International Journal of Sport Nutrition and Exercise Metabolism, 2014, 24, 553 -558 http://dx.doi.org/10.1123/ijsnem.2014-0069 © 2014 Human Kinetics, Inc.
www.IJSNEM-Journal.com RAPID COMMUNICATION
Dairy-Based Preexercise Meal Does Not Affect Gut Comfort or Time-Trial Performance in Female Cyclists Eric C. Haakonssen, Megan L. Ross, Louise E. Cato, Alisa Nana, and Emma J. Knight Australian Institute of Sport
David G. Jenkins University of Queensland
David T. Martin and Louise M. Burke Australian Institute of Sport Some athletes avoid dairy in the meal consumed before exercise due to fears about gastrointestinal discomfort. Regular exclusion of dairy foods may unnecessarily reduce intake of high quality proteins and calcium with possible implications for body composition and bone health. This study compared the effects of meals that included (Dairy) or excluded (Control) dairy foods on gastric comfort and subsequent cycling performance. Well-trained female cyclists (n = 32; mean ± SD; 24.3 ± 4.1 y; VO2peak 57.1 ± 4.9 ml/kg/min) completed two trials (randomized cross-over design) in which they consumed a meal (2 g/kg carbohydrate and 54 kJ/kg) 2 hr before a 90-min cycle session (80 min at 60% maximal aerobic power followed by a 10-min time trial; TT). The dairy meal contained 3 servings of dairy foods providing ~1350 mg calcium. Gut comfort and palatability were measured using questionnaires. Performance was measured as maximum mean power during the TT (MMP10min). There was no statistical or clinical evidence of an effect of meal type on MMP10min with a mean difference (Dairy – Control) of 4 W (95% CI [–2, 9]). There was no evidence of an association between pretrial gut comfort and meal type (p = .15) or between gut comfort delta scores and meal type postmeal (p = .31), preexercise (p = .17) or postexercise (p = .80). There was no statistical or clinical evidence of a difference in palatability between meal types. In summary, substantial amounts of dairy foods can be included in meals consumed before strenuous cycling without impairing either gut comfort or performance. Keywords: bone, calcium, cycling Endurance athletes may avoid dairy foods in meals consumed before high-intensity exercise due to fears about negative side-effects or to preferentially increase carbohydrate intake. Although the perception that dairy foods increase mucous production is disproved (Wüthrich et al., 2005), concerns persist that they may cause gasHaakonssen, Ross, Cato, Nana, and Burke are with the Dept. of Sports Nutrition, Knight the Dept. of Performance Research, and Martin the Dept. of Physiology, Australian Institute of Sport, Belconnen, Australia. Jenkins is with the Dept. of Human Movement Studies, University of Queensland, St. Lucia, Australia. Address author correspondence to Eric C. Haakonssen at [email protected].
trointestinal (GI) discomfort (de Vrese et al., 2001; Ray, 2013) thus impairing performance. Exclusion of dairy foods from preexercise meals may unnecessarily reduce an athlete’s total intake of proteins with high biological value and calcium which may favorably influence body composition (Phillips & Zemel, 2011; Zemel, 2004) and bone health (Cao et al., 2014). Recent investigations have shown that consuming calcium supplements before and during exercise may attenuate bone resorption by maintaining calcium homeostasis, which may be perturbed by sweat calcium losses (Barry et al., 2011; Guillemant et al., 2004). Dairy may present an option to increase preexercise calcium intake while meeting other sports nutrition goals. Before this is investigated it is important to ascertain how dairy affects gut comfort and performance.
553
554 Haakonssen et al.
The aim of this study was to investigate the effects of a dairy-based preexercise meal on GI comfort and subsequent exercise performance. A population of well-trained female cyclists was chosen due to our previous observations of their perceptions about dairy foods as well as their known problems with body composition management (Haakonssen et al., 2014) and bone health (Sherk et al., 2013). It was hypothesized that a dairy based preexercise meal would not significantly affect performance or gut comfort following intense cycling. This study was part of a larger investigation of bone turnover and calcium homeostasis in response to exercise.
Methods Subjects Thirty-two healthy, competitive female cyclists (mean ± SD; 24.3 ± 4.1 y, 60.9 ± 7.5 kg, 169.3 ± 7.0 cm, maximal aerobic power (MAP) 283 ± 28 W, peak oxygen consumption (V̇ O2peak) 57.1 ± 4.9 ml/kg/≥ min) were recruited from the 107 female cyclists registered with Australian National Road Series teams with an average (± SD) race attendance of 47 ± 16. Of these, 33 expressed interest in participating and 25 met inclusion criteria (17 to 32 years; 18-month racing experience). The remaining participants included an international professional, an ultra-endurance mountain biker and five well-trained national club-level cyclists. This study was approved by the human research ethics committee of the Australian Institute of Sport. Subjects were informed of testing protocols and risks of the study before providing written informed consent.
Baseline Fitness Test Maximal aerobic power (MAP) was determined using an incremental step test on a cycle ergometer (Lode Excalibur Sport, Groningen, Netherlands) starting at 125 W and increasing 25 W every 3 min until volitional fatigue. MAP was calculated as the highest mean power maintained for the last 3 min of the test.
Pretrial Diet Standardization For 24-hr before each experimental trial, subjects consumed a standardized prepackaged diet providing 5.0 g/ kg BM carbohydrate (CHO), 1.5 g/kg BM protein and 1.5 g/kg BM fat. The first 22 hr of the standard diet was supplied in the form of prepackaged meals, with the pretrial meal (accounting for the final 2 hr) provided to subjects in the laboratory. Individualized menus were prepared accounting for food preferences and intolerances using FoodWorks Professional Edition (v6.0, Xyris Software, Brisbane, Australia), as previously described (Jeacocke & Burke, 2010). In the case of gluten sensitivity (n = 2) and lactose-intolerance (n = 1), low lactose and gluten-free versions of foods matched for nutrient composition were used. Training was standardized for both pretrial days. Subjects refrained from alcohol consumption over the 24-hr period but followed (and replicated) usual prerace caffeine habits for the pretrial meal. Compliance to the diet, determined from a self-reported checklist, was noted by a dietitian on the morning of the trial.
