March, 2007
Fueling During Exercise
By Ellen Coleman, MA, MPH, RD
Today’s Dietitian
Vol. 9 No. 3 P. 12

Learning Code: 4060; CDR Level II

Competitive athletes and professional trainers and advisors are constantly seeking to maximize performance. Their quest for excellence has spawned an industry: nutritional supplements, drinks, and foods that make the right fuel available to the muscles in the right amounts at the right time.

Typically, these products are thought of in conjunction with endurance sports—marathons, cycling, etc. However, even casual exercisers and people involved in nonendurance sports that require periods of intense exertion spend billions of dollars on nutritional products. Are these “weekend warriors” wasting their money?

Dietitians need information on this complex subject to counsel their clients. This article provides an overview and update of current research and consensus opinions on the use of carbohydrates to maximize exercise efficiency and athletic performance while addressing the question of added protein. It will also address the questions of how much, what form, and when.

It is well-established that consuming carbohydrates during endurance exercise enhances performance by maintaining blood glucose levels and carbohydrate oxidation when muscle glycogen stores have dropped to low levels. Coyle and colleagues have demonstrated that consuming carbohydrate during cycling exercise at 70% of VO2 max can delay fatigue by 30 to 60 minutes.1,2 Practically speaking, the athlete can exercise longer and/or sprint harder at the end of exercise.

Now we learn that carbohydrates are no longer only for endurance athletes. Research suggests that carbohydrate feedings may also improve performance in stop-and-go sports such as football, basketball, soccer, and tennis, which require repeated bouts of high-intensity, short-duration effort.3-5

Blood Glucose and Exercise
Liver glycogen stores maintain blood glucose levels both at rest and during exercise. At rest, the brain and central nervous system utilize most of the blood glucose, and the muscle accounts for less than 20% of blood glucose utilization. During exercise, however, muscle glucose uptake can increase 30-fold, depending on exercise intensity and duration. The utilization of blood glucose rises as the exercise duration increases.

At the beginning of exercise, hepatic glucose output matches the increased muscle glucose uptake so blood glucose levels remain near resting levels. Although muscle glycogen is the primary source of carbohydrate during exercise intensities above 65% of VO2 max, blood glucose becomes an increasingly important source of carbohydrate as muscle glycogen stores decline. When hepatic glucose output can no longer keep up with muscle glucose uptake during prolonged exercise, the blood glucose level drops. While some athletes experience central nervous system symptoms typical of hypoglycemia, most athletes note local muscular fatigue and have to reduce their exercise intensity.

Carbohydrate and Endurance Exercise
Coyle and colleagues compared the effects of carbohydrate feedings on the onset of fatigue and decrease in work capacity of cyclists. The carbohydrate feedings enabled the cyclists to exercise an average of 33 minutes longer (159 minutes compared with 126 minutes) before reaching the point of fatigue. The carbohydrate feedings maintained blood glucose at higher levels, thereby increasing the utilization of blood glucose for energy.1

The Coyle group also measured performance during strenuous prolonged bicycling with and without carbohydrate feedings. During the ride without carbohydrate feedings, fatigue occurred after three hours and was preceded by a drop in blood glucose. During the ride with the cyclists who were fed carbohydrate, blood glucose levels were maintained, and the cyclists were able to ride an additional hour before reaching the point of fatigue. Both groups utilized muscle glycogen at the same rate, indicating that endurance was improved by maintaining blood glucose levels rather than glycogen sparing.2

Running performances with and without carbohydrate feedings have also been evaluated. During a 40-kilometer run in the heat, Millard-Stafford and colleagues found that a carbohydrate feeding (55 grams per hour) increased blood glucose levels and enabled runners to finish the last 5 kilometers significantly faster compared with the run without carbohydrate.6 In a treadmill run at 80% of VO2 max, Wilber and Moffatt found that the run time when fed carbohydrate (35 grams per hour) was 23 minutes longer (115 minutes) than the run without carbohydrate (92 minutes).7

During endurance exercise, carbohydrate feedings maintain blood glucose levels when muscle glycogen stores are diminished. Thus, carbohydrate utilization (and, therefore, adenosine triphosphate production) can continue at a high rate, and performance is enhanced.

