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Gender Differences in Carbohydrate Metabolism and Carbohydrate Loading

Abstract

Prior to endurance competition, many endurance athletes participate in a carbohydrate loading regimen in order to help delay the onset of fatigue. The "classic" regimen generally includes an intense glycogen depleting training period of approximately two days followed by a glycogen loading period for 3–4 days, ingesting approximately 60–70% of total energy intake as carbohydrates, while the newer method does not consist of an intense glycogen depletion protocol. However, recent evidence has indicated that glycogen loading does not occur in the same manner for males and females, thus affecting performance. The scope of this literature review will include a brief description of the role of estradiol in relation to metabolism and gender differences seen in carbohydrate metabolism and loading.

Introduction

During bouts of endurance exercise lasting longer than 90 minutes, fatigue generally coincides with low muscle glycogen content, suggesting that simply ingesting carbohydrates during exercise and having glucose available in the blood is not enough to sustain exercise for an extended period of time. This notion led researchers to believe that it may be necessary to load one's body with glucose prior to the long exercise bout [1]. Carbohydrate loading (>6 g/kg/d) prior to participation in an endurance exercise competition has been shown to help delay the onset of fatigue by approximately 20% during endurance events lasting longer than 90 minutes [24]. One exception to this rule is a study conducted by Burke et al.[5], where seven trained cyclists ingesting 6–9 g/kg/d of carbohydrate showed no improvement in performance in a 100 kilometer timed trial, despite significantly increased muscle glycogen concentrations.

Nutritional recommendations for endurance athletes directly prior to competition have traditionally included an intense glycogen depleting training period of approximately two days followed by a glycogen loading period for 3–4 days, ingesting approximately 60–70% of total energy intake as carbohydrates [6]. These recommendations were constructed based on several studies conducted for performance enhancement for this type of athlete [79]. However, most of these studies were conducted using only male subjects and the nutritional recommendations have since been used for populations including both males and females. This idea of normality across genders has recently proved to be incorrect as research has shown that there are many metabolic differences between genders that are stemmed from inherent hormonal differences. Specifically, the role of estradiol appears to be the mediator of these metabolic differences and could therefore affect the ability of a female to store, breakdown, and utilize carbohydrates in the same manner as a male [1013]. The scope of this literature review will include a brief description of the role of estradiol in relation to metabolism and gender differences seen in carbohydrate metabolism and loading.

The Role of Estradiol in Metabolism

Estradiol primarily serves in development of female secondary sex characteristics. This steroid hormone is secreted cyclically by ovaries, peaking at the time of ovulation (see Figure 1) [14]. In addition to assisting with development, estradiol has also been linked with various enzymes that play a role in energy metabolism. Decreased circulating levels of adipocyte lipoprotein lipase (LPL) has been correlated with high estradiol levels [15], which may result in enhanced triglyceride use in skeletal muscle at varying time points during the menstrual cycle [1619]. Some studies have also shown lipid utilization to be higher during the luteal phase of the menstrual cycle [20, 21]. In addition, there is no evidence that indicates variations in muscle glycogen concentrations throughout the menstrual cycle.

Figure 1
figure1

Secretory cycle of female gonadal hormones during a 28-day menstrual cycle. Note the increase in estradiol during the follicular phase just before ovulation, and more even levels during the luteal phase after ovulation. Adapted from http://wikipedia.org

Carbohydrate Metabolism

Prior to examining gender related differences in carbohydrate loading, gender differences between carbohydrate metabolism must be examined. There appears to be no difference between genders in basal levels of muscle glycogen [13, 2224], skeletal muscle GLUT-4 [25], or hexokinase [13]. However, females do appear to have an enhanced sensitivity to insulin in skeletal muscle [19], which would theoretically result in increased muscle glycogen storage, as well as enhanced fat storage, but the gender differences in insulin sensitivity are beyond the scope of this paper. In addition, there have yet to be any studies conducted assessing differences in glycogen synthase activity or branching enzyme [26]. Knowledge of changes of these enzymes could assist in the understanding of inherent metabolic differences that exist between genders.

