (Baur et al., 2018). While the metabolic responses to exercise have been well studied, less is known about how environmental conditions alter these metabolic responses.
Military personnel and athletes are often exposed to challenging environments during training, athletic competition, and military operations (Pasiakos, 2020). These environmental conditions pose safety risks to the athlete or warfighter, alter physiological response and nutritional requirements, and can impair exercise performance (Pasiakos, 2020; Périard et al., 2021). Increased thermal strain of the environment (i.e., greater ambient temperature and humidity) is known to reduce exercise performance (Périard et al., 2021) and to result in greater muscle glycogenolysis, increased carbohydrate (CHO) oxidation, and increased blood lactate (Fink et al., 1975; Hargreaves et al., 1996).
In contrast, cold ambient temperatures may induce greater reliance on fat as a fuel source during exercise (Gagnon et al., 2013, 2020). However, the contribution of various fat depots during exercise in the cold has not been elucidated. Cold exposure may induce vasoconstriction to peripheral adipose tissue, reduce blood flow, and potentially impair lipid mobilization (Doubt, 1991; Layden et al., 2002). Though SCAAT represents a major adipose depot, no studies have examined the effect of cold ambient temperature on SCAAT lipolysis or SCAAT blood flow during endurance exercise. As cold ambient temperatures are common among athletes and warfighters, determining the metabolic response and the contributions of specific metabolic sites (e.g., SCAAT) to cold ambient temperatures during exercise may impact safety, nutritional and training recommendations, and performance optimization. Trained individuals have altered substrate metabolism compared to untrained individuals, making it essential to examine these responses in athletes (Phillips et al., 1996). Therefore, this study investigated the effect of cold ambient temperature during cycling exercise on SCAAT lipolysis and SCAAT blood flow in endurance-trained cyclists. We hypothesized that SCAAT lipolysis would increase and SCAAT blood flow would decrease in COLD compared to neutral (NEU) ambient temperatures.
Materials and Methods
Participants
Ten healthy, endurance-trained male cyclists participated in this study. Subjects were required to meet the following inclusion criteria: (a) ages 18–45 years, (b) cycling peak oxygen consumption (
Study Design
This was a randomized, crossover study consisting of five visits to the laboratory (separated by four to nine days). Lactate threshold (LT) and
Baseline Testing
Height and weight were assessed via wall-mounted stadiometer and digital scale, respectively (Seca Corporation). Body composition was assessed using dual-energy X-ray absorptiometry (Hologic Discovery W) by a certified technician according to manufacturer’s specifications. Participants were then fitted to an electronically braked cycle ergometer (Velotron). Participants wore their personal cycling shoes and kit during testing. A chest strap heart rate (HR) monitor (Polar Electro Inc.) was fitted prior to performing a 5-min self-selected warm-up for a graded exercise test. Expired gases were continuously measured using a face mask (Cosmed V2 mask, COSMED) and TrueOne 2400 metabolic cart (ParvoMedics). Following the warm-up, participants cycled at a workload which was “comfortable, but not an easy pace for a 1-hr ride.” Workload increased 20 W every 3 min until LT was achieved. Fingerstick blood samples were taken and analyzed immediately after each stage to determine power output at LT (blood lactate ≥4.0 mmol/L). Once LT was achieved, workload increased 30 W and stages were shortened to 2 min to determine
Experimental Trials
To assess core temperature (CT), each participant consumed a CorTemp radio-frequency telemetered thermometer pill (HQ, Inc.) 8–10 hr prior to arriving at the laboratory. Upon arrival, each participant immediately lay supine for insertion of the microdialysis probe using techniques previously described (Hickner, 2000). After probe insertion, 60 min was allowed for equilibration while the participant lay supine. During the final 10 min of the equilibration period, venous blood, urine-specific gravity (Atago PAL-10S; Atago USA, Inc.), and nude body weight measurements were taken. A resting microdialysis sample was taken for 5 min while seated following equilibration. Energy expenditure (5-min collection) via breath analysis was also measured using indirect calorimetry, and a resting fingerstick blood sample was obtained. Total CHO and fat oxidation were calculated via stoichiochemical equations described elsewhere (Jeukendrup & Wallis, 2005).