The performance benefits of a preexercise carbohydrate feeding appear to be additive to those of consuming carbohydrate during exercise. In a study by Wright and colleagues, cyclists who received carbohydrate both three hours before and during exercise were able to exercise longer (289 minutes) than when receiving carbohydrate either before exercise (236 minutes) or during exercise (266 minutes).8

Combining carbohydrate feedings improved performance more than either feeding alone. However, the improvement in performance with preexercise carbohydrate feedings was less than when smaller quantities of carbohydrate were consumed during exercise. Thus, to obtain a continuous supply of glucose, athletes engaging in endurance exercise and stop-and-go sports should consume carbohydrate during exercise.

Carbohydrate and Intermittent Exercise
Nicholas and colleagues examined the effects of a 6.9% carbohydrate-electrolyte drink on performance during intermittent, high-intensity shuttle running designed to replicate the activity pattern of stop-and-go sports.3 The players who consumed carbohydrate rather than a placebo were able to run significantly longer (2 minutes) during the performance trial compared with the placebo (8.9 vs. 6.7 minutes). In a later study, Nicholas and associates evaluated the effect of carbohydrate feedings on muscle glycogen utilization during intermittent, high-intensity shuttle running.4 This study established that muscle glycogen utilization was reduced by 22% following ingestion of a carbohydrate-electrolyte drink that provided 51 grams of carbohydrate per hour.

Davis and colleagues evaluated the effect of carbohydrate feedings on performance during intermittent, high-intensity cycling.5 The average time to fatigue in the carbohydrate trial was 89 minutes (21 sprints) compared with 58 minutes (14 sprints) for the placebo. The results of these three studies suggest that the benefits of carbohydrate feedings are not limited to prolonged endurance exercise.

Carbohydrate feedings improve performance in stop-and-go sports by selectively sparing glycogen in type II muscle fibers, increasing glycogen resynthesis in type II muscle fibers during rest or low-intensity periods (or a combination of both).4

How Much Carbohydrate?
During moderate-intensity exercise, the maximum rate of exogenous carbohydrate oxidation from a single carbohydrate source such as glucose is approximately 1 gram per minute. When a mixture of glucose and sucrose or a mixture of glucose and fructose is ingested at a rate of 1.8 grams per minute, the rate of exogenous carbohydrate oxidation can reach 1.3 grams per minute. A mixture of two carbohydrate sources increases exogenous carbohydrate oxidation by approximately 20% to 55% compared with the ingestion of an isocaloric amount of glucose.

When glucose, fructose, and sucrose are ingested together during exercise at a rate of 2.4 grams per minute, the rate of exogenous carbohydrate oxidation can reach 1.7 grams per minute. A mixture of three carbohydrate sources increases exogenous carbohydrate oxidation by approximately 44% compared with an isocaloric amount of glucose.9

Practically speaking, the athlete can absorb and oxidize a maximum of 1 gram of carbohydrate per kilogram of body weight per hour from either carbohydrate-rich foods or fluids providing a mixture of carbohydrates.

Water absorption is also enhanced when carbohydrate-electrolyte solutions (sports drinks) include two or three different carbohydrate sources (glucose, sucrose, fructose, or maltodextrins) compared with solutions containing only one carbohydrate source. The addition of a second or third carbohydrate appears to activate additional mechanisms for intestinal solute transport, as well as involve transport by separate pathways that are noncompetitive.10

Liquid vs. Solid Carbohydrate
The benefits of consuming beverages containing carbohydrate during exercise are well-established.11 However, athletes often consume high-carbohydrate foods such as sports bars, fig bars, cookies, and fruit. The protein and fat found in many high-carbohydrate foods can delay gastric emptying. Despite this, liquid and solid carbohydrate feedings are equally effective in increasing blood glucose levels and improving performance.

Lugo and colleagues evaluated the metabolic effects of consuming liquid carbohydrate, solid carbohydrate, or both during two hours of cycling at 70% of VO2 max, followed by a time trial.12 The liquid was a 7% carbohydrate-electrolyte beverage, and the solid carbohydrate was a sports bar that provided 76% of calories from carbohydrate, 18% from protein, and 6% from fat. Each feeding provided 0.4 grams of carbohydrate per kilogram (an average of 28 grams per feeding and 56 grams per hour) and was consumed immediately before and every 30 minutes during the first 120 minutes of exercise.