Preexercise Meal Interventions This was a randomized, counterbalanced crossover design. The preexercise meals were scaled to provide 54 kJ/kg and 2 g/kg BM CHO. The dairy-rich meal (Dairy) consisted of rolled-oats cooked with calcium-fortified (Tricalcium phosphate, Nano-calcium) Anlene milk (Fonterra, Auckland, NZ), yogurt (Yoplait, BoulogneBillancourt, France) and additional milk while the Control meal provided oats cooked with water and served with canned fruit and nuts (see Table 1). Since the Dairy meal provided more protein and less fat than Control, the standardized meals were manipulated to match total protein and fat intake over the whole 24-hr period (see Table 2). The Dairy meal provided ~1350 mg of calcium and an equivalent of three servings of dairy foods. Meals were designed to look similar although cyclists were not blinded to the meal condition given the difficulty of concealing such a high dairy content.
Table 1 Example Preexercise Breakfast for Dairy and Control Trials for 60 kg Cyclist Dairy Uncle Toby’s quick oats
Control 57 g
Anlene milk
500 ml
Uncle Toby’s quick oats
65 g
water
250 ml
Yoplait yogurt vanilla
175 g
Goulburn Valley fruit salad diced
140 g
Brown sugar
13 g
brown sugar
23 g
Sultanas
20 g
sultana
23 g
macadamias
24 g
MeadowLea margarine sachet Just Juice, apple
15g 200 ml
Effects of Dairy on Cycling Performance 555
Table 2 Macronutrient Composition and Calcium Content of Standardized Diets for the Dairy and Control Trials Nutrient
24-hr Dietary Standardization Dairy (x– ± SD) Control (x– ± SD)
Preexercise Breakfast Dairy (x– ± SD) Control (x–± SD)
Energy(kJ·kg-1)
169 ± 4
170 ± 4
54 ± 2
54 ± 2
CHO (g·kg-1)
5.1 ± 0.2
5.1 ± 0.2
2.0 ± 0.0
2.0 ± 0.0
Protein (g·kg-1)
1.5 ± 0.0
1.5 ± 0.0
0.6 ± 0.1
0.2 ± 0.0
Fat (g·kg-1)
1.5 ± 0.0
1.5 ± 0.0
0.3 ± 0.0
0.4 ± 0.0
1658 ± 174
640 ± 226
1352 ± 53
46 ± 7
Calcium (mg)
Exercise Protocol Two hours after starting the pretrial breakfast, cyclists cycled on an ergometer (Watttbike Ltd. Nottingham, UK) at 60% MAP for 80 min (intensity based on race data from Ebert et al (2005)) followed by a 10 min time trial (TT) during which they were instructed to maintain the maximum mean power for the duration (MMP10min). The TT was limited to 10 min to avoid fatigue for the second trial. The two trial days started 48 hour apart to minimize changes in menstrual status. Cyclists were blinded to heart rate, power and cadence but were able to see time remaining. Water was consumed ad libitum during the first trial and this hydration strategy was replicated during the second trial. Cyclists consumed a carbohydrate gel (27 g; PowerBar PowerGel, Australia) at 30 and 65 min.
Questionnaires We developed a Likert questionnaire to check gastrointestinal comfort during the trial. Cyclists were asked at five time points (before pretrial meal, 30 min and 60 min after starting pretrial meal, immediately preexercise, and immediately postexercise) how comfortable does your stomach feel at the moment?, according to a five point scale (1 = very comfortable; 2 = comfortable; 3 = average comfort; 4 = uncomfortable; 5 = very uncomfortable). Cyclists were made aware that gut comfort is a different construct to hunger or satiety and that discomfort on this scale included symptoms such as nausea, bloating and gut pain. After consuming the pretrial meal, cyclists were asked to indicate how strongly they felt about five criteria relating to that meal (visual appeal, smell, taste, aftertaste, palatability) using a palatability questionnaire (Flint et al., 2000). Responses were recorded on 100 mm visual analog scales (VAS).
Data Analyses The effect of pretrial meal type on MMP10min was investigated using a linear mixed model with meal (Dairy or Control) as a fixed effect and subject as a random effect. Fisher’s exact test was used to assess the association between pretrial meal gut comfort and meal type.
Postmeal gut comfort responses were normalized to the pretrial response. A negative value implied a relative reduction in gut comfort from pretrial with the converse true for a positive value. Fisher’s exact tests were used to assess the association between pretrial meal type and the delta scores for each of the four postmeal time points. To examine the difference in VAS palatability scores between the two meal types, paired t tests were used for each of the palatability criteria. Statistical analyses were conducted using JMP Pro v10 (SAS Institute Inc., Cary, NC, USA).
Results The average MMP10min was 4 W higher for Dairy compared with Control (95% CI [–2, –9]). This is not a statistically significant difference (t31 = 1.35, p = .19) and it is not a clinically meaningful difference as it is less than the margin of reliability (~2%) of the Wattbike at these power outputs (Hopker et al., 2010). Fisher’s exact test showed no evidence of a statistically significant association between pretrial meal gut comfort (Table 3) and meal type (p = .15), and no evidence of a statistically significant association between gut comfort delta scores (Table 3) and meal type at 30 min (p = .31) or 60 min postmeal (p = .17); immediately preexercise (p = .80) or immediately postexercise (p = .77). The estimated differences in mean VAS palatability suggest that for all criteria except for aftertaste, the dairy meal may have been slightly more palatable (Table 4). However, the differences were not statistically significant or clinically meaningful based on a minimal clinically significant difference of 20 mm (Fischer & Singer, 1999).
Discussion In contrast to the beliefs of some athletes, we found that consuming substantial amounts of dairy foods in a meal consumed ~90 min before prolonged strenuous stationary cycling neither impaired nor enhanced gut comfort or performance compared with a control breakfast that excluded dairy foods. Consuming dairy foods during the preexercise breakfast should assist in increasing total daily intake
556 Haakonssen et al.
Table 3 Frequency Distribution of Gut Comfort Scores Across Time Points for Dairy and Control Meal Conditions Pre-Trial
1
2
3
4
5
Dairy
15
8
6
1
2
Control
9
16
5
2
0
Change Scoresa –4
–3
–2
–1
0
1
2
dairy
1
2
7
8
10
3
1
control
0
0
4
7
14
7
0
dairy
0
0
5
10
13
3
1
control
0
1
2
5
14
9
1
dairy
0
0
4
13
9
4
2
control
1
1
4
11
10
5
0
dairy
1
6
3
7
10
4
1
control
1
5
4
12
6
4
0
30 min post-meal
60 min post-meal
Preexercise
Postexercise
aNegative
values indicate a relative decrease in gut comfort from pretrial values.