Participants then entered the environmental chamber and began the cycling protocol. No food, water, outside encouragement, or music was permitted. Cycling began at a wattage that elicited 70% LT for 25 min. The cycling intensity increased to a wattage that elicited 90% LT for an additional 25 min.
HR, CT, and dialysate measurements were taken at rest and every 5 min during the exercise protocol. Dialysate samples were stored on ice until completion of the testing bout, then at 4 °C, and analyzed for ethanol within 24 hr as described below. Subsequently, dialysate samples were stored at −80 °C for later analysis of interstitial glycerol concentration. Metabolic measurements via gas exchange were measured for 5 min at rest and for 1.5 min during exercise (rest: −5 to 0 min; 70% LT: 3.5 to 5 min, 23.5–25 min; 90% LT: 28.5–30 min, and 48.5–50 min). Fingerstick blood samples were also taken (rest: 0 min; 70% LT: 5 min, 25 min; 90% LT: 30 min, 50 min) to analyze blood glucose and lactate concentrations, then stored on ice until the end of data collection and analyzed via a glucose and lactate analyzer (YSI 2300 Stat, Yellow Springs Instruments).
Dialysate Analysis
The ethanol technique (Hickner et al., 1992; Pierce et al., 2015) was used to estimate blood flow in the area surrounding the probes. As ethanol is not metabolized to any significant degree in adipose tissue, its local removal is related to blood flow surrounding the probe (Hickner et al., 1992). A multimode microplate reader (SpectraMax M5, Molecular Devices) was used to measure ethanol concentrations within 24 hr of dialysate collection. Dialysate sample (2 μl) was added to a mixture containing an ethanol buffer (pH 8.9; 74 mM sodium pyrophosphate, 60 mM hydrazine sulfate, and 22 mM glycine) and a nicotinamide adenine dinucleotide solution (NADH, 100 mM) in black 96-well microplates (ThermoScientific Immuno Plates). Alcohol dehydrogenase (10 μl) was added to each well and incubated for 1 hr at room temperature in the dark. Samples were read with fluorescence at an excitation and emission of 360 and 415 nm, respectively. The fluorescent NADH product is directly proportional to ethanol in the sample (Hickner et al., 1992; Pierce et al., 2015). The intraassay CV for ethanol was 7.1%.
Statistical Analysis
Data were analyzed using SPSS (version 27) Statistics software package (IBM) with significance set at p < .05. Mixed repeated-measures analysis of variance (ANOVA) was used to identify differences between conditions for: CT, HR, SCAAT glycerol, blood glucose and lactate, CHO and fat oxidation rates,
Results
Descriptive Characteristics
Ten volunteers were recruited from the local community. Table 1 summarizes the participant characteristics at baseline.
Baseline Descriptive Variables
| n | Baseline | |
|---|---|---|
| Age (years) | 10 | 23 ± 3 |
| Height (cm) | 10 | 178.6 ± 5.9 |
| Body mass (kg) | 10 | 74.0 ± 11.4 |
| Body fat (%) | 10 | 18.4 ± 3.5 |
| 10 | 60.60 ± 4.84 | |
| Power output at LT (W) | 10 | 234 ± 35 |
| Urine-specific gravity (g/ml) | 9 | 1.015 ± 0.008 |
Note. Data are expressed as mean ± SD. LT = lactate threshold;
Environmental Conditions
Chamber temperatures (COLD: 3.1 ± 1.8 °C, NEU: 19.4 ± 1.0 °C; p < .001) but not humidity (COLD: 41.6% ± 5.6%, NEU: 39.0% ± 2.2%; p = .202) were significantly different between conditions.