While the caloric content of the treatments varied, they were isoenergetic with respect to carbohydrate. Carbohydrate availability and time trial performance were similar when equal amounts of carbohydrate were consumed as liquid, solid, or in combination. Regardless of carbohydrate form, there were no differences in blood glucose, insulin, or total carbohydrate oxidized during 120 minutes of cycling at 70% of VO2 max.12

Robergs and associates compared blood glucose and glucoregulatory hormone (insulin and glucagon) responses to solid and liquid carbohydrate feedings during two hours of cycling at 65% of VO2 max, followed by a 30-minute maximal isokinetic ride.13 The liquid was a 7% carbohydrate-electrolyte beverage, and the solid carbohydrate was a meal replacement bar that provided 67% of calories from carbohydrate, 10% from protein, and 23% from fat. Each feeding provided 0.6 grams of carbohydrate per kilogram of body weight per hour (an average of 20 grams per feeding and 40 grams per hour) and was consumed at 0, 30, 60, 90, and 120 minutes of exercise. Two resting glycemic response trials were also conducted. Following consumption of 75 grams of either liquid or solid carbohydrate, blood glucose and insulin levels were measured every 20 minutes for two hours.

The resting glycemic response study found that the liquid carbohydrate feeding was associated with greater insulin-dependent glucose disposal than the solid carbohydrate feeding for the same total carbohydrate intake. This was attributed to the combined protein, fat, and fiber in the solid carbohydrate, which are known to delay gastric emptying and subsequently blunt the insulin response to a given amount and type of carbohydrate in the food. However, there were no differences between liquid and solid carbohydrate feedings on blood glucose, glucoregulatory hormones, and exercise performance during prolonged cycling.13

Each carbohydrate form (liquid vs. solid) holds certain advantages for the athlete.14 Sports drinks and other liquids encourage the consumption of water needed to maintain hydration during exercise. Also, carbohydrate must be in a liquid or semiliquid state before leaving the stomach. However, compared with liquids, high-carbohydrate foods, sports bars, and gels can be easily carried by the athlete during exercise and provide both variety and satiety. Ingesting the amount of carbohydrate supplied by one PowerBar (47 grams) would require eating 11/2 bananas (45 grams).

Drinking 8 ounces (240 milliliters of a sports drink containing 4% to 8% carbohydrate [eg, Gatorade, Cytomax, or Powerade]) every 15 minutes can provide the proper amount of carbohydrate. For example, drinking 32 ounces each hour of a sports drink that contains 6% carbohydrate provides 56 grams of carbohydrate. Eating one PowerBar (47 grams), two gels (approximately 50 grams), or three large graham crackers (66 grams) every hour can also supply an adequate amount of carbohydrate.

Athletes should drink plenty of water when they eat solid foods, especially a sports bar. Otherwise, the product will settle poorly, and athletes may feel like they have a rock in their gut. In addition to aiding digestion, drinking water while eating solid foods encourages athletes to hydrate adequately.

Although it makes sense that athletes consume carbohydrate sources that are rapidly digested and absorbed to promote carbohydrate oxidation, the glycemic response to carbohydrate feedings during exercise has not been systematically studied. However, most athletes choose carbohydrate-rich foods (sports bars and gels) and fluids (sports drinks) that would be classified as having a moderate to high glycemic index.15

Athletes should eat and drink before feeling hungry or tired, usually within 30 to 60 minutes after starting to exercise. Consuming small amounts at frequent intervals (every 15 to 30 minutes) helps promote hydration, maintain blood glucose levels, and prevent gastrointestinal upset. The athletes’ foods and fluids should be familiar (tested in training), easily digested, and enjoyable (to encourage eating and drinking). New foods and fluids should never be tested during competition. The result may be severe indigestion and/or impaired performance.

Protein in Sports Drinks
Some practitioners claim that consuming carbohydrate-protein sports drinks during exercise provides greater performance benefits than sports drinks containing only carbohydrate.

Ivy and colleagues compared the effects of a carbohydrate with a carbohydrate-protein drink on variable intensity endurance performance.16 The nine trained male cyclists exercised on three separate occasions at intensities that varied between 45% and 75% of VO2 max for three hours, followed by a performance trial at 85% of VO2 max until fatigued. Every 20 minutes, the cyclists received either 200 milliliters of the placebo, a 7.75% carbohydrate solution, or a 7.75% carbohydrate and 1.94% protein solution. Compared with the placebo, the carbohydrate supplement improved performance by 36% and the carbohydrate-protein supplement improved performance by 55%.

