Next Article in Journal
Favism: Clinical Features at Different Ages
Next Article in Special Issue
Mechanistic Understanding of D-Glucaric Acid to Support Liver Detoxification Essential to Muscle Health Using a Computational Systems Biology Approach
Previous Article in Journal
Longitudinal Association between Physical Activity, Blood Lipids, and Risk of Dyslipidemia among Chinese Adults: Findings from the China Health and Nutrition Surveys in 2009 and 2015
Previous Article in Special Issue
Nutritional Compounds to Improve Post-Exercise Recovery
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Nutrients
Volume 15
Issue 2
10.3390/nu15020342
nutrients-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Supplementation with Whey Protein, but Not Pea Protein, Reduces Muscle Damage Following Long-Distance Walking in Older Adults

by
Marcia Spoelder
†,
Lotte Koopmans
†,
Yvonne A. W. Hartman
,
Coen C. W. G. Bongers
,
Merle C. A. Schoofs
,
Thijs M. H. Eijsvogels
and
Maria T. E. Hopman
*
Radboud Institute for Health Sciences, Department of Physiology, Radboud University Medical Center, 6500 HB Nijmegen, The Netherlands
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Nutrients 2023, 15(2), 342; https://doi.org/10.3390/nu15020342
Submission received: 16 November 2022 / Revised: 23 December 2022 / Accepted: 28 December 2022 / Published: 10 January 2023
(This article belongs to the Special Issue Nutrition-Based Strategies to Reduce Exercise-Induced Muscle Damage and Soreness)
Browse Figures
Versions Notes

Abstract

:
Background: Adequate animal-based protein intake can attenuate exercise induced-muscle damage (EIMD) in young adults. We examined the effects of 13 days plant-based (pea) protein supplementation compared to whey protein and placebo on EIMD in active older adults. Methods: 47 Physically active older adults (60+ years) were randomly allocated to the following groups: (I) whey protein (25 g/day), (II) pea protein (25 g/day) or (III) iso-caloric placebo. Blood concentrations of creatine kinase (CK) and lactate dehydrogenase (LDH), and skeletal muscle mass, muscle strength and muscle soreness were measured prior to and 24 h, 48 h and 72 h after a long-distance walking bout (20–30 km). Results: Participants walked 20–30 km and 2 dropped out, leaving n = 15 per subgroup. The whey group showed a significant attenuation of the increase in EIMD at 24 h post-exercise compared to the pea and placebo group (CK concentration: 175 ± 90 versus 300 ± 309 versus 330 ± 165, p = p < 0.001). No differences in LDH levels, muscle strength, skeletal muscle mass and muscle soreness were observed across groups (all p-values > 0.05). Conclusions: Thirteen days of pea protein supplementation (25 g/day) does not attenuate EIMD in older adults following a single bout of prolonged walking exercise, whereas the whey protein supplementation group showed significantly lower post-exercise CK concentrations.

1. Introduction

The post-exercise inflammatory response, characterized by muscle damage and elevated plasma levels of creatine kinase (CK), is a normal physiological process that is thought to play a vital role in tissue damage repair and enhancing muscle adaptation [1]. Older adults exhibit higher levels of muscle damage and a slower recovery rate upon an exercise bout compared to younger adults [2,3], which may hamper them in pursuing an active lifestyle, accelerating sarcopenia [4].
Daily dietary protein intake is an important factor for muscle repair by enhancing muscle protein synthesis [5,6,7,8]. It has been shown that more than 50% of physically active older adults do not reach the recommended protein intake of 1.2 g/kg/day [9]. Moreover, an increasing number of individuals avoid animal based products in order to reduce their ecological footprint [10]. Studies in young adults have shown that plant-based proteins were able to induce muscle protein synthesis upon digestion, leading to increases in muscle mass after resistance training, comparable to whey protein [11,12,13]. In addition, a reduction in muscle damage was observed in young and middle-aged men after 4 days of eccentric exercise and supplementation both with pea and whey protein [5]. However, no studies have investigated the effect of plant-based protein supplementation on muscle damage markers in older adults who performed a bout of endurance exercise.
This randomized double-blind placebo-controlled trial aimed to assess the effect of pea versus whey protein supplementation in comparison to placebo on exercise-induced increases in muscle damage markers in older adults 1, 2 and 3 days after endurance walking exercise. Secondary outcome measures included differences in changes in muscle soreness, muscle strength and muscle mass among groups after endurance walking exercise. We hypothesized that pea protein supplementation would be able to reduce muscle damage after endurance walking exercise in adults comparable to whey protein supplementation.