Table 4 Palatability Scores (VAS) for Dairy and Control Meal Conditions Dairy x– ± SD
Control x– ± SD
Dairy—Control x– (95% CI)
T-test statistic; p-value
Visual
27 ± 27
34 ± 25
–7 (–17,3)
–1.461; 0.154
Smell
24 ± 20
30 ± 20
–6 (–14,1)
–1.740; 0.092
Taste
21 ± 22
25 ± 20
–4 (–12,3)
–1.205; 0.238
Aftertaste
53 ± 31
51 ± 26
2 (–10,13)
0.285; 0.777
Palatability
23 ± 20
25 ± 21
–2 (–10,5)
–0.630; 0.534
Note. The Visual Analog Scale (VAS) was scored so that Good was labeled the 0 point of the scale and Bad at the 100 point of the scale. A negative score (Dairy—Control) indicates a more favorable rating for the Dairy preexercise meal compared with Control.
of dairy foods and allow the consumption of key nutrients before exercise to meet new recommendations in sports nutrition. Our findings may alleviate concerns expressed by cyclists that consuming dairy in this way would cause gut discomfort leading to performance impairments, at least under the conditions of our study which allowed sufficient time for digestion (~90 min). Possible reasons for GI distress during cycling include ischemic factors that delay gastric emptying and mechanical factors such as an increased pressure gradient between the stomach and the esophagus which may be exacerbated by relaxation of the lower esophageal sphincter during high intensity exercise (Casey et al., 2005; de Oliveira & Burini, 2009). Our study, the first to investigate the effects of a dairy
preexercise meal on gut comfort and performance, suggests that this food source does not further increase the incidence of GI distress among cyclists. Further research involving runners and triathletes is warranted given the higher prevalence of GI distress in these sports (Pfeiffer et al., 2012). It is acknowledged that GI symptoms among athletes are variable and some are less likely to tolerate certain foods than others. A limitation of this study is that history of GI distress was not measured and this has been shown to have a strong correlation to GI symptoms reported during exercise trials (Pfeiffer et al., 2009). The Australian Dietary Guidelines (2013) recommend that females aged 18 to 50 years old consume 2.5 servings of dairy per day (one serving = 1 cup milk, 200
Effects of Dairy on Cycling Performance 557
g yogurt or 40 g cheese). These guidelines focus on bone health, where dairy foods are identified as a unique source of well-absorbed calcium. Low bone mineral density is prevalent in both male (Barry & Kohrt, 2008; Campion et al., 2010; Lombardi et al., 2012; Medelli et al., 2009; Nichols et al., 2003; Olmedillas et al., 2011; Rector et al., 2008) and female cyclists (Sherk et al., 2013), possibly owing to the absence of load-bearing exercise (Milgrom et al., 2000) and low energy availability (Barry & Kohrt, 2008; Loucks et al., 2011). A new hypothesis in sports nutrition involves the specific intake of calcium before strenuous exercise to counter sweat calcium loss and its disrupting effects on bone homeostasis, mediated via alterations in serum ionic calcium levels (Barry & Kohrt, 2008; Barry et al., 2011; Guillemant et al., 2004). There is evidence that supplemental calcium intake before/during cycling attenuates the increase in biomarkers of bone turnover seen in cyclists (Barry et al., 2011; Guillemant et al., 2004). A high calcium dairy-based preexercise meal may confer similar bone protective benefits while also meeting other nutritional guidelines. A further recent theme in sports nutrition is the recommendation that athletes consume an even spread of high quality protein (20 to 25 g of protein per eating occasion) sources every ~3 hr over the day to promote optimal muscle protein synthesis (Areta et al., 2013). The inclusion of several servings of dairy foods provides a simple and versatile solution to meeting new protein intake guidelines. Indeed, our dairy-rich meal provided ~36 g of protein (60 kg athlete), including a rich source of whey protein which is particularly valuable for muscle protein synthetic needs (Phillips & Zemel, 2011). Although the intake of dairy foods in a preexercise meal seems able to target these themes, we considered it important to establish that it was also compatible with other sports nutrition requirements and performance goals. Novelty Statement. Cyclists are observed to avoid dairy
before exercise for fear of gastrointestinal discomfort with potential implications for long-term bone health. This is the first study of preexercise dairy intake, gut comfort and performance in a representative sample of competitive female cyclists.
Practical Application Statement. Cyclists can
consume a dairy-based meal of oats, milk and yogurt containing ~1350 mg approximately 90 min before starting exercise without any significant effects to gut comfort or performance. This provides an opportunity to consume key nutrients (calcium and high biological value protein) in the total diet as well as specifically before exercise. Acknowledgments
The study was designed by ECH, LMB, MR and LEC; data were collected and analyzed by ECH, MR, LEC and AN; data
interpretation and manuscript preparation were undertaken by ECH, LMB, EJK, DGJ and DTM. All authors approved the final version of the paper. This study was funded by Dairy Australia.
References Areta, J.L., Burke, L.M., Ross, M.L., Camera, D.M., West, D.W.D., Broad, E.M., . . . Coffey, V.G. (2013). Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. The Journal of Physiology, 591(Pt 9), 2319–2331. PubMed Australian Dietary Guidelines. (2013). National Health and Medical Research Council. Retrieved from https://www. nhmrc.gov.au/guidelines/publications/n55 Barry, D.W., Hansen, K.C., van Pelt, R.E., Witten, M., Wolfe, P., & Kohrt, W.M. (2011). Acute calcium ingestion attenuates exercise-induced disruption of calcium homeostasis. Medicine and Science in Sports and Exercise, 43(4), 617–623. PubMed doi:10.1249/MSS.0b013e3181f79fa8 Barry, D.W., & Kohrt, W.M. (2008). BMD decreases over the course of a year in competitive male cyclists. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 23(4), 484–491. PubMed doi:10.1359/jbmr.071203 Campion, F., Nevill, A.M., Karlsson, M.K., Lounana, J., Shabani, M., Fardellone, P., & Medelli, J. (2010). Bone status in professional cyclists. International Journal of Sports Medicine, 31(7), 511–515. PubMed doi:10.1055/s-0029-1243616 Cao, J.J., Pasiakos, S.M., Margolis, L.M., Sauter, E.R., Whigham, L.D., McClung, J.P., . . . Combs, G.F. Jr. (2014). Calcium homeostasis and bone metabolic responses to high-protein diets during energy deficit in healthy young adults: a randomized control trial. The American Journal of Clinical Nutrition, 99(2), 400–407. PubMed doi:10.3945/ ajcn.113.073809 Casey, E., Mistry, D. J., & MacKnight, J. M. (2005). Training room management of medical conditions: sports gastroenterology. Clinics in Sports Medicine, 24(3), 525–540, viii. de Oliveira, E.P., & Burini, R.C. (2009). The impact of physical exercise on the gastrointestinal tract. Current Opinion in Clinical Nutrition and Metabolic Care, 12(5), 533–538. PubMed doi:10.1097/MCO.0b013e32832e6776 de Vrese, M., Stegelmann, A., Richter, B., Fenselau, S., Laue, C., & Schrezenmeir, J. (2001). Probiotics: compensation for lactase insufficiency. The American Journal of Clinical Nutrition, 73(2, Suppl) 421S–429S. PubMed Ebert, T.R., Martin, D.T., McDonald, W., Victor, J., Plummer, J., & Withers, R.T. (2005). Power output during women’s World Cup road cycle racing. European Journal of Applied Physiology, 95(5), 529–536. PubMed doi:10.1007/s00421005-0039-y Fischer, T.F.X., & Singer, A.J. (1999). Comparison of the Palatabilities of Standard and Superactivated Charcoal in Toxic Ingestions: A Randomized Trial.
