Marathon Running Increases Synthesis and Decreases Catabolism of Joint Cartilage Type II Collagen Accompanied by High-Energy Demands and an Inflamatory Reaction.

José A Hernández-Hermoso,Lexa Nescolarde,Elena Revuelta-López,Jordi Ara,Emma Roca,Antoni Bayes-Genis

doi:10.3389/fphys.2021.722718

Abstract

Objective: To determine the effect of marathon running on serum levels of inflammatory, high energy, and cartilage matrix biomarkers and to ascertain whether these biomarkers levels correlate.Design: Blood samples from 17 Caucasian male recreational athletes at the Barcelona Marathon 2017 were collected at the baseline, immediately and 48 h post-race. Serum C reactive protein (CRP), creatin kinase (CK), and lactate dehydrogenase (LDH) were determined using an AU-5800 chemistry analyser. Serum levels of hyaluronan (HA), cartilage oligomeric matrix protein (COMP), aggrecan chondroitin sulphate 846 (CS846), glycoprotein YKL-40, human procollagen II N-terminal propeptide (PIINP), human type IIA collagen N-propeptide (PIIANP), and collagen type II cleavage (C2C) were measured by sandwich enzyme-linked immune-sorbent assay (ELISA).Results: Medians CK and sLDH levels increased (three-fold, two-fold) post-race [429 (332) U/L, 323 (69) U/L] (p < 0.0001; p < 0.0001) and (six-fold, 1.2-fold) 48 h post-race [658 (1,073) U/L, 218 (45) U/L] (p < 0.0001; p < 0.0001). Medians CRP increased (ten-fold) after 48 h post-race [6.8 (4.1) mg/L] (p < 0.0001). Mean sHA levels increased (four-fold) post-race (89.54 ± 53.14 ng/ml) (p < 0.0001). Means PIINP (9.05 ± 2.15 ng/ml) levels increased post-race (10.82 ± 3.44 ng/ml) (p = 0.053) and 48 h post-race (11.00 ± 2.96 ng/ml) (p = 0.001). Mean sC2C levels (220.83 ± 39.50 ng/ml) decreased post-race (188.67 ± 38.52 ng/ml) (p = 0.002). In contrast, means COMP, sCS846, sPIIANP, and median sYKL-40 were relatively stable. We found a positive association between sCK levels with sLDH pre-race (r = 0.758, p < 0.0001), post-race (r = 0.623, p = 0.008) and 48-h post-race (r = 0.842, p < 0.0001); sHA with sCRP post-race vs. 48 h post-race (r = 0.563, p = 0.019) and sPIINP with sCK pre-race vs. 48-h post-race (r = 0.499, p = 0.044) and with sLDH 48-h pre-race vs. post-race (r = 0.610, p = 0.009) and a negative correlation of sPIIANP with sCRP 48-h post-race (r = −0.570, p = 0.017).Conclusion: Marathon running is an exercise with high-energy demands (sCK and sLDH increase) that provokes a high and durable general inflammatory reaction (sCRP increase) and an immediately post-marathon mechanism to protect inflammation and cartilage (sHA increase). Accompanied by an increase in type II collagen cartilage fibrils synthesis (sPIINP increase) and a decrease in its catabolism (sC2C decrease), without changes in non-collagenous cartilage metabolism (sCOMP, sC846, and sYKL-40). Metabolic changes on sPIINP and sHA synthesis may be related to energy consumption (sCK, sLDH) and the inflammatory reaction (sCRP) produced.

Highlights

Pre-race median sCK and sLDH levels increased immediately post-race, up to three-fold and two-fold increase, respectively (p < 0.0001) [10 (59%) runners over three-fold and 12 (71%) over two-fold, respectively]
The median sCRP increased up to ten-fold 48 h post-race compared to pre-race (p < 0.0001) [6 (35%) runners over tenfold] and immediately post (p < 0.0001)
We found an increase in high-energy consumption and, in general, inflammatory reaction during 48 h correlated with collagen synthesis and an immediate post-marathon cartilage inflammatory and degradation protection mechanism

Summary

Introduction

Despite the substantial increase in marathon runners, still, it is not known what is a physiological or expected acute inflammatory or cartilage metabolic response to an increase in physical activity (Cattano et al, 2017b; Driban et al, 2017).Long-distance running imposes high levels of stress on the musculoskeletal system, causing changes in cartilage volume (Boocock et al, 2009; Doré et al, 2013) and numerous cellular and molecular changes (Cattano et al, 2017b). Blood-circulating biomarkers used to monitor inflammation and joint homeostasis change after joint loading with different types of activity level or sports, and offer a method to analyse cartilage metabolic response to physical activity, data available give contrasting results (Cattano et al, 2017b) The discrepancy of these results may be attributable to differences in the study methods and to many confounding factors such as ethnicity (Jordan et al, 2003), gender (Jordan et al, 2003; Niehoff et al, 2010), body weight (Matt Denning et al, 2015), activity time or level (Cattano et al, 2017a), loading protocols (Niehoff et al, 2010), vibration (Cattano et al, 2017b), food intake (Gordon et al, 2008), diurnal variation (Andersson et al, 2006), and osteoarthritis (Chu et al, 2018); further, biomarkers may adapt to training over time (Cattano et al, 2017b). The correlation between inflammatory, energy enzymes, and collagenous and noncollagenous cartilage markers after a marathon run is unknown

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Discussion

Conclusion