2. Materials and Methods

2.1. Participants

Participants were recruited in July 2021 via the Nijmegen Exercise Study database [14] and advertisements via social media. Individuals aged ≥60 years and capable of walking ≥20 km in a single exercise bout were eligible for inclusion. Exclusion criteria were diabetes mellitus type I and II, being allergic or sensitive for milk proteins or lactose intolerance, a BMI > 30 kg/m2, Chronic Obstructive Pulmonary Disease (COPD), renal insufficiency, and an intestinal disease that may influence protein uptake. Moreover, consumption of other freely available protein supplements was not allowed during the study period and participants were requested not to perform prolonged exercises in the 4 days before or after the endurance walking exercise. All participants provided written informed consent prior to any experimental procedure. The study conformed to the principles of the Declaration of Helsinki, was approved by the local Medical Ethical committee (Study-ID: NL77522.091.21) and registered at the Dutch trial registry (#NL9499).

2.2. Study Design

In this randomized double-blind placebo-controlled trial, a total of 47 participants were randomly allocated to a whey protein, pea protein or placebo supplement group. Participants were invited for 5 study visits at the department of Physiology of the Radboud university medical center (Figure 1). Measurements were performed at baseline (i.e., before supplement use), pre-exercise (i.e., after a 10 day pre-load period of supplement use) and three times post-exercise (+24 h, +48 h and +72 h). The exercise bout consisted of a self-selected 20–30 km walk to provoke muscle damage and muscle soreness. Supplement use was continued on the day of the exercise bout and on the three days thereafter.

2.3. Supplementation Protocol

Participants were instructed to consume the assigned supplement twice a day for a period of 13 days (10 days prior to the exercise bout and 3 days post exercise). This pre-loading period was chosen as previous studies have demonstrated its importance [15,16], as the lack of pre-loading may prevent the effect of protein supplementation on attenuation of exercise induced muscle damage [17] possibly due to insufficient circulating amino acids. The supplements were provided as a dried powder product (Table 1) in a white container with a twist cap and a measurement spoon inside. Participants were instructed to accurately weigh the correct grams of supplement. Participants were instructed to consume 12.5 g of protein (i.e., 15 g of dry powder) in the morning and 12.5 g of protein in the afternoon/evening (or after exercise). The supplement powder had to be dissolved in a liquid (water, juice) and ingested by the participant. All supplements were provided by NewCare (Waalwijk, The Netherlands) and obtained from DuSart Pharma (Katwijk aan Zee, The Netherlands). Participants were provided with a diary at their first study visit and were asked to report their daily supplement intake throughout the study. The diaries were collected during the last study visit of the participants to assess the adherence of supplement intake. Containers of the supplement were also collected and the remaining content was weighted.

2.4. Measurements

2.4.1. Blood Samples

Venous blood was drawn from the antecubital vein during each visit, and serum and lithium heparin plasma samples were stored at −80 °C until further analyses. Analyses were performed by trained technicians using standard operating procedures. CK and LDH levels were measured using a C8000 module C720 clinical chemistry analyzer (Roche, Almere, The Netherlands) to identify muscle damage and tissue damage, respectively.