Differences in Substrate Utilization

While there appears to be no inherent difference at basal levels of muscle glycogen, there does appear to be a gender related difference in the actual breakdown and metabolism of carbohydrates (Table 1 provides a summary of specific studies). There is evidence that females tend to oxidize less total carbohydrate than men; however, the mechanism behind this phenomenon remains unclear [26]. One possible explanation could be that women have a lower rate of glucose appearance than that of men during endurance exercise [2729]. Roepstorff et al. [29] assessed gender differences in substrate utilization during submaximal exercise. Males and females were matched according to peak oxygen consumption (VO2peak) per kg lean body mass, training history, and physical activity level. All females were tested during mid-follicular phase of the menstrual cycle to avoid possible elevated lipid utilization that has been shown during the luteal phase [20, 21]. Results of the study showed no gender differences for utilization of fatty acids, blood glucose, and glycogen, and that females oxidized more myocellular triglycerides than males, making up 25% of total VO2peak for females and only 5% of total VO2peak for males. This indicates that while there were no gender differences in the relative contribution of carbohydrates and lipids, there does seem to be a difference in the utilization of various lipid sources. This coincides with observations seen at rest, indicating greater utilization of fatty acids in the skeletal muscle rather than those derived from the adipose tissue [1619].

Table 1 Articles related to gender differences in substrate utilization

Tarnopolsky et al. [22, 23] conducted two similar studies evaluating glycogen depletion in the vastus lateralis during endurance exercise. The 1990 study [22] showed that women had significantly less glycogen depletion than men during treadmill running, but the 1995 study [23] showed no gender difference in glycogen depletion during submaximal cycling. Despite no difference in glycogen depletion, the study did show that women oxidized significantly more lipid and less carbohydrate and protein compared to men during an exercise bout at 75% VO2peak. These data concur with previous observations of greater lipid oxidation of females during submaximal endurance exercise [18, 30, 31], but the source of fatty acids differ. It appears as though females tend to utilize more fatty acids from adipose tissue during submaximal exercise, whereas the main source of increased fatty acid utilization at rest is from skeletal muscle [1619]. Romijin and colleagues [32, 33] also addressed intensity in relation to gender differences in substrate utilization in rats. In both studies, the participants exercised at intensities of 25, 65, and 85% of VO2max. The 1993 study [32] showed that in males muscle triglyceride lipolysis was stimulated only at higher intensities and that at 65% VO2max muscle glycogen and triglyceride oxidation decreased. The 2000 [33] study showed that in females carbohydrate oxidation increased progressively with exercise intensity, and that the highest rate of fat oxidation was during exercise at 65% of VO2max. When comparing the two studies, the authors concluded that after correction for differences in lean body mass, there were no differences between these results and previously reported data in endurance-trained men studied under the same conditions, except for slight differences in glucose metabolism during low-intensity exercise [33]. It is important to note that not all of these studies controlled for variations of lipid metabolism during the menstrual cycle, thus the observed differences between rest and exercise may simply be due to measurement of fatty acid utilization during different phases of the menstrual cycle.

Tarnopolsky also assessed glycogen use in the vastus lateralis via muscle biopsy over the course of a 31-day endurance cycling training protocol [13] and found no gender difference in glycogen sparing. A possible explanation of this contradiction with previous literature could be from different muscle recruitment between running and cycling. However, two other studies found that men use more glycogen than women during cycle exercise, but these two studies assessed glycogen use via a stable isotope method rather than muscle biopsy [28, 34].

Horton et al. [18] conducted a study to assess gender differences in fuel metabolism during long-duration exercise. Fuel oxidation was measured using indirect calorimetry and blood samples were drawn for circulating substrate and hormone levels. Results indicated that females expended more total energy from fat oxidation (50.9%) than that of men (43.7%), but less total energy from carbohydrates (45.7% for women and 53.1% for men). In addition to differences in fuel metabolism, males also had higher circulating levels of catecholamines. These results suggest that females may be more sensitive to the lipolytic actions of catecholamines than men.