558 Haakonssen et al.
cademic Emergency Medicine, 6(9), 895–899. PubMed A doi:10.1111/j.1553-2712.1999.tb01237.x Flint, A., Raben, A., Blundell, J.E., & Astrup, A. (2000). Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. International Journal Of Obesity And Related Metabolic Disorders: Journal Of The International Association For The Study Of Obesity, 24(1), 38–48. PubMed doi:10.1038/sj.ijo.0801083 Guillemant, J., Accarie, C., Peres, G., & Guillemant, S. (2004). Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcified Tissue International, 74(5), 407–414. PubMed doi:10.1007/s00223-003-0070-0 Haakonssen, E.C., Martin, D.T., Jenkins, D.G., & Burke, L.M. (2014).Race weight: Perceptions from elite female road cyclists. International Journal of Sports Physiology and Performance, Epub ahead of print.. Hopker, J., Myers, S., Jobson, S.A., Bruce, W., & Passfield, L. (2010). Validity and reliability of the Wattbike cycle ergometer. International Journal of Sports Medicine, 31(10), 731–736. PubMed doi:10.1055/s-0030-1261968 Jeacocke, N.A., & Burke, L.M. (2010). Methods to standardize dietary intake before performance testing. International Journal of Sport Nutrition and Exercise Metabolism, 20(2), 87–103. PubMed Lombardi, G., Lanteri, P., Graziani, R., Colombini, A., Banfi, G., & Corsetti, R. (2012). Bone and energy metabolism parameters in professional cyclists during the Giro d’Italia 3-weeks stage race. PLoS ONE, 7(7), e42077. PubMed doi:10.1371/journal.pone.0042077 Loucks, A.B., Kiens, B., & Wright, H.H. (2011). Energy availability in athletes. Journal of Sports Sciences, 29(Suppl 1), S7–S15. PubMed doi:10.1080/02640414.2011.588958 Medelli, J., Shabani, M., Lounana, J., Fardellone, P., & Campion, F. (2009). Low bone mineral density and calcium intake in elite cyclists. Journal of Sports, Medicine, and Physical Fitness, 49(1), 44–53. PubMed Milgrom, C., Finestone, A., Simkin, A., Ekenman, I., Mendelson, S., Millgram, M., . . . Burr, D. (2000). In vivo strain measurements to evaluate the strengthening potential of exercises on the tibial bone. The Journal of Bone and Joint Surgery. British Volume, 82(4), 591–594. PubMed doi:10.1302/0301-620X.82B4.9677
Nichols, J.F., Palmer, J.E., & Levy, S.S. (2003). Low bone mineral density in highly trained male master cyclists. Osteoporosis International, 14(8), 644–649. PubMed doi:10.1007/s00198-003-1418-z Olmedillas, H., González-Agüero, A., Moreno, L.A., Casajús, J.A., & Vicente-Rodríguez, G. (2011). Bone related health status in adolescent cyclists. PLoS ONE, 6(9), e24841. PubMed doi:10.1371/journal.pone.0024841 Pfeiffer, B., Coterill, A., Grathwohl, D., Stellingwerff, T., & Jeukendrup, A.E. (2009). The effect of carbohydrate gels on gastrointestinal tolerance during a 16-km run. International Journal of Sport Nutrition and Exercise Metabolism, 19(5), 485–503. PubMed Pfeiffer, B., Stellingwerff, T., Hodgson, A.B., Randell, R., Pöttgen, K., Res, P., & Jeukendrup, A.E. (2012). Nutritional intake and gastrointestinal problems during competitive endurance events. Medicine and Science in Sports and Exercise, 44(2), 344–351. PubMed doi:10.1249/ MSS.0b013e31822dc809 Phillips, S. M., & Zemel, M. B. (2011). Effect of protein, dairy components and energy balance in optimizing body composition. Nestlé Nutrition Institute Workshop Series, 69, 97–108. Ray, L. (2013). What Causes Gas Pain When Exercising? LIVESTRONG.COM. Retrieved from http://www. livestrong.com/article/433216-gas-pain-when-exercising/ Rector, R.S., Rogers, R., Ruebel, M., & Hinton, P.S. (2008). Participation in road cycling vs running is associated with lower bone mineral density in men. Metabolism: Clinical and Experimental, 57(2), 226–232 doi:10.1016/j. metabol.2007.09.005 Sherk, V.D., Barry, D.W., Villalon, K.L., Hansen, K.C., Wolfe, P., & Kohrt, W.M. (2013). Bone loss over 1 year of training and competition in female cyclists. Clinical Journal of Sports Medicine, 24(4):331–336. Wüthrich, B., Schmid, A., Walther, B., & Sieber, R. (2005). Milk consumption does not lead to mucus production or occurrence of asthma. Journal of the American College of Nutrition, 24(6 Suppl) 547S–555S. PubMed doi:10.1080/ 07315724.2005.10719503 Zemel, M.B. (2004). Role of calcium and dairy products in energy partitioning and weight management. The American Journal of Clinical Nutrition, 79(5), 907S–912S. PubMed
Copyright of International Journal of Sport Nutrition & Exercise Metabolism is the property of Human Kinetics Publishers, Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
www.IJSNEM-Journal.com RAPID COMMUNICATION
Dairy-Based Preexercise Meal Does Not Affect Gut Comfort or Time-Trial Performance in Female Cyclists Eric C. Haakonssen, Megan L. Ross, Louise E. Cato, Alisa Nana, and Emma J. Knight Australian Institute of Sport
David G. Jenkins University of Queensland