2.4.2. Habitual Walking Characteristics

The habitual walking activity in the past year (July 2020–July 2021) was assessed at baseline using an online questionnaire. Participants were asked to indicate how frequent they walked per week, the average number of kilometers per walking bout and how many weeks in the past year they performed the reported walking bouts. Hence, the cumulative walking distance was calculated.

2.4.3. Exercise Intervention

Participants were instructed to perform a single walking bout with a minimum of 20 km and a maximum of 30 km. Walking distance, exercise duration and whether participants suffered from physical discomfort were registered directly following the exercise bout.

2.4.4. Muscle Soreness

Muscle soreness was assessed using a Numeric (pain) Rating Scale (NPRS) where participants could mark a pain score between no pain at all (NRS = 0) and extremely painful (NRS = 10). NPRS scores of 1–5 were considered as mild pain, 6–7 as moderate pain and >8 as severe pain [18,19].

2.4.5. Dietary Intake

Food consumption patterns were assessed using an online Dutch tool (i.e., ‘Mijn Voedingscentrum’) [20]. Participants entered their full eating and drinking pattern during 2 days (at least one weekend day) in the pre-load period. Participants were instructed to exclude the supplement from their dietary assessment. The average total energy intake, as well as micro- and macro-nutrient intake of the two recorded days was subsequently calculated and used in the data analyses.

2.4.6. Muscle Strength

Handgrip strength of the right hand was measured with a hydraulic, analogue handheld dynamometer (JAMAR®, Chicago, IL, USA). Participants were asked to shortly squeeze the handgrip instrument as hard as they could for three times, with one minute rest in between each measurement [21]. Maximum strength in kilograms was used for analysis.
Leg muscle strength was measured in kilograms with an EN-Dynamic seated leg press (Enraf-Nonius, Rotterdam, The Netherlands). After adjusting the seat and a warm-up, participants had to perform one leg press per fixed step. The weight was increased gradually in seven fixed steps dependent on their body weight to directly determine the 1 repetition maximum (1 RM). There were only 7 attempts to determine the 1 RM to prevent injury and overexerting participants.

2.4.7. Anthropometrics and Muscle Mass

Body height and weight of the participants were measured. Total skeletal muscle mass (SMM) of both legs were estimated with bioelectrical impedance analyses (InBody 770 Body Composition Analyzed, Seoul, Republic of Korea) [22]. Participants were instructed not to eat or drink for 2 h before the measurement and were asked to use the bathroom shortly before their body composition measurement.

3. Statistical Analysis

Statistical analyses were performed using SPSS software (IBM SPSS Statistics for Windows, Version 25.0 IBM Corp., Armonk, NY, USA) and graphs were made using Graphpad Prism 9. All continuous variables and the residuals of the variables used in the linear-effects model were visually inspected and tested for normality with the Kolmogorov–Smirnov test. Logarithmic transformations were applied when data were not normally distributed and subsequently the normality was retested. Logarithmic transformations of CK and LDH were used in the statistical analyses in all cases. Data were displayed as mean ± SD or median (interquartile range [IQR]) for parametric and non-parametric continuous variables, respectively. Group differences were analyzed using a One-Way ANOVA or Kruskal–Wallis for parametric or non-parametric continuous variables, respectively. Repeated observations over days, such as CK, LDH and skeletal muscle mass, were analyzed using linear mixed-effects models with compound symmetry as the repeated covariance type in which group and time (e.g., 24 h, 48 h and 72 h upon walking) were treated as independent variables. The pre-exercise values were used as a covariate in the linear mixed model analyses. When significant main effects or interactions were detected, Bonferroni post hoc comparisons were made in case of parametric variables and Mann–Whitney U tests in case of non-parametric variables. Repeated measures analyses for the non-parametric muscle soreness values were performed using a Friedman analysis. The level of significance was set at p < 0.05 (two-sided).