Central Response
HR and CT (Figure 1) were not different at baseline (p = .964 and p = .324, respectively). HR (p < .001) and CT (p < .001) increased over time. No Condition × Time (F3.646, 61.977 = 2.011, p = .110,
—Central response during cycling exercise. Core temperature (top; n = 10) and heart rate (bottom; COLD: n = 10, NEU: n = 9) are presented as mean ± SD. There were no differences between temperature conditions. *Significantly greater compared with rest (p < .01). #Significantly greater from 70% LT (p < .01). NEU = neutral; LT = lactate threshold.
Citation: International Journal of Sport Nutrition and Exercise Metabolism 34, 3; 10.1123/ijsnem.2023-0150
Metabolic Response: All Data
There were no differences at baseline for any measure. When all time points were analyzed (0–50 min), interstitial glycerol significantly increased over time (p < .001) but no Condition × Time (F1.316, 18.428 = 0.354, p = .618,
—Interstitial glycerol concentration during cycling exercise (due to missed samples, n = 8; mean ± SD). There were no significant differences between temperature conditions. *Significantly greater compared with rest (p < .01). NEU = neutral; LT = lactate threshold.
Citation: International Journal of Sport Nutrition and Exercise Metabolism 34, 3; 10.1123/ijsnem.2023-0150
—Whole-body substrate utilization during cycling exercise for fat oxidation (top) and CHO oxidation (bottom; due to missed samples, COLD: n = 6; NEU: n = 7; mean ± SD). *Significantly greater compared with rest (p < .001). #Significantly greater from 70% LT (p < .01). †CHO oxidation was significantly greater in COLD at 70% LT (p < .05). NEU = neutral; LT = lactate threshold; CHO = carbohydrate.
Citation: International Journal of Sport Nutrition and Exercise Metabolism 34, 3; 10.1123/ijsnem.2023-0150
—Blood glucose (top) and blood lactate (bottom) response during cycling exercise (n = 9; mean ± SD). There were no differences between temperature conditions. *Significantly greater compared with rest (p < .05). #Significantly greater from 70% LT (p < .05). LT = lactate threshold; NEU = neutral.
Citation: International Journal of Sport Nutrition and Exercise Metabolism 34, 3; 10.1123/ijsnem.2023-0150
—
Citation: International Journal of Sport Nutrition and Exercise Metabolism 34, 3; 10.1123/ijsnem.2023-0150
Metabolic Response: 70% LT
When analyzing only the 70% LT portion of the exercise bout (0–25 min), interstitial glycerol increased over time (p < .001) but no Condition × Time (F1.780, 30.255 = 1.533, p = .233,
Metabolic Response: 90% LT
When analyzing only the 90% LT portion of the exercise bout (25–50 min), interstitial glycerol continued to increase (p < .001) with no Condition × Time (F1.311, 18.357 = 0.477, p = .549,
Blood Flow
SCAAT blood flow did not change over time (p = .320) and was not different between conditions at rest (p = .144) or during exercise (p = .308). No main effects were observed (p = .816). Therefore, no blood flow adjustments were necessary.
Discussion
Exercise increases lipid mobilization from SCAAT (Baur et al., 2018; Ormsbee et al., 2007, 2009); however, there are no data demonstrating the effect of cold exposure during exercise on glycerol mobilization from SCAAT using microdialysis. Using microdialysis, we were able to determine dialysate glycerol concentration in SCAAT before and during exercise. The novel finding from the present study is that COLD did not influence SCAAT lipolysis, SCAAT blood flow, or fat oxidation during steady-state exercise below the LT (70% and 90% LT) compared to NEU.