David T. Martin and Louise M. Burke Australian Institute of Sport Some athletes avoid dairy in the meal consumed before exercise due to fears about gastrointestinal discomfort. Regular exclusion of dairy foods may unnecessarily reduce intake of high quality proteins and calcium with possible implications for body composition and bone health. This study compared the effects of meals that included (Dairy) or excluded (Control) dairy foods on gastric comfort and subsequent cycling performance. Well-trained female cyclists (n = 32; mean ± SD; 24.3 ± 4.1 y; VO2peak 57.1 ± 4.9 ml/kg/min) completed two trials (randomized cross-over design) in which they consumed a meal (2 g/kg carbohydrate and 54 kJ/kg) 2 hr before a 90-min cycle session (80 min at 60% maximal aerobic power followed by a 10-min time trial; TT). The dairy meal contained 3 servings of dairy foods providing ~1350 mg calcium. Gut comfort and palatability were measured using questionnaires. Performance was measured as maximum mean power during the TT (MMP10min). There was no statistical or clinical evidence of an effect of meal type on MMP10min with a mean difference (Dairy – Control) of 4 W (95% CI [–2, 9]). There was no evidence of an association between pretrial gut comfort and meal type (p = .15) or between gut comfort delta scores and meal type postmeal (p = .31), preexercise (p = .17) or postexercise (p = .80). There was no statistical or clinical evidence of a difference in palatability between meal types. In summary, substantial amounts of dairy foods can be included in meals consumed before strenuous cycling without impairing either gut comfort or performance. Keywords: bone, calcium, cycling Endurance athletes may avoid dairy foods in meals consumed before high-intensity exercise due to fears about negative side-effects or to preferentially increase carbohydrate intake. Although the perception that dairy foods increase mucous production is disproved (Wüthrich et al., 2005), concerns persist that they may cause gasHaakonssen, Ross, Cato, Nana, and Burke are with the Dept. of Sports Nutrition, Knight the Dept. of Performance Research, and Martin the Dept. of Physiology, Australian Institute of Sport, Belconnen, Australia. Jenkins is with the Dept. of Human Movement Studies, University of Queensland, St. Lucia, Australia. Address author correspondence to Eric C. Haakonssen at [email protected].
trointestinal (GI) discomfort (de Vrese et al., 2001; Ray, 2013) thus impairing performance. Exclusion of dairy foods from preexercise meals may unnecessarily reduce an athlete’s total intake of proteins with high biological value and calcium which may favorably influence body composition (Phillips & Zemel, 2011; Zemel, 2004) and bone health (Cao et al., 2014). Recent investigations have shown that consuming calcium supplements before and during exercise may attenuate bone resorption by maintaining calcium homeostasis, which may be perturbed by sweat calcium losses (Barry et al., 2011; Guillemant et al., 2004). Dairy may present an option to increase preexercise calcium intake while meeting other sports nutrition goals. Before this is investigated it is important to ascertain how dairy affects gut comfort and performance.
553
554 Haakonssen et al.
The aim of this study was to investigate the effects of a dairy-based preexercise meal on GI comfort and subsequent exercise performance. A population of well-trained female cyclists was chosen due to our previous observations of their perceptions about dairy foods as well as their known problems with body composition management (Haakonssen et al., 2014) and bone health (Sherk et al., 2013). It was hypothesized that a dairy based preexercise meal would not significantly affect performance or gut comfort following intense cycling. This study was part of a larger investigation of bone turnover and calcium homeostasis in response to exercise.
Methods Subjects Thirty-two healthy, competitive female cyclists (mean ± SD; 24.3 ± 4.1 y, 60.9 ± 7.5 kg, 169.3 ± 7.0 cm, maximal aerobic power (MAP) 283 ± 28 W, peak oxygen consumption (V̇ O2peak) 57.1 ± 4.9 ml/kg/≥ min) were recruited from the 107 female cyclists registered with Australian National Road Series teams with an average (± SD) race attendance of 47 ± 16. Of these, 33 expressed interest in participating and 25 met inclusion criteria (17 to 32 years; 18-month racing experience). The remaining participants included an international professional, an ultra-endurance mountain biker and five well-trained national club-level cyclists. This study was approved by the human research ethics committee of the Australian Institute of Sport. Subjects were informed of testing protocols and risks of the study before providing written informed consent.
Baseline Fitness Test Maximal aerobic power (MAP) was determined using an incremental step test on a cycle ergometer (Lode Excalibur Sport, Groningen, Netherlands) starting at 125 W and increasing 25 W every 3 min until volitional fatigue. MAP was calculated as the highest mean power maintained for the last 3 min of the test.
Pretrial Diet Standardization For 24-hr before each experimental trial, subjects consumed a standardized prepackaged diet providing 5.0 g/ kg BM carbohydrate (CHO), 1.5 g/kg BM protein and 1.5 g/kg BM fat. The first 22 hr of the standard diet was supplied in the form of prepackaged meals, with the pretrial meal (accounting for the final 2 hr) provided to subjects in the laboratory. Individualized menus were prepared accounting for food preferences and intolerances using FoodWorks Professional Edition (v6.0, Xyris Software, Brisbane, Australia), as previously described (Jeacocke & Burke, 2010). In the case of gluten sensitivity (n = 2) and lactose-intolerance (n = 1), low lactose and gluten-free versions of foods matched for nutrient composition were used. Training was standardized for both pretrial days. Subjects refrained from alcohol consumption over the 24-hr period but followed (and replicated) usual prerace caffeine habits for the pretrial meal. Compliance to the diet, determined from a self-reported checklist, was noted by a dietitian on the morning of the trial.
