A Short-Term Ketogenic Diet Impairs Markers of Bone Health in Response to Exercise

Abstract

Objectives: To investigate diet-exercise interactions related to bone markers in elite endurance athletes after a 3.5-week ketogenic low-carbohydrate, high-fat (LCHF) diet and subsequent restoration of carbohydrate (CHO) feeding. Methods: World-class race walkers (25 male, 5 female) completed 3.5-weeks of energy-matched (220 kJ·kg·d-1) high CHO (HCHO; 8.6 g·kg·d-1 CHO, 2.1 g·kg·d-1 protein, 1.2 g·kg·d-1 fat) or LCHF (0.5 g·kg·d-1 CHO, 2.1 g·kg·d-1 protein, 75-80% of energy from fat) diet followed by acute CHO restoration. Serum markers of bone breakdown (cross-linked C-terminal telopeptide of type I collagen, CTX), formation (procollagen 1 N-terminal propeptide, P1NP) and metabolism (osteocalcin, OC) were assessed at rest (fasting and 2 h post meal) and after exercise (0 and 3 h) at Baseline, after the 3.5-week intervention (Adaptation) and after acute CHO feeding (Restoration). Results: After Adaptation, LCHF increased fasting CTX concentrations above Baseline (p = 0.007, Cohen's d = 0.69), while P1NP (p < 0.001, d = 0.99) and OC (p < 0.001, d = 1.39) levels decreased. Post-exercise, LCHF increased CTX concentrations above Baseline (p = 0.001, d = 1.67) and above HCHO (p < 0.001, d = 0.62), while P1NP (p < 0.001, d = 0.85) and OC concentrations decreased (p < 0.001, d = 0.99) during exercise. Exercise-related area under curve (AUC) for CTX was increased by LCHF after Adaptation (p = 0.001, d = 1.52), with decreases in P1NP (p < 0.001, d = 1.27) and OC (p < 0.001, d = 2.0). CHO restoration recovered post-exercise CTX and CTX exercise-related AUC, while concentrations and exercise-related AUC for P1NP and OC remained suppressed for LCHF (p = 1.000 compared to Adaptation). Conclusion: Markers of bone modeling/remodeling were impaired after short-term LCHF diet, and only a marker of resorption recovered after acute CHO restoration. Long-term studies of the effects of LCHF on bone health are warranted.

Keywords: bone health; endurance athletes; exercise; ketogenic diet; nutrition.

Copyright © 2020 Heikura, Burke, Hawley, Ross, Garvican-Lewis, Sharma, McKay, Leckey, Welvaert, McCall and Ackerman.

Figures

Figure 1

Study flowchart and overview. Thirty-two data sets were gathered from 30 participants who participated in one or more training camps. After Baseline testing on a carbohydrate-rich (HCHO) diet, they elected to follow a 3.5-week energy-matched dietary intervention of either HCHO or ketogenic low carbohydrate-high fat (LCHF) principles. After Adaptation, the participants underwent an acute period of Restoration of high carbohydrate availability. At Baseline and at the end (Adaptation) of this intervention, as well as after acute carbohydrate reintroduction (Restoration) they undertook a test block including a 25 km (2 h) hybrid laboratory/field race walking protocol at ~75% VO2 max. Venous blood samples were collected after an overnight fast, 2 h after an energy-matched breakfast based on their diet (immediately pre-exercise), immediately post exercise and after 3 h of passive recovery during which an intervention-matched recovery shake was consumed at 30 min. Blood samples were analyzed for serum concentrations of C-terminal telopeptide of type I collagen (CTX), procollagen 1 N-terminal propeptide (P1NP), and osteocalcin (OC).

Figure 2

Percentage change in fasting serum C-terminal telopeptide of type I collagen (CTX), procollagen 1 N-terminal propeptide (P1NP) and osteocalcin (OC) for high carbohydrate (HCHO; solid bars) and low CHO high fat (LCHF; striped bars) after the 3.5-week dietary intervention. Data are means ± standard deviations. ***p < 0.001 Significant between-group difference; ##p < 0.01; ###p < 0.001 Significant change from Baseline within-group.

Figure 3

Time course of changes in bone marker concentrations across exercise (left panel) and exercise area under curve (right panel) for serum C-terminal telopeptide of type I collagen (CTX) (A,D), procollagen 1 N-terminal propeptide (P1NP) (B,E), and osteocalcin (OC) (C,F) after the 3.5-week dietary intervention. Black bars/symbols represent Baseline, gray bars/symbols represent Adaptation. Squares and circles represent high carbohydrate (HCHO) and low carbohydrate high fat (LCHF), respectively. Gray bars represent a hybrid laboratory/field 19–25 km walk test at ~75% VO2 max. Data are means ± standard deviations. ##p < 0.01; ###p < 0.001 denotes significant differences at time points or tests within diet groups. *p < 0.05; **p < 0.01; ***p < 0.001 denotes significant differences between diet groups at a specific time point.

Figure 4

Time course of changes in bone marker concentrations across exercise (left panel) and exercise area under curve (right panel) for serum C-terminal telopeptide of type I collagen (CTX) (A,D), procollagen 1 N-terminal propeptide (P1NP) (B,E), and osteocalcin (OC) (C,F) after acute reintroduction of carbohydrate (right panel). Gray bars/symbols represent Adaptation, and white bars/symbols represent Restoration. Squares and circles represent high carbohydrate (HCHO) and low carbohydrate high fat (LCHF), respectively. Gray bars represent a hybrid laboratory/field 19–25 km walk test at ~75% VO2 max. Data are means ± standard deviations. $$p < 0.01; $$$p > 0.001 denotes significant within-group difference compared to Restoration. *p < 0.05; **p < 0.01; ***p < 0.001 denotes significant differences between diet groups at a specific time point.