Effects of Estradiol Administration

With the knowledge that females tend to oxidize a greater amount of fatty acids than males, researchers then assessed the effects of estradiol administration to males. Results indicated that with the addition of 17-β-estradiol to male rats, breakdown of muscle tissue was not diminished during endurance exercise [35]. In fact, administration of 17-β-estradiol to males and oophorectomized female rats resulted in hepatic and muscle glycogen sparing during endurance exercise [36], increased intramuscular triglyceride content, and decreased adipocyte LPL [10]. Similar results have been observed in human studies with 17-β-estradiol administration to males [37] and ammenorrheic females [38] resulting in a lower rate of glucose disappearance. The addition of 17-β-estradiol also appears to increase the activity of enzymes in fat oxidation pathways such as carnotine-palmitoyl transferase-1 (CPT-1) [39]. The role of CPT-1 is to transfer the fatty acyl group from CoA to carnitine on the cytosolic side of the inner membrane. Enhancement of this pathway allows for greater oxidation of fatty acids in skeletal muscle [40]. Together, these findings suggest that the gender-related differences in carbohydrate metabolism and glycogen use in skeletal muscle may be due to both hepatic glycogen sparing [26], as well as enhanced muscle triglyceride utilization [19].

Carbohydrate Loading

Increased dietary carbohydrate intake can result in enhanced endurance exercise performance by increasing muscle glycogen stores [26], but may not in all instances as displayed by Burke et al. [5] Most of the early studies proving this performance enhancing strategy were conducted with predominantly male subjects [79]. The need to assess gender differences with carbohydrate loading and glycogen storage stems from altered glycogen storing ability at different phases of the menstrual cycle [41] and the influence of estradiol on glycogen utilization [11, 12, 36]. One of the first studies to evaluate a possible gender difference in glycogen storage after carbohydrate loading was conducted by Tarnopolsky et al. in 1995 [23]. In this study, male and female runners were asked to increase carbohydrate intake for four days, manipulating carbohydrate intake from 55% to 75% of total energy intake. The results of the study showed that men increased muscle glycogen content 41% and improved performance time 45% following a one-hour cycling bout, whereas women showed no increase in muscle glycogen and improved performance time by only 5%. The authors speculated that a possible reason for this gender-related difference could be that the increase in dietary carbohydrate intake may not have been enough to elicit glycogen super-compensation. The female participants in this particular study ingested 6.4 g/kg body weight of carbohydrate, while the men ingested 8.2 g/kg body weight of carbohydrate. However, several studies suggest that there is a "carbohydrate loading threshold," of 8–10 g/kg that is necessary to achieve the ergogenic benefits of carbohydrate loading [79, 42].

With this knowledge of a "carbohydrate loading threshold," James et al. [43] also conducted a study to assess these gender differences, but rather than a moderate increase in dietary carbohydrate intake, participants ingested a carbohydrate level of 12 g/kg of fat free mass per day. James found that by regulating for fat free mass in conjunction with cessation of daily physical training, women and men were able to achieve similar levels of glycogen super-compensation.

After the "carbohydrate loading threshold" was determined, three other studies [13, 43, 44] assessed the loading ability of females at this level of dietary carbohydrate ingestion and found that in order to achieve this intake, women would need to increase their total energy intake by 34% during the carbohydrate loading period. By increasing energy intake 34%, females were able to achieve similar concentrations of glycogen as males, and there were no gender differences in hexokinase activity [13]. However, one study found that even with this increase in carbohydrate ingestion, the females were only able to achieve an increase in glycogen stores that was 50% of what was observed in males [44]. Therefore, for a female to carbohydrate load and achieve benefits comparable to those of a male, the female must consume extra calories rather than simply increasing the percentage of dietary carbohydrate load. Specifically, a female needs to consume about 30% more daily energy for four days to ensure that carbohydrate intake achieves levels higher than 8 g/kg/d [13]. For a 55 kg distance runner, this would be 440 g of carbohydrate, equaling about 1760 calories daily. If this runner is active and consuming 2500 calories per day, this would represent approximately 70% of the total daily energy intake from carbohydrate, which is in concurrence with current recommendations, and is only 5% higher than the 45–65% American Daily Recommendation for carbohydrate. One possible option that may assist with increased carbohydrate consumption and increased carbohydrate utilization is to employ both a loading method and carbohydrate supplementation prior to competition. Andrews et al. [1] showed that females used significantly more carbohydrates during submaximal performance following carbohydrate loading and supplementation compared to females who either only supplemented carbohydrates or ingested a placebo. However, the difference in performance time was negligible between three groups.

