The effects of resistance exercise and hydrolysed collagen supplementation on changes in collagen synthesis and muscle-tendon properties in middle-aged athletes

Nulty, C (2025) The effects of resistance exercise and hydrolysed collagen supplementation on changes in collagen synthesis and muscle-tendon properties in middle-aged athletes. Doctoral thesis, Liverpool John Moores University.

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Abstract

Tendon comprises approximately 70 % type I collagen and is responsible for force transmission from muscle to bone, thus its efficiency is crucial for rapid force production. Human tendons, such as the Achilles and patellar tendons, are mechanosensitive to exercise conferring a high level of mechanical strain, such as resistance exercise (RE), which stimulates type I collagen synthesis. When repeated, chronic RE, i.e. resistance training (RT), leads to an increase in both the cross-sectional area (CSA) and stiffness of the tendon, however, the magnitude of change is often lower in both female and older populations compared to young males.
Considering the high collagen content of tendon, dietary supplementation with collagen has been suggested as a strategy to augment training adaptation. It has very recently been shown that RE with supplementation of 30 g, but not 15 g, hydrolysed collagen (HC) acutely increases whole body type I collagen synthesis in young, resistance trained men to a greater extent than RE alone. Similar benefits were observed following RE with 30 g HC ingestion in a young, female athlete. However, the positive effect was diminished when circulating oestrogen was high compared to when it was low, thus suggesting collagen synthesis varies according to menstrual cycle phase. Furthermore, recent studies have shown that RT and HC supplementation promote greater tendon adaptations (e.g. augmented CSA and stiffness) compared to RT alone. However, all these studies have been performed in young adults, and it remains to be seen if similar benefits can be seen in older individuals, who tend to demonstrate diminished anabolic responses to protein ingestion. Furthermore, studies investigating the effect of ageing on muscle-tendon health and function focus on the extremes of the adult age spectrum, i.e. neglecting middle-aged individuals. This means that exercise and nutrition guidance for optimal tendon health in this population is lacking. Therefore, the overall aim of this thesis was to investigate the effects of RE with HC ingestion on markers of collagen turnover, and to examine the effect of HC supplementation on muscle-tendon adaptations to chronic RT in middle-aged men and women.
In order to ascertain whether HC supplementation is required in middle-aged individuals, and if a potential requirement is sex-dependent, we first needed to determine the collagen composition of habitual diets in adults of different ages. Aside from one recent study on the American adult population (with substantial methodological flaws), collagen intake at population level is yet to be described. Chapter Three comprehensively estimated habitual collagen intake among Irish adults using data from the National Adult Nutrition Survey (NANS), the most recent population-level data for Ireland, analysing 4-day semi-weighed food diaries from 1500 adults. The collagen mean daily intake for the entire sample was 3.2 ± 2.0 g∙day-1, representing just 3.6 ± 1.9 % of total protein intake. These findings suggest that, if collagen intake is beneficial for musculoskeletal health, sufficient quantities are difficult to obtain through habitual diet alone, and thus supplementation is likely warranted, especially in ageing and female populations, who had the lowest intakes.
The first lab-based experimental study of this thesis (Chapter Four) used a double-blind, randomised crossover design to determine the optimal dose of HC for maximising whole-body collagen synthesis in eight middle-aged, resistance trained men. Venous blood samples were analysed for respective markers of collagen synthesis and degradation, the N-terminal propeptide of type 1 pro-collagen (PINP), and β-isomerized C-terminal telopeptide of type 1 collagen (β-CTx), as well as postprandial serum aminoacidemia regarding 18 collagen amino acids. Strikingly, serum PINP did not increase following RE alone. However, both 15 and 30 g HC ingested prior to RE elevated the serum PINP concentration × time area-under-the-curve (AUC). The PINP AUC was even higher when 30 g HC was ingested compared to 15 g HC (169 ± 28 vs. 134 ± 23 µg/mL × h, P < 0.05), and this effect was mirrored in higher amino acid serum concentration × time AUCs regarding glycine, proline, and hydroxyproline (amongst other collagen amino acids). Although β-CTx decreased immediately following RE, there was no additional effect of HC ingestion on this marker of collagen degradation.
The second lab-based experimental study (Chapter Five) extended this work to middle-aged, eumenorrheic, premenopausal women. In this case study, two resistance trained women performed 4 sets of high intensity RE in the late follicular phase of their menstrual cycles, where one participant ingested 30 g HC, and the other an energy matched placebo (0 g HC). The findings were consisted with the male cohort, i.e. there was no change in serum PINP concentration in the 6 h following RE with 0 g HC. However, the participant who ingested 30 g HC experienced a noticeable peak in PINP 4 h post-RE (37.4 µg/mL, approximately 2-fold baseline), and a greater concentration × time AUC (193 µg/mL × h) compared to the participant who ingested the 0 g beverage (85 µg/mL × h). These findings were also consistent with the bioavailability of 18 collagen amino acids, i.e. the serum concentration × time AUCs were low during the 0 g HC intervention but high during the 30 g HC intervention.