Preexercise Meal Interventions This was a randomized, counterbalanced crossover design. The preexercise meals were scaled to provide 54 kJ/kg and 2 g/kg BM CHO. The dairy-rich meal (Dairy) consisted of rolled-oats cooked with calcium-fortified (Tricalcium phosphate, Nano-calcium) Anlene milk (Fonterra, Auckland, NZ), yogurt (Yoplait, BoulogneBillancourt, France) and additional milk while the Control meal provided oats cooked with water and served with canned fruit and nuts (see Table 1). Since the Dairy meal provided more protein and less fat than Control, the standardized meals were manipulated to match total protein and fat intake over the whole 24-hr period (see Table 2). The Dairy meal provided ~1350 mg of calcium and an equivalent of three servings of dairy foods. Meals were designed to look similar although cyclists were not blinded to the meal condition given the difficulty of concealing such a high dairy content.
Table 1 Example Preexercise Breakfast for Dairy and Control Trials for 60 kg Cyclist Dairy Uncle Toby’s quick oats
Control 57 g
Anlene milk
500 ml
Uncle Toby’s quick oats
65 g
water
250 ml
Yoplait yogurt vanilla
175 g
Goulburn Valley fruit salad diced
140 g
Brown sugar
13 g
brown sugar
23 g
Sultanas
20 g
sultana
23 g
macadamias
24 g
MeadowLea margarine sachet Just Juice, apple
15g 200 ml
Effects of Dairy on Cycling Performance 555
Table 2 Macronutrient Composition and Calcium Content of Standardized Diets for the Dairy and Control Trials Nutrient
24-hr Dietary Standardization Dairy (x– ± SD) Control (x– ± SD)
Preexercise Breakfast Dairy (x– ± SD) Control (x–± SD)
Energy(kJ·kg-1)
169 ± 4
170 ± 4
54 ± 2
54 ± 2
CHO (g·kg-1)
5.1 ± 0.2
5.1 ± 0.2
2.0 ± 0.0
2.0 ± 0.0
Protein (g·kg-1)
1.5 ± 0.0
1.5 ± 0.0
0.6 ± 0.1
0.2 ± 0.0
Fat (g·kg-1)
1.5 ± 0.0
1.5 ± 0.0
0.3 ± 0.0
0.4 ± 0.0
1658 ± 174
640 ± 226
1352 ± 53
46 ± 7
Calcium (mg)
Exercise Protocol Two hours after starting the pretrial breakfast, cyclists cycled on an ergometer (Watttbike Ltd. Nottingham, UK) at 60% MAP for 80 min (intensity based on race data from Ebert et al (2005)) followed by a 10 min time trial (TT) during which they were instructed to maintain the maximum mean power for the duration (MMP10min). The TT was limited to 10 min to avoid fatigue for the second trial. The two trial days started 48 hour apart to minimize changes in menstrual status. Cyclists were blinded to heart rate, power and cadence but were able to see time remaining. Water was consumed ad libitum during the first trial and this hydration strategy was replicated during the second trial. Cyclists consumed a carbohydrate gel (27 g; PowerBar PowerGel, Australia) at 30 and 65 min.
Questionnaires We developed a Likert questionnaire to check gastrointestinal comfort during the trial. Cyclists were asked at five time points (before pretrial meal, 30 min and 60 min after starting pretrial meal, immediately preexercise, and immediately postexercise) how comfortable does your stomach feel at the moment?, according to a five point scale (1 = very comfortable; 2 = comfortable; 3 = average comfort; 4 = uncomfortable; 5 = very uncomfortable). Cyclists were made aware that gut comfort is a different construct to hunger or satiety and that discomfort on this scale included symptoms such as nausea, bloating and gut pain. After consuming the pretrial meal, cyclists were asked to indicate how strongly they felt about five criteria relating to that meal (visual appeal, smell, taste, aftertaste, palatability) using a palatability questionnaire (Flint et al., 2000). Responses were recorded on 100 mm visual analog scales (VAS).
Data Analyses The effect of pretrial meal type on MMP10min was investigated using a linear mixed model with meal (Dairy or Control) as a fixed effect and subject as a random effect. Fisher’s exact test was used to assess the association between pretrial meal gut comfort and meal type.
Postmeal gut comfort responses were normalized to the pretrial response. A negative value implied a relative reduction in gut comfort from pretrial with the converse true for a positive value. Fisher’s exact tests were used to assess the association between pretrial meal type and the delta scores for each of the four postmeal time points. To examine the difference in VAS palatability scores between the two meal types, paired t tests were used for each of the palatability criteria. Statistical analyses were conducted using JMP Pro v10 (SAS Institute Inc., Cary, NC, USA).
Results The average MMP10min was 4 W higher for Dairy compared with Control (95% CI [–2, –9]). This is not a statistically significant difference (t31 = 1.35, p = .19) and it is not a clinically meaningful difference as it is less than the margin of reliability (~2%) of the Wattbike at these power outputs (Hopker et al., 2010). Fisher’s exact test showed no evidence of a statistically significant association between pretrial meal gut comfort (Table 3) and meal type (p = .15), and no evidence of a statistically significant association between gut comfort delta scores (Table 3) and meal type at 30 min (p = .31) or 60 min postmeal (p = .17); immediately preexercise (p = .80) or immediately postexercise (p = .77). The estimated differences in mean VAS palatability suggest that for all criteria except for aftertaste, the dairy meal may have been slightly more palatable (Table 4). However, the differences were not statistically significant or clinically meaningful based on a minimal clinically significant difference of 20 mm (Fischer & Singer, 1999).
Discussion In contrast to the beliefs of some athletes, we found that consuming substantial amounts of dairy foods in a meal consumed ~90 min before prolonged strenuous stationary cycling neither impaired nor enhanced gut comfort or performance compared with a control breakfast that excluded dairy foods. Consuming dairy foods during the preexercise breakfast should assist in increasing total daily intake
556 Haakonssen et al.
Table 3 Frequency Distribution of Gut Comfort Scores Across Time Points for Dairy and Control Meal Conditions Pre-Trial
1
2
3
4
5
Dairy
15
8
6
1
2
Control
9
16
5
2
0
Change Scoresa –4
–3
–2
–1
0
1
2
dairy
1
2
7
8
10
3
1
control
0
0
4
7
14
7
0
dairy
0
0
5
10
13
3
1
control
0
1
2
5
14
9
1
dairy
0
0
4
13
9
4
2
control
1
1
4
11
10
5
0
dairy
1
6
3
7
10
4
1
control
1
5
4
12
6
4
0
30 min post-meal
60 min post-meal
Preexercise
Postexercise
aNegative
values indicate a relative decrease in gut comfort from pretrial values.