Conclusion and Future Recommendations

Despite many questions that remain to be answered in regards to gender differences in carbohydrate metabolism during endurance exercise, it appears as though female athletes do have the capacity for glycogen super-compensation at levels comparable to males when fed comparable amounts of carbohydrates relative to lean body mass [43]. In order to enhance glycogen-storing ability and obtain peak performance from female endurance athletes, it is necessary for future studies to control for menstrual cycle phase. In addition, future studies should assess the influence of estradiol on energy substrate utilization at rest and during various submaximal bouts of endurance exercise in relation to glycogen storage. With this research and knowledge, female athletes could not potentially erase physiological gender differences, but gender differences in performance as well.

References

  1. 1.

    Andrews JL, Sedlock DA, Flynn MG, Navalta JW: Carbohydrate loading and supplementation in endurance-trained women runners. J Appl Physiol. 2003, 95: 584–90.

    CAS  Article  Google Scholar 

  2. 2.

    Hawley JA, Schabort EJ, Noakes TD, Dennis SC: Carbohydrate-loading and exercise performance. An update. Sports Med. 1997, 24: 73–81. 10.2165/00007256-199724020-00001.

    CAS  Article  Google Scholar 

  3. 3.

    Lambert EV, Goedecke JH: The role of dietary macronutrients in optimizing endurance performance. Curr Sports Med Rep. 2003, 2: 194–201. 10.1007/s11932-003-0005-6.

    Article  Google Scholar 

  4. 4.

    Kiens B: Diet and training in the week before competition. Can J Appl Physiol. 2001, 26 (Suppl): S56–63.

    Article  Google Scholar 

  5. 5.

    Burke LM, Hawley JA, Schabort EJ, St Clair Gibson A: Carbohydrate loading failed to improve 100-km cycling performance in a placebo-controlled trial. J Appl Physiol. 2000, 88: 1284–90.

    CAS  Article  Google Scholar 

  6. 6.

    Brooks GA, Fahey TD, White TP, Baldwin KP: Exercise Physiology: Human Bioenergetics and Its Appplications. 2000, London: Mayfield, 3

    Google Scholar 

  7. 7.

    Bergstrom J, Hermansen L, Hultman E, Saltin B: Diet, muscle glycogen and physical performance. Acta Physiol Scand. 1967, 71: 140–50.

    CAS  Article  Google Scholar 

  8. 8.

    Karlsson J, Saltin B: Diet, muscle glycogen, and endurance performance. J Appl Physiol. 1971, 31: 203–6.

    CAS  Article  Google Scholar 

  9. 9.

    Sherman WM, Costill DL, Fink WJ, Miller JM: Effect of exercise-diet manipulation on muscle glycogen and its subsequent utilization during performance. Int J Sports Med. 1981, 2: 114–8.

    CAS  Article  Google Scholar 

  10. 10.

    Ellis GS, Lanza-Jacoby S, Gow A, Kendrick ZV: Effects of estradiol on lipoprotein lipase activity and lipid availability in exercised male rats. J Appl Physiol. 1994, 77: 209–15.

    CAS  Article  Google Scholar 

  11. 11.

    Kendrick ZV, Ellis GS: Effect of estradiol on tissue glycogen metabolism and lipid availability in exercised male rats. J Appl Physiol. 1991, 71: 1694–9.

    CAS  Article  Google Scholar 

  12. 12.

    Rooney TP, Kendrick ZV, Carlson J, Ellis GS: Effect of estradiol on the temporal pattern of exercise-induced tissue glycogen depletion in male rats. J Appl Physiol. 1993, 75: 1502–6.

    CAS  Article  Google Scholar 

  13. 13.

    Tarnopolsky MA, Zawada C, Richmond LB, Carter S: Gender differences in carbohydrate loading are related to energy intake. J Appl Physiol. 2001, 91: 225–30.