Based on the findings of chapters four and five, showing that 15 g recovers the collagen synthesis response to RT in middle-aged men, but that 30 g HC is most effective at increasing post-RE collagen synthesis in middle-age, resistance trained men and women, the third (Chapter Six) and fourth (Chapter Seven) experimental chapters explored the chronic effects (8 – 12 weeks) of RT with 30 g HC on patellar tendon adaptations in middle-aged women and men, respectively.
Chapter Six investigated the effects of eight weeks’ eccentric RT with 30 g HC supplementation on changes in tendon properties in premenopausal, middle-aged female athletes. Specifically, 22 international Master field hockey athletes were recruited from the Ireland over 35s and over 40s squads, and randomly assigned to either a collagen (COL, n = 10) or placebo (PLA, n = 12) group in a double-blind manner. Participants ingested either 30 g HC (COL) or 30 g maltodextrin (PLA), both with 500 mg vitamin C, three times a week for eight weeks. Alongside supplementation, they completed one high-intensity flywheel squat RE session and two lower-limb eccentric bodyweight RE sessions per week, which was in addition to their regular hockey training. Both groups experienced increases in muscle size and maximal voluntary force. Patellar tendon CSA increased in both groups (F1, 20 = 36.482, p < .001, ηp2 = 0.646) but the 4.6 ± 2.7 % increase in COL was greater than the 2.0 ± 2.8 % increase in PLA (t20 = 2.18, p = 0.021, d = 0.935). Similarly, peak rate of force development (pRFD) increased in both groups (F1,17 = 14.26, P = 0.002, ηp2 = 0.456) but the 27.3 ± 19.2 % increase in COL was greater than the 8.0 ± 19.6 % increase in PLA (t1,18 = 2.16, p = 0.045, d = 0.994).
Chapter Seven, the final experimental study of this thesis, involved a double-blind, parallel designed study, where 20 recreationally active men (age, 47 ± 5 years) were randomly assigned to either a placebo (PLA, n = 11) or collagen (COL, n = 9) group. Both groups performed progressive lower limb RT twice weekly for 12 weeks. Participants consumed either 30 g HC and 50 mg vitamin C (COL) or an energy-matched beverage, containing 30.5 g maltodextrin and 50 mg vitamin C (PLA). Following RT, patellar tendon CSA increased in COL but not in PLA. Patellar tendon stiffness and Young’s modulus increased more in COL (+661 ± 331 N/mm; + 0.21 ± 0.13 GPa) than in PLA (+ 247 ± 305 N/mm, group × time P = 0.009; + 0.09 ± 0.13 GPa, group × time, p = 0.018). Both groups experienced similar increases in muscle size, strength and peak rate of torque development. Although there were increases in tendon stiffness with RT alone, the lack of change in tendon CSA in PLA aligns with the potential tendon anabolic resistance suggested in Chapter Three, and further supports the changes in collagen turnover were mostly reflective of tendon, rather than muscle or bone.
This thesis provides the first evidence that adult populations in Ireland consume low amounts of collagen, especially females and older adults, which is likely to have implications for musculoskeletal health. Novel findings show the collagen synthesis response to a single bout of high intensity RE is blunted in middle-aged, resistance-trained men and women, but that it can be rescued by ingesting 15 g HC, while 30 g HC provides an even greater benefit.
The effect of chronic RT with 30 g HC supplementation produced positive, but slightly differing outcomes in male and female muscle-tendon adaptations, likely due to methodological differences between the studies. After 12 weeks, high intensity RT increased patellar tendon stiffness and Young’s modulus, but not tendon CSA, in recreationally active, healthy, middle-aged men. Supplementing RT with 30 g HC, on the other hand, increased patellar tendon CSA and enhanced gains in tendon stiffness and Young’s modulus, without translating to greater increases in pRFD. In international female Master athletes, eight weeks’ eccentric RT increased patellar tendon CSA and pRFD, but these gains were augmented by ingesting 30 g HC alongside training. Taken together, the novel findings from these exercise-nutrition studies have the potential to impact training and nutrition prescription in middle-aged athletic populations. Future studies should focus on the optimal HC dosing strategies for middle-age and older females across diverse hormonal profiles, including post-menopausal women and those prescribed exogenous hormone replacement. Given the positive effects observed on tendon properties and muscle-tendon unit function, long-term prospective studies could examine whether these adaptations lead to a reduction in injury risk in recreationally active middle-aged cohorts and Master athletes.

Item Type:	Thesis (Doctoral)
Uncontrolled Keywords:	tendon stiffness; glycine; proline; hydroxyproline; collagen synthesis; collagen breakdown; cross sectional area
Subjects:	R Medicine > RC Internal medicine > RC1200 Sports Medicine
Divisions:	Sport and Exercise Sciences
Date of acceptance:	28 April 2025
Date of first compliant Open Access:	25 June 2025
Date Deposited:	25 Jun 2025 08:57
Last Modified:	25 Jun 2025 08:57
DOI or ID number:	10.24377/LJMU.t.00026503
Supervisors:	Erskine, RM, Enright, K and Stewart, C
URI:	https://researchonline.ljmu.ac.uk/id/eprint/26503

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