Table 4 Palatability Scores (VAS) for Dairy and Control Meal Conditions Dairy x– ± SD
Control x– ± SD
Dairy—Control x– (95% CI)
T-test statistic; p-value
Visual
27 ± 27
34 ± 25
–7 (–17,3)
–1.461; 0.154
Smell
24 ± 20
30 ± 20
–6 (–14,1)
–1.740; 0.092
Taste
21 ± 22
25 ± 20
–4 (–12,3)
–1.205; 0.238
Aftertaste
53 ± 31
51 ± 26
2 (–10,13)
0.285; 0.777
Palatability
23 ± 20
25 ± 21
–2 (–10,5)
–0.630; 0.534
Note. The Visual Analog Scale (VAS) was scored so that Good was labeled the 0 point of the scale and Bad at the 100 point of the scale. A negative score (Dairy—Control) indicates a more favorable rating for the Dairy preexercise meal compared with Control.
of dairy foods and allow the consumption of key nutrients before exercise to meet new recommendations in sports nutrition. Our findings may alleviate concerns expressed by cyclists that consuming dairy in this way would cause gut discomfort leading to performance impairments, at least under the conditions of our study which allowed sufficient time for digestion (~90 min). Possible reasons for GI distress during cycling include ischemic factors that delay gastric emptying and mechanical factors such as an increased pressure gradient between the stomach and the esophagus which may be exacerbated by relaxation of the lower esophageal sphincter during high intensity exercise (Casey et al., 2005; de Oliveira & Burini, 2009). Our study, the first to investigate the effects of a dairy
preexercise meal on gut comfort and performance, suggests that this food source does not further increase the incidence of GI distress among cyclists. Further research involving runners and triathletes is warranted given the higher prevalence of GI distress in these sports (Pfeiffer et al., 2012). It is acknowledged that GI symptoms among athletes are variable and some are less likely to tolerate certain foods than others. A limitation of this study is that history of GI distress was not measured and this has been shown to have a strong correlation to GI symptoms reported during exercise trials (Pfeiffer et al., 2009). The Australian Dietary Guidelines (2013) recommend that females aged 18 to 50 years old consume 2.5 servings of dairy per day (one serving = 1 cup milk, 200
Effects of Dairy on Cycling Performance 557
g yogurt or 40 g cheese). These guidelines focus on bone health, where dairy foods are identified as a unique source of well-absorbed calcium. Low bone mineral density is prevalent in both male (Barry & Kohrt, 2008; Campion et al., 2010; Lombardi et al., 2012; Medelli et al., 2009; Nichols et al., 2003; Olmedillas et al., 2011; Rector et al., 2008) and female cyclists (Sherk et al., 2013), possibly owing to the absence of load-bearing exercise (Milgrom et al., 2000) and low energy availability (Barry & Kohrt, 2008; Loucks et al., 2011). A new hypothesis in sports nutrition involves the specific intake of calcium before strenuous exercise to counter sweat calcium loss and its disrupting effects on bone homeostasis, mediated via alterations in serum ionic calcium levels (Barry & Kohrt, 2008; Barry et al., 2011; Guillemant et al., 2004). There is evidence that supplemental calcium intake before/during cycling attenuates the increase in biomarkers of bone turnover seen in cyclists (Barry et al., 2011; Guillemant et al., 2004). A high calcium dairy-based preexercise meal may confer similar bone protective benefits while also meeting other nutritional guidelines. A further recent theme in sports nutrition is the recommendation that athletes consume an even spread of high quality protein (20 to 25 g of protein per eating occasion) sources every ~3 hr over the day to promote optimal muscle protein synthesis (Areta et al., 2013). The inclusion of several servings of dairy foods provides a simple and versatile solution to meeting new protein intake guidelines. Indeed, our dairy-rich meal provided ~36 g of protein (60 kg athlete), including a rich source of whey protein which is particularly valuable for muscle protein synthetic needs (Phillips & Zemel, 2011). Although the intake of dairy foods in a preexercise meal seems able to target these themes, we considered it important to establish that it was also compatible with other sports nutrition requirements and performance goals. Novelty Statement. Cyclists are observed to avoid dairy
before exercise for fear of gastrointestinal discomfort with potential implications for long-term bone health. This is the first study of preexercise dairy intake, gut comfort and performance in a representative sample of competitive female cyclists.
Practical Application Statement. Cyclists can
consume a dairy-based meal of oats, milk and yogurt containing ~1350 mg approximately 90 min before starting exercise without any significant effects to gut comfort or performance. This provides an opportunity to consume key nutrients (calcium and high biological value protein) in the total diet as well as specifically before exercise. Acknowledgments
The study was designed by ECH, LMB, MR and LEC; data were collected and analyzed by ECH, MR, LEC and AN; data
interpretation and manuscript preparation were undertaken by ECH, LMB, EJK, DGJ and DTM. All authors approved the final version of the paper. This study was funded by Dairy Australia.
References Areta, J.L., Burke, L.M., Ross, M.L., Camera, D.M., West, D.W.D., Broad, E.M., . . . Coffey, V.G. (2013). Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. The Journal of Physiology, 591(Pt 9), 2319–2331. PubMed Australian Dietary Guidelines. (2013). National Health and Medical Research Council. Retrieved from https://www. nhmrc.gov.au/guidelines/publications/n55 Barry, D.W., Hansen, K.C., van Pelt, R.E., Witten, M., Wolfe, P., & Kohrt, W.M. (2011). Acute calcium ingestion attenuates exercise-induced disruption of calcium homeostasis. Medicine and Science in Sports and Exercise, 43(4), 617–623. PubMed doi:10.1249/MSS.0b013e3181f79fa8 Barry, D.W., & Kohrt, W.M. (2008). BMD decreases over the course of a year in competitive male cyclists. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research, 23(4), 484–491. PubMed doi:10.1359/jbmr.071203 Campion, F., Nevill, A.M., Karlsson, M.K., Lounana, J., Shabani, M., Fardellone, P., & Medelli, J. (2010). Bone status in professional cyclists. International Journal of Sports Medicine, 31(7), 511–515. PubMed doi:10.1055/s-0029-1243616 Cao, J.J., Pasiakos, S.M., Margolis, L.M., Sauter, E.R., Whigham, L.D., McClung, J.P., . . . Combs, G.F. Jr. (2014). Calcium homeostasis and bone metabolic responses to high-protein diets during energy deficit in healthy young adults: a randomized control trial. The American Journal of Clinical Nutrition, 99(2), 400–407. PubMed doi:10.3945/ ajcn.113.073809 Casey, E., Mistry, D. J., & MacKnight, J. M. (2005). Training room management of medical conditions: sports gastroenterology. Clinics in Sports Medicine, 24(3), 525–540, viii. de Oliveira, E.P., & Burini, R.C. (2009). The impact of physical exercise on the gastrointestinal tract. Current Opinion in Clinical Nutrition and Metabolic Care, 12(5), 533–538. PubMed doi:10.1097/MCO.0b013e32832e6776 de Vrese, M., Stegelmann, A., Richter, B., Fenselau, S., Laue, C., & Schrezenmeir, J. (2001). Probiotics: compensation for lactase insufficiency. The American Journal of Clinical Nutrition, 73(2, Suppl) 421S–429S. PubMed Ebert, T.R., Martin, D.T., McDonald, W., Victor, J., Plummer, J., & Withers, R.T. (2005). Power output during women’s World Cup road cycle racing. European Journal of Applied Physiology, 95(5), 529–536. PubMed doi:10.1007/s00421005-0039-y Fischer, T.F.X., & Singer, A.J. (1999). Comparison of the Palatabilities of Standard and Superactivated Charcoal in Toxic Ingestions: A Randomized Trial.