As no studies have examined the effects of cold ambient temperature on SCAAT lipolysis with microdialysis, it is not possible to make direct comparisons. However, since previous research has shown that circulating plasma glycerol and local SCAAT glycerol concentrations respond to stimuli in a similar manner (Hickner et al., 1999), and as we observed no alteration in SCAAT blood flow which suggests fuel mobilization impairment was unlikely, inferences can be made based on currently available literature. Aerobic exercise increases SCAAT lipolysis (Baur et al., 2018), and the present study validates those findings. Previous work investigating cold air exposure, alone, on lipolysis has reported increased plasma glycerol concentrations in 5 °C compared to 29 °C (Vallerand et al., 1999). Yet, when aerobic exercise is combined with cold exposure, it does not appear that plasma glycerol concentrations are altered (Gagnon et al., 2013; Galloway & Maughan, 1997). No differences in plasma glycerol during walking or running exercise in 0 or 22 °C were observed despite increased fat oxidation in the cold (Gagnon et al., 2013). To explain the increased fat oxidation despite no change in blood parameters, these authors speculated an increased reliance on intramuscular triglyceride (IMTG) stores in cold conditions, though this was not measured. While SCAAT represents the largest contribution of fatty acids during exercise (Horowitz, 2003), IMTGs are also utilized to a significant degree, contributing between 10% and 50% of total fat oxidation during moderate-intensity exercise (Horowitz, 2003; van Loon et al., 2003) with endurance-trained individuals having an increased capacity to utilize IMTGs compared to sedentary (Phillips et al., 1996). Given the highly trained status of our participants, it is possible that no differences were observed between conditions due to partitioning of other adipose tissue depots (e.g., IMTGs). Therefore, multiple sites of lipolytic activity during exercise in cold ambient temperatures should be investigated to quantify the contribution of each depot. However, as we observed no differences in fat oxidation between COLD and NEU, it seems unlikely that IMTG utilization altered our findings.
No differences in blood glycerol concentrations or total fat oxidation rates were observed between 4°C and 21 °C during time to exhaustion cycling at 70%
It has been suggested that results not showing an augmented, cold-induced lipolytic response are due, at least partially, to peripheral perfusion limitations to adipose during exercise, as cold exposure has been speculated to decrease adipose blood flow via potentiation of adrenergic vasoconstriction (Hjemdahl & Sollevi, 1978). Thus, diminished peripheral blood flow may limit the liberation of FFA and glycerol from adipose into the blood (Doubt, 1991; Hjemdahl & Sollevi, 1978; Layden et al., 2002), although this has not been verified. Therefore, we measured the microcirculatory blood flow in SCAAT to ensure that any alterations in interstitial markers were a direct result of environmental temperature and not temperature-induced alterations in blood flow. In contrast, we observed no reduction of SCAAT blood flow in COLD. Our data demonstrated that neither cycling exercise nor the environmental conditions alter in situ SCAAT blood flow. To our knowledge, this is the first study to address the environmental influence on SCAAT blood flow during endurance exercise. Others reported increased SCAAT lipolysis and no change in SCAAT blood flow with moderate-intensity cycling, alone (de Glisezinski et al., 1998). In contrast, treadmill running increased SCAAT blood flow (Baur et al., 2018). The disparity in exercise modality likely explains incongruent findings.
We observed increased CHO oxidation in COLD compared to NEU at 70% LT. In agreement, increased CHO oxidation was reported during cycling at 0 °C and −10 °C compared to 10 °C and 20 °C (Layden et al., 2002). These authors speculated increased CHO utilization could be due to reduced lipolysis, mobilization of FFA, uptake of FFA into muscle, or oxidative capacity of the muscle. As we observed no differences in SCAAT lipolysis, this explanation appears unlikely. While we did not observe alterations in SCAAT blood flow, we cannot rule out impairments to FFA mobilization as blood glycerol was not measured. Similarly, FFA uptake into the muscle was not directly measured and, therefore, cannot be ruled out. Others reported increased CHO oxidation in 4 °C compared to 11 °C and 21 °C (Galloway & Maughan, 1997). These authors suggested reduced mechanical efficiency during cold exposure may explain their findings. We observed increased CHO utilization at lower exercise intensities but not higher exercise intensities where greater metabolic heat production would occur. Therefore, it is possible that we observed increased CHO reliance at 70% LT in COLD due to reduced mechanical efficiency.
