Low versus high carbohydrates in the diet of the world‐class athlete: insights from McArdle's disease

Burke et al. have elegantly shown in world‐class race walkers undergoing a 3 week period of intense training that, compared with a diet providing high carbohydrate (CHO) availability (8.6 g kg⁻¹ day⁻¹), a low CHO diet (< 1.0 g kg⁻¹ day⁻¹) impaired performance, in part due to worsened exercise economy (Burke et al. 2017). Their study adds valuable information to the field of sports nutrition given the ongoing debate (also in the mass media) about which dietary pattern is more suitable for endurance athletes. Recent alternatives to the ‘classic’ high CHO approach, such as diets with periodic or chronic low CHO availability, are receiving growing attention.

No universal recommendation can be given to athletes regarding dietary CHO content. Personalised nutrition appears to be the wiser approach. Yet it should always be considered that any diet resulting in very low glycogen levels is likely not only to preclude achievement of top‐level endurance sports performance, but also to impair the ability to perform intense endurance exercise in general. This phenomenon is best illustrated by the results of research conducted with elite athletes, such as the valuable study by Burke and coworkers, as well as by studies on patients with McArdle's disease (glycogenosis type V). This rare, often ignored disorder can provide mechanistic insight into the importance of muscle glycogen for intense endurance exercise performance.

McArdle's disease is a pure myopathy caused by inherited deficiency of the skeletal‐muscle isoform of glycogen phosphorylase, ‘myophosphorylase’, encoded by the PYGM gene. Because this enzyme catalyses the breakdown of glycogen into glucose 1‐phosphate in muscle fibres, patients are unable to obtain energy from their muscle glycogen stores, with the remaining body tissues retaining normal metabolic function (Santalla et al. 2014). McArdle's disease therefore represents an excellent model with which to study the biological consequences of exercising with unavailability of muscle glycogen, and is arguably the paradigm of exercise intolerance, typically consisting of acute ‘crises’ of fatigue and muscle stiffness and contractures upon the start of endurance exercise such as brisk walking. Such crises are frequently accompanied by marked muscle damage or rhabdomyolysis (see below for the potential implications of the latter phenomenon) (Santalla et al. 2014).

The poor aerobic capacity of McArdle's patients (e.g. mean peak oxygen consumption (${\dot{V}}_{{\mathrm{O}}_2\mathrm{peak}}$) in Spanish patients = 18.2 ± 6.5 ml kg⁻¹ min⁻¹ (range 5.9, 37.8)) and the intolerance to endurance sports in virtually all of them (Lucia et al. 2012) is consistent with the classic findings reported by Scandinavian scientists 50 years ago that decreasing pre‐exercise muscle glycogen reserves by dietary and/or exercise manipulation severely decreases tolerance to fatigue during endurance exercise (Bergstrom et al. 1967). Observations in McArdle's patients are also consistent with the vital role that glycogen‐derived ATP plays in key muscle functions whose failure might accelerate onset of fatigue. One such function is Ca²⁺ handling by the sarcoplasmic reticulum (Ortenblad et al. 2013), which is affected both in patients (Nogales‐Gadea et al. 2012) and in the genetically manipulated mouse model of McArdle's disease that we recently generated (harbouring the commonest Pygm genotype causing the disorder among Caucasians, p.R50X/p.R50X; Fiuza‐Luces et al. 2016). Further, the endurance capacity of p.R50X/p.R50X mice is much lower (∼48%) than that of healthy (wild‐type (wt)/wt) mice and, although in mice heterozygous for the p.R50X mutation (p.R50X/wt) the ability to utilise glycogen is not totally blocked (∼50% of normal), their endurance capacity remains considerably reduced (by ∼18%) when compared with their wt/wt peers (Brull et al. 2015).

A main consequence of the low CHO diet in the study by Burke et al. was impaired walking economy (Burke et al. 2017). In this regard, the oxygen consumed by the muscles of McArdle's patients is not converted into the expected power production, as shown by the very low gross mechanical efficiency values of these individuals during submaximal bicycling, i.e. 13% vs 19% in their age/gender‐matched healthy controls (Mate‐Munoz et al. 2007). The main reasons for this phenomenon are likely to be excessive muscle recruitment and increased dependence on fat metabolism owing to the inherited block in muscle glycogen metabolism since CHO is a more efficient fuel than fat in terms of generating ATP per mole of oxygen (Santalla et al. 2014).

Another consequence of blocked glycogenolysis, with potential clinical implications, is muscle damage, especially after hard exertion (sometimes leading to rhabdomyolysis), as reflected by high levels of intramyocellular proteins (e.g. creatine kinase [CK]) in the blood of McArdle's patients (their CK levels are usually >1000 U l⁻¹, well above the normal upper limit; 200 U l⁻¹; Lucia et al. 2012). Although mechanistic explanations that fully account for this phenomenon remain elusive, one reason might be down‐regulation of Na⁺–K⁺ pumps in patients’ muscles (Haller et al. 1998), which are fuelled by glycogenolysis‐dependent ATP and are responsible for maintaining cellular volume and integrity (Santalla et al. 2014). Interestingly, muscle damage might further impair the efficiency of muscle contractions (Warren et al. 1996), as reflected by impaired running economy (Calbet et al. 2001).

It would have been interesting to assess the effects of the different diets on muscle damage markers in the study by Burke et al. Further research might determine whether low CHO diets can increase muscle damage (and subsequent risk for rhabdomyolysis), especially during a demanding endurance training approach that is gaining adepts among Westerners (partly for its advocated health benefits while taking up little time), the so‐called high intense interval training (‘HIIT’).

Additional information

Competing interests

None declared

Funding

Research on McArdle disease and related disordes by the authors is funded by from Fondo de Investigaciones Sanitarias and Fondos Feder: A.L.M., PI15/00558; G.N.G, PI15/01756 and CP14/00032.