While adding protein to the carbohydrate supplement improved performance, the mechanism was not apparent. The researchers provide three possible explanations for their results: The addition of protein to carbohydrate may have facilitated muscle glycogen sparing by an unknown process. The carbohydrate-protein supplement may have helped prevent central fatigue by maintaining plasma amino acids. Lastly, the addition of protein may have provided precursors for the reactions required to maintain Krebs cycle intermediates in the skeletal muscle.16

The researchers did not address whether the calorie difference between the two supplements may have influenced the study results. The carbohydrate supplement provided 46.5 grams of carbohydrate and 186 kilocalories per hour. The carbohydrate-protein supplement provided 46.5 grams of carbohydrate, 11.6 grams of protein, and 232 kilocalories per hour. Although only a difference of 46 kilocalories per hour, the 20% higher calorie content in the carbohydrate-protein supplement may have been responsible for the improvement in performance compared with the carbohydrate supplement.

Saunders and associates evaluated the effect of a carbohydrate (7.3%) and a carbohydrate-protein (7.3% and 1.8%) beverage on endurance cycling performance and postexercise muscle damage.17 Fifteen male cyclists rode a cycle ergometer at 75% of VO2max until fatigued, followed 12 to 15 hours later by a second ride to exhaustion at 85% of VO2 max. Subjects consumed 1.8 milliliters per kilogram of the carbohydrate or carbohydrate and protein beverage every 15 minutes during exercise and 10 milliliters per kilogram immediately after exercise. Beverages were matched for carbohydrate content, resulting in 20% lower total calorie intake from the carbohydrate beverage.

In the first ride at 75% of VO2 max, subjects rode 29% longer when consuming the carbohydrate-protein beverage compared with the carbohydrate beverage. In the second ride at 85% of VO2 max, the subjects performed 40% longer when consuming the carbohydrate-protein beverage compared with the carbohydrate beverage. Peak postexercise plasma creatine phosphokinase levels, indicative of muscle damage, were 83% lower after the carbohydrate-protein beverage compared with the carbohydrate beverage.

Although the carbohydrate-protein drink produced significant improvements in time to fatigue and reductions in muscle damage in endurance athletes, further research is necessary to determine whether these effects were the result of higher total calorie content of the carbohydrate-protein beverage or due to other specific protein-mediated mechanisms.

Romano-Ely and colleagues evaluated the effect of a carbohydrate-protein (7.5% and 1.8%) antioxidant beverage and an isocaloric carbohydrate-only (9.3%) beverage on endurance cycling performance and postexercise muscle damage.18 Fourteen male subjects rode a cycle ergometer at 70% of VO2 max until fatigued, followed 24 hours later by a second ride to exhaustion at 80% of VO2 max. The subjects consumed 2 milliliters per kilogram of the carbohydrate or carbohydrate-protein-antioxidant beverage every 15 minutes during exercise and 10 milliliters per kilogram immediately after exercise.

There were no significant differences between the two beverages for exercise time to fatigue at 70% of VO2 max and at 80% of VO2 max or for total performance time. Postexercise plasma creatine kinase and lactate dehydrogenase levels, indicative of muscle damage, were higher after the carbohydrate beverage compared with the carbohydrate-protein-antioxidant beverage.18

van Essen and Gibala have suggested that the practical relevance of these studies is hampered by the way the research was conducted. First, the rate of carbohydrate delivered in the carbohydrate drink was less than what is considered optimal for performance (less than 60 grams per hour) and second, the method of the performance test (exercise time to fatigue) did not mimic the manner in which athletes typically compete.19

van Essen and Gibala evaluated whether adding 2% protein to a 6% carbohydrate drink would improve 80-kilometer cycling time trial performance compared with a 6% carbohydrate drink and a noncaloric sweetened placebo. Ten male cyclists performed an 80-kilometer laboratory time trial on three occasions separated by one week. The subjects consumed 250 milliliters every 15 minutes of the carbohydrate-protein drink, carbohydrate drink, or placebo in a double-blind crossover design. The average performance time was identical during the carbohydrate and carbohydrate-protein trials, and both were significantly faster (by approximately 4%) than the placebo trial. This study demonstrated that when athletes ingested carbohydrate during exercise at a rate considered optimal for carbohydrate delivery, protein provided no additional performance benefit during an event that simulated cycling competition.19

Presently, research does not support the claim that consuming carbohydrate-protein sports drinks during exercise improves performance more than drinks containing an isocaloric amount of carbohydrate. Further research is required to determine whether consuming carbohydrate-protein beverages during exercise attenuates muscle damage following exercise.