We observed no differences in CT between conditions, suggesting the cold stimuli may have been insufficient to induce physiological alterations. Lind (1963) described the “prescriptive zone,” whereby CT is influenced by metabolic rate during treadmill walking rather than ambient temperature within a certain range of environmental conditions (Lind, 1963). This work investigated temperatures as low as 10 °C; however, it is possible that the ambient temperature utilized in the present study falls within this prescriptive zone. Previous reports have shown reduced CT during cycling exercise at 4 °C (Galloway & Maughan, 1997), while we, and others, did not observe differences in CT during cycling (Layden et al., 2002) or running (Gagnon et al., 2013). This would suggest that the present study likely does fall within the prescriptive zone. Nonetheless, previous reports have shown alterations in glycerol concentrations with no change in CT (Layden et al., 2002) and no alterations in glycerol concentration despite CT differences (Galloway & Maughan, 1997). Thus, the impact of internal temperature on lipolysis remains unclear. Others have suggested fat metabolism is altered only when temperatures are ≤0 °C (Layden et al., 2002, 2004). Our findings seemingly support this as the COLD condition in the current study was 3.1 ± 1.8 °C, and we observed no differences in fat metabolism. Therefore, the cold stimulus in the present study was perhaps insufficient to induce fat-related metabolic alterations. Future work should investigate the effect of temperatures at or below that threshold on SCAAT lipolysis during endurance exercise.
Neither skin nor muscle temperature was measured in the present study, limiting our ability to quantify the magnitude of cold exposure experienced by our participants. However, as cold ambient air has been suggested to result in little or no change in muscle temperature (Castellani et al., 2021), this is unlikely to have influenced our results. Further, studies utilizing similar environmental conditions have consistently shown reduced skin temperature with mixed results on metabolic alterations (Gagnon et al., 2013; Galloway & Maughan, 1997; Layden et al., 2002; Sink et al., 1989), suggesting that, though not directly measured, skin temperature would have been reduced. Though ice storage preserves samples compared with no ice (Higgins et al., 2023), it is possible that our results, particularly lactate, were altered compared with immediate analysis. LT was determined in thermoneutral conditions. Due to the fixed-rate protocol (70% and 90% LT), it is possible that temperature-mediated alterations in work rate ensued. As females were not included in this study, results may not translate to females. Finally, our observed power for metabolic variables was low. While our initial sample size was in line with other studies investigating cold-induced metabolic alterations during exercise (Gagnon et al., 2013, 2020; Sink et al., 1989), the present study is likely underpowered to detect smaller differences which may exist. With a larger sample size, differences could have emerged between temperature conditions. Despite these limitations, we believe the present study has practical implications as athletes and military personnel are likely to experience similar environmental conditions during training, competition, or military operations. These findings suggest that training, nutrition, and supplementation strategies need not be altered to accommodate cold, but above freezing, ambient temperatures.
In conclusion, by using microdialysis, we observed an increase in SCAAT lipolysis during cycling exercise. However, cold ambient temperature did not influence in situ SCAAT lipolysis or SCAAT blood flow, nor did it alter whole-body fat metabolism below the LT.
Acknowledgments
We are grateful to the National Strength and Conditioning Association for helping fund this study through the National Strength and Conditioning Association Doctoral Student Research Grant. We also thank Joey Hibbard for assisting with data collection and procedure preparation. Michael J. Ormsbee serves on the scientific advisory board for the Korey Stringer Institute. The other authors declare no conflicts of interest. The authors declare that the results of this study are presented clearly, honestly, and without fabrication, falsification, or inappropriate manipulation. Author Contributions: Bach and Saracino contributed equally to this work. Funding: Christopher W. Bach and Michael J. Ormsbee. Study conception and design: Christopher W. Bach, Michael J. Ormsbee, and Brent C. Ruby. Data collection: Christopher W. Bach, Daniel A. Baur, and Brandon D. Willingham. Data analysis and preparation of the first draft of the manuscript: Patrick G. Saracino. Critical revision and editing of all drafts, and the reading and approval of the final manuscript: All authors.
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