558 Haakonssen et al.
cademic Emergency Medicine, 6(9), 895–899. PubMed A doi:10.1111/j.1553-2712.1999.tb01237.x Flint, A., Raben, A., Blundell, J.E., & Astrup, A. (2000). Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. International Journal Of Obesity And Related Metabolic Disorders: Journal Of The International Association For The Study Of Obesity, 24(1), 38–48. PubMed doi:10.1038/sj.ijo.0801083 Guillemant, J., Accarie, C., Peres, G., & Guillemant, S. (2004). Acute effects of an oral calcium load on markers of bone metabolism during endurance cycling exercise in male athletes. Calcified Tissue International, 74(5), 407–414. PubMed doi:10.1007/s00223-003-0070-0 Haakonssen, E.C., Martin, D.T., Jenkins, D.G., & Burke, L.M. (2014).Race weight: Perceptions from elite female road cyclists. International Journal of Sports Physiology and Performance, Epub ahead of print.. Hopker, J., Myers, S., Jobson, S.A., Bruce, W., & Passfield, L. (2010). Validity and reliability of the Wattbike cycle ergometer. International Journal of Sports Medicine, 31(10), 731–736. PubMed doi:10.1055/s-0030-1261968 Jeacocke, N.A., & Burke, L.M. (2010). Methods to standardize dietary intake before performance testing. International Journal of Sport Nutrition and Exercise Metabolism, 20(2), 87–103. PubMed Lombardi, G., Lanteri, P., Graziani, R., Colombini, A., Banfi, G., & Corsetti, R. (2012). Bone and energy metabolism parameters in professional cyclists during the Giro d’Italia 3-weeks stage race. PLoS ONE, 7(7), e42077. PubMed doi:10.1371/journal.pone.0042077 Loucks, A.B., Kiens, B., & Wright, H.H. (2011). Energy availability in athletes. Journal of Sports Sciences, 29(Suppl 1), S7–S15. PubMed doi:10.1080/02640414.2011.588958 Medelli, J., Shabani, M., Lounana, J., Fardellone, P., & Campion, F. (2009). Low bone mineral density and calcium intake in elite cyclists. Journal of Sports, Medicine, and Physical Fitness, 49(1), 44–53. PubMed Milgrom, C., Finestone, A., Simkin, A., Ekenman, I., Mendelson, S., Millgram, M., . . . Burr, D. (2000). In vivo strain measurements to evaluate the strengthening potential of exercises on the tibial bone. The Journal of Bone and Joint Surgery. British Volume, 82(4), 591–594. PubMed doi:10.1302/0301-620X.82B4.9677
Nichols, J.F., Palmer, J.E., & Levy, S.S. (2003). Low bone mineral density in highly trained male master cyclists. Osteoporosis International, 14(8), 644–649. PubMed doi:10.1007/s00198-003-1418-z Olmedillas, H., González-Agüero, A., Moreno, L.A., Casajús, J.A., & Vicente-Rodríguez, G. (2011). Bone related health status in adolescent cyclists. PLoS ONE, 6(9), e24841. PubMed doi:10.1371/journal.pone.0024841 Pfeiffer, B., Coterill, A., Grathwohl, D., Stellingwerff, T., & Jeukendrup, A.E. (2009). The effect of carbohydrate gels on gastrointestinal tolerance during a 16-km run. International Journal of Sport Nutrition and Exercise Metabolism, 19(5), 485–503. PubMed Pfeiffer, B., Stellingwerff, T., Hodgson, A.B., Randell, R., Pöttgen, K., Res, P., & Jeukendrup, A.E. (2012). Nutritional intake and gastrointestinal problems during competitive endurance events. Medicine and Science in Sports and Exercise, 44(2), 344–351. PubMed doi:10.1249/ MSS.0b013e31822dc809 Phillips, S. M., & Zemel, M. B. (2011). Effect of protein, dairy components and energy balance in optimizing body composition. Nestlé Nutrition Institute Workshop Series, 69, 97–108. Ray, L. (2013). What Causes Gas Pain When Exercising? LIVESTRONG.COM. Retrieved from http://www. livestrong.com/article/433216-gas-pain-when-exercising/ Rector, R.S., Rogers, R., Ruebel, M., & Hinton, P.S. (2008). Participation in road cycling vs running is associated with lower bone mineral density in men. Metabolism: Clinical and Experimental, 57(2), 226–232 doi:10.1016/j. metabol.2007.09.005 Sherk, V.D., Barry, D.W., Villalon, K.L., Hansen, K.C., Wolfe, P., & Kohrt, W.M. (2013). Bone loss over 1 year of training and competition in female cyclists. Clinical Journal of Sports Medicine, 24(4):331–336. Wüthrich, B., Schmid, A., Walther, B., & Sieber, R. (2005). Milk consumption does not lead to mucus production or occurrence of asthma. Journal of the American College of Nutrition, 24(6 Suppl) 547S–555S. PubMed doi:10.1080/ 07315724.2005.10719503 Zemel, M.B. (2004). Role of calcium and dairy products in energy partitioning and weight management. The American Journal of Clinical Nutrition, 79(5), 907S–912S. PubMed
Copyright of International Journal of Sport Nutrition & Exercise Metabolism is the property of Human Kinetics Publishers, Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