Following exercise, the addition of protein to a carbohydrate feeding does not increase muscle glycogen synthesis compared with an isocaloric carbohydrate feeding.20 However, consuming a small amount of high-quality protein after exercise promotes muscle protein synthesis compared with an isocaloric amount of carbohydrate and may enhance the body’s response to long-term training.21

Summary
Consuming carbohydrate improves performance in both endurance and stop-and-go sports. Athletes can absorb and oxidize a maximum of 1 gram of carbohydrate per kilogram each hour. Consuming a mixture of two to three carbohydrate sources increases exogenous carbohydrate oxidation and water absorption. Adding protein to a sports drink does not improve performance compared with an isocaloric amount of carbohydrate.

— Ellen Coleman, MA, MPH, RD, is a nutrition consultant at The Sport Clinic in Riverside, Calif.

References
1. Coyle EF, Hagberg JM, Hurley BF, et al. Carbohydrate feeding during prolonged strenuous exercise can delay fatigue. J Appl Physiol. 1983;55(1 Pt 1):230-235.

2. Coyle EF, Coggan AR, Hemmert MK, et al. Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate. J Appl Physiol. 1986;61(1):165-172.

3. Nicholas CW, Williams C, Lakomy HK, et al. Influence of ingesting a carbohydrate-electrolyte solution on endurance capacity during intermittent, high-intensity shuttle running. J Sport Sci. 1995;13(4):283-290.

4. Nicholas CW, Tsintzas K, Boobis L, et al. Carbohydrate-electrolyte ingestion during intermittent high-intensity running. Med Sci Sports Exerc. 1999;31(9):1280-1286.

5. Davis JM, Jackson DA, Broadwell MS, et al. Carbohydrate drinks delay fatigue during intermittent high-intensity cycling in active men and women. Int J Sport Nutr. 1997;7(4):261-273.

6. Millard-Stafford ML, Sparling PB, Rosskopf LB, et al. Carbohydrate-electrolyte replacement improves distance running performance in the heat. Med Sci Sports Exerc. 1992;24(8):934-940.

7. Wilber RL, Moffatt RJ. Influence of carbohydrate ingestion on blood glucose and performance in runners. Int J Sport Nutr. 1994;2(4):317-327.

8. Wright DA, Sherman WM, Dernbach AR. Carbohydrate feedings before, during, or in combination improves cycling endurance performance. J Appl Physiol. 1991;71(3):1082-1088.

9. Jentjens RL, Achten J, Jeukendrup AE. High oxidation rates from combined carbohydrates ingested during exercise. Med Sci Sports Exerc. 2004;36(9):1551-1558.

10. Shi X, Summers RW, Schedl HP, et al. Effects of carbohydrate type and concentration and solution osmolality on water absorption. Med Sci Sports Exerc. 1995;27(12):1607-1615.

11. Position of the American Dietetic Association, Dietitians of Canada, and the American College of Sports Medicine: Nutrition and athletic performance. J Am Diet Assoc. 2000;100(12):1543-1556.

12. Lugo M, Sherman WM, Wimer GS, et al. Metabolic responses when different forms of carbohydrate energy are consumed during cycling. Int J Sport Nutr. 1993;3(4):398-407.

13. Robergs RA, McMinn SB, Mermier C, et al. Blood glucose and glucoregulatory hormone responses to solid and liquid carbohydrate ingestion during exercise. Int J Sport Nutr. 1998;8(1):70-83.

14. Coleman E. Update on carbohydrate: Solid versus liquid. Int J Sport Nutr. 1994;4(2):80-88.

15. Burke LM, Collier GR, Hargreaves M. Glycemic index—a new tool in sport nutrition? Int J Sport Nutr. 1998;8(4):401-415.