    CAS  Article  Google Scholar 

  14. 14.

    Menstrual Cycle. 2006, [cited], [http://en.wikipedia.org/wiki/Image:MenstrualCycle.png]

  15. 15.

    Schaefer EJ, Lamon-Fava S, Spiegelman D, Dwyer JT: Changes in plasma lipoprotein concentrations and composition in response to a low-fat, high-fiber diet are associated with changes in serum estrogen concentrations in premenopausal women. Metabolism. 1995, 44: 749–56. 10.1016/0026-0495(95)90188-4.

    CAS  Article  Google Scholar 

  16. 16.

    Hardman AE: Interaction of physical activity and diet: implications for lipoprotein metabolism. Public Health Nutr. 1999, 2: 369–76.

    CAS  Article  Google Scholar 

  17. 17.

    Millet L, Barbe P, Lafontan M, Berlan M: Catecholamine effects on lipolysis and blood flow in human abdominal and femoral adipose tissue. J Appl Physiol. 1998, 85: 181–8.

    CAS  Article  Google Scholar 

  18. 18.

    Horton TJ, Pagliassotti MJ, Hobbs K, Hill JO: Fuel metabolism in men and women during and after long-duration exercise. J Appl Physiol. 1998, 85: 1823–32.

    CAS  Article  Google Scholar 

  19. 19.

    Driskell JA, Wolinsky I: Energy-Yielding Macronutrients and Energy Metabolism in Sports Nutrition. 2000, Boca Raton: CRC Press

    Google Scholar 

  20. 20.

    Galliven EA, Singh A, Michelson D, Bina S: Hormonal and metabolic responses to exercise across time of day and menstrual cycle phase. J Appl Physiol. 1997, 83: 1822–31.

    CAS  Article  Google Scholar 

  21. 21.

    Hackney AC, McCracken-Compton MA, Ainsworth B: Substrate responses to submaximal exercise in the midfollicular and midluteal phases of the menstrual cycle. Int J Sport Nutr. 1994, 4: 299–308.

    CAS  Article  Google Scholar 

  22. 22.

    Tarnopolsky LJ, MacDougall JD, Atkinson SA, Tarnopolsky MA: Gender differences in substrate for endurance exercise. J Appl Physiol. 1990, 68: 302–8.

    CAS  Article  Google Scholar 

  23. 23.

    Tarnopolsky MA, Atkinson SA, Phillips SM, MacDougall JD: Carbohydrate loading and metabolism during exercise in men and women. J Appl Physiol. 1995, 78: 1360–8.

    CAS  Article  Google Scholar 

  24. 24.

    Lamont LS, McCullough AJ, Kalhan SC: Gender differences in leucine, but not lysine, kinetics. J Appl Physiol. 2001, 91: 357–62.

    CAS  Article  Google Scholar 

  25. 25.

    Hansen PA, McCarthy TJ, Pasia EN, Spina RJ: Effects of ovariectomy and exercise training on muscle GLUT-4 content and glucose metabolism in rats. J Appl Physiol. 1996, 80: 1605–11. 10.1063/1.362958.

    CAS  Article  Google Scholar 

  26. 26.

    Tarnopolsky M: Females and males: Should nutritional recommendations be gender specific?. Sportmedizin und Sporttraumatologie. 2003, 51: 39–46.

    Google Scholar 

  27. 27.

    Friedlander AL, Casazza GA, Horning MA, Huie MJ: Training-induced alterations of carbohydrate metabolism in women: women respond differently from men. J Appl Physiol. 1998, 85: 1175–86.

    CAS  Article  Google Scholar 

  28. 28.

    Carter S, McKenzie S, Mourtzakis M, Mahoney DJ: Short-term 17beta-estradiol decreases glucose R(a) but not whole body metabolism during endurance exercise. J Appl Physiol. 2001, 90: 139–46.

    CAS  Article  Google Scholar 

  29. 29.

    Roepstorff C, Steffensen CH, Madsen M, Stallknecht B: Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects. Am J Physiol Endocrinol Metab. 2002, 282: E435–47.