16. Ivy JL, Res PT, Sprague RC, et al. Effect of a carbohydrate-protein supplement on endurance performance during exercise of varying intensity. Int J Sports Nutr Exerc Metab. 2003;13(3):382-395.

17. Saunders MJ, Kane MD, Todd MK. Effects of a carbohydrate-protein beverage on cycling endurance and muscle damage. Med Sci Sports Exerc. 2004;36(7):1233-1238.

18. Romano-Ely BC, Todd MK, Saunders MJ, et al. Effect of an isocaloric carbohydrate-protein-antioxidant drink on cycling performance. Med Sci Sports Exerc. 2006;38(9):1608-1616.

19. van Essen M, Gibala MJ. Failure of protein to improve time trial performance when added to a sports drink. Med Sci Sports Exerc. 2006;38(8):1476-1483.

20. van Loon LJ, Saris WH, Kruijshoop M, et al. Maximizing postexercise muscle glycogen synthesis: Carbohydrate supplementation and the application of amino acid or protein hydrolysate mixtures. Am J Clin Nutr. 2000;72(1):106-111.

21. Borsheim E, Aarsland A, Wolfe RR. Effect of an amino acid, protein, and carbohydrate mixture on net muscle protein balance after resistance exercise. Int J Sport Nutr Exerc Metab. 2004;14(3):255-271.

Examination
1. Consuming carbohydrate during endurance exercise enhances performance by:
a. promoting sparing of muscle glycogen.
b. maintaining blood glucose levels and carbohydrate oxidation.
c. increasing fat metabolism.
d. promoting muscle glycogen resynthesis.
e. a and d

2. Consuming carbohydrate during stop-and-go exercise enhances performance by:
a. selectively sparing glycogen in type II muscle fibers.
b. increasing glycogen resynthesis in type II muscle fibers during rest or low-intensity periods.
c. increasing fat metabolism.
d. a and b
e. none of the above

3. The utilization of blood glucose decreases as the exercise duration increases.
a. True
b. False

4. The maximum rate of exogenous carbohydrate oxidation from a mixture of three carbohydrate sources is:
a. 1.7 grams per minute.
b. 1.3 grams per minute.
c. 1 gram per minute.
d. 0.5 grams per minute.
e. none of the above

5. An athlete can absorb and oxidize a maximum of ____ of carbohydrate per kilogram of body weight per hour of exercise.
a. 1.7 grams
b. 1.3 grams
c. 1 gram
d. 0.5 grams
e. None of the above

6. The following statement(s) is (are) true:
a. Sports drinks improve performance more than sports bars.
b. Liquid and solid carbohydrate feedings are equally effective in improving performance.
c. Each carbohydrate form holds certain advantages for the athlete.
d. a and c
e. b and c

7. The following statement(s) is (are) true about research studies comparing carbohydrate-protein beverages with carbohydrate beverages:
a. The higher calorie content in the carbohydrate-protein supplement may have been responsible for the improvement in performance compared with the carbohydrate supplement.
b. Carbohydrate-protein sports drinks provide greater performance benefits than sports drinks containing an isocaloric amount of carbohydrate.
c. Consuming carbohydrate-protein sports drinks during exercise does not improve performance more than drinks containing an isocaloric amount of carbohydrate.
d. a and b
e. a and c

8. Which of the following statement(s) is (are) true about research studies comparing carbohydrate-protein beverages with carbohydrate beverages:
a. Following exercise, the addition of protein to a carbohydrate feeding does not increase muscle glycogen synthesis compared with an isocaloric carbohydrate feeding.
b. More research is required to determine whether consuming carbohydrate-protein beverages during exercise may attenuate muscle damage following exercise.
c. Consuming a small amount of high-quality protein after exercise promotes muscle protein synthesis compared with an isocaloric amount of carbohydrate.
d. a, b, and c
e. a and c

9. An athlete weighing 70 kilograms can absorb and oxidize a maximum of:
a. 30 grams of carbohydrate each hour.
b. 40 grams of carbohydrate each hour.
c. 50 grams of carbohydrate each hour.
d. 60 grams of carbohydrate each hour.
e. 70 grams of carbohydrate each hour.

10. Consuming a mixture of two to three carbohydrate sources increases:
a. water absorption.
b. carbohydrate absorption.
c. the risk of gastrointestinal distress.
d. a and b
e. b and c