    CAS  Article  Google Scholar 

  30. 30.

    Mittendorfer B, Horowitz JF, Klein S: Effect of gender on lipid kinetics during endurance exercise of moderate intensity in untrained subjects. Am J Physiol Endocrinol Metab. 2002, 283: E58–65.

    CAS  Article  Google Scholar 

  31. 31.

    Tate CA, Holtz RW: Gender and fat metabolism during exercise: a review. Can J Appl Physiol. 1998, 23: 570–82.

    CAS  Article  Google Scholar 

  32. 32.

    Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A: Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol. 1993, 265: E380–91.

    CAS  PubMed  Google Scholar 

  33. 33.

    Romijn JA, Coyle EF, Sidossis LS, Rosenblatt J: Substrate metabolism during different exercise intensities in endurance-trained women. J Appl Physiol. 2000, 88: 1707–14.

    CAS  Article  Google Scholar 

  34. 34.

    Ruby BC, Coggan AR, Zderic TW: Gender differences in glucose kinetics and substrate oxidation during exercise near the lactate threshold. J Appl Physiol. 2002, 92: 1125–32.

    CAS  Article  Google Scholar 

  35. 35.

    Tarnopolsky MAES, MacDonald JR, Roy BD, MacKenzie S: Short-term 17-beta-estradiol administration does not affect metabolism in young males. Int J Sports Med. 2000, 21: 1–6. 10.1055/s-2000-8847.

    Article  Google Scholar 

  36. 36.

    Kendrick ZV, Steffen CA, Rumsey WL, Goldberg DI: Effect of estradiol on tissue glycogen metabolism in exercised oophorectomized rats. J Appl Physiol. 1987, 63: 492–6.

    CAS  Article  Google Scholar 

  37. 37.

    Ruby BC, Robergs RA, Waters DL, Burge M: Effects of estradiol on substrate turnover during exercise in amenorrheic females. Med Sci Sports Exerc. 1997, 29: 1160–9.

    CAS  Article  Google Scholar 

  38. 38.

    Carter SL, Rennie CD, Hamilton SJ, Tarnopolsky : Changes in skeletal muscle in males and females following endurance training. Can J Physiol Pharmacol. 2001, 79: 386–92. 10.1139/cjpp-79-5-386.

    CAS  Article  Google Scholar 

  39. 39.

    Campbell SE, Febbraio MA: Effect of ovarian hormones on mitochondrial enzyme activity in the fat oxidation pathway of skeletal muscle. Am J Physiol Endocrinol Metab. 2001, 281: E803–8.

    CAS  Article  Google Scholar 

  40. 40.

    Borer KT: Exercise Endocrinology. 2003, Champagne: Human Kinetics

    Google Scholar 

  41. 41.

    Nicklas BJ, Hackney AC, Sharp RL: The menstrual cycle and exercise: performance, muscle glycogen, and substrate responses. Int J Sports Med. 1989, 10: 264–9.

    CAS  Article  Google Scholar 

  42. 42.

    Burke LM, Hawley JA: Carbohydrate and exercise. Curr Opin Clin Nutr Metab Care. 1999, 2: 515–20. 10.1097/00075197-199911000-00015.

    CAS  Article  Google Scholar 

  43. 43.

    James AP, Lorraine M, Cullen D, Goodman C: Muscle glycogen supercompensation: absence of a gender-related difference. Eur J Appl Physiol. 2001, 85: 533–8. 10.1007/s004210100499.

    CAS  Article  Google Scholar 

  44. 44.

    Walker JL, Heigenhauser GJ, Hultman E, Spriet LL: Dietary carbohydrate, muscle glycogen content, and endurance performance in well-trained women. J Appl Physiol. 2000, 88: 2151–8.

    CAS  Article  Google Scholar 

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Wismann, J., Willoughby, D. Gender Differences in Carbohydrate Metabolism and Carbohydrate Loading. J Int Soc Sports Nutr 3, 28 (2006). https://doi.org/10.1186/1550-2783-3-1-28

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Keywords

  • glycogen loading
  • estradiol
  • eummenorrheic