4. Results

4.1. Participants

One participant from the placebo group withdrew from further participation after the baseline measurement due to personal reasons not related to the study protocol. Another participant from the pea supplement group dropped out due to heavy muscle cramps during the walking exercise bout and was therefore unable to complete the minimum walking distance of 20 km. This resulted in 15 participants per subgroup. Participants were predominantly male (80%), aged 70 ± 6 years with a BMI of 24.2 ± 2.8 kg/m2. No differences were observed for demographics and anthropometrics across the three supplementation groups (Table 2).

4.2. Habitual Dietary Intake and Walking Activity

Total energy intake was 2078 ± 528 kcal and comparable across groups (p = 0.57, Table 2). The habitual daily protein intake was 1.13 g/kg/day at baseline and did not differ between the whey, pea and placebo supplemented group (p = 0.82). A total of 40% of the participants had a protein intake below 1.0 g/kg/day, but the prevalence was comparable among the three groups. The cumulative walking distance in kilometers in the past year was highly variable across participants (range: 0 to 4680 km/year), with a significantly lower cumulative walking distance for the pea versus whey protein group (p = 0.004).

4.3. Exercise Bout Characteristic

Participants covered a walking distance of 24.3 ± 4.9 km with a duration of 5.2 ± 1.1 h. Walking distance and exercise duration did not differ across the three groups (p = 0.19 and p = 0.28, respectively).

4.4. Muscle Damage

The time-dependent exercise-induced increase in creatine kinase (CK) levels were significantly different between the three groups (Pinteraction = 0.018). Peak CK concentrations (+24 h) were significantly lower in the whey (175 ± 90 U/l) versus placebo (300 ± 309 U/l, p = 0.024) and pea supplemented group (330 ± 125 U/l, p = 0.022, Figure 2A). No differences were observed between the pea- and placebo supplemented group (p = 1.00). Correction for the cumulative walking distance in the past year did not alter the observed findings in the statistical analyses (p = 0.020). Lactate dehydrogenase (LDH) levels increased over time (p < 0.001), and post hoc analyses showed that serum LDH levels at 72 h post-exercise were higher compared to 24 h and 48 h post-exercise (p < 0.001, Figure 2B). Nevertheless, no group differences (p = 0.25) or interaction effects (p = 0.54) were observed in LDH levels.

4.5. Muscle Parameters

Maximum recorded handgrip strength was not different between groups (p = 0.45), but handgrip strength increased over time (p = 0.030). This increase did not differ across groups (Pinteraction = 0.33, Figure 3A). Leg strength, corrected for body weight, showed no group differences (p = 0.98), nor differences over time (p = 0.55, Figure 3B). The skeletal muscle mass of the participants, corrected for body weight (SMM%), was comparable between groups (p = 0.39), decreased over time-points (p = 0.015), but did not differ across groups (p = 0.40, Figure 3C). Muscle soreness increased following exercise (p = 0.042), but was comparable between groups (p = 0.49, Figure 3D).

5. Discussion

The aim of this randomized double-blind placebo-controlled trial was to assess the effect of pea protein and whey protein supplementation versus placebo on exercise-induced increases in muscle damage markers within older adults. We found that long-distance walking exercise provoked muscle damage, with peak CK levels around 24 h post-exercise in physically active older men and women. The CK increase is in line with a previous study who measured CK release in vital elderly after comparable bout of walking exercise [2]. Thirteen days of pea protein supplementation did not impact exercise-induced elevations in CK levels, as reflected by comparable CK responses compared to the placebo group. However, whey protein supplementation attenuated the increase in CK levels at 24 h post-exercise compared to the placebo- and pea protein supplementation group. No differences in LDH levels, muscle strength, skeletal muscle mass and muscle soreness were observed across groups. Findings from this study suggest that thirteen days of pea protein supplementation is not able to attenuate exercise-induced muscle damage in active older adults comparable to whey protein supplementation.
The magnitude of exercise-induced CK elevations was similar in active older adults receiving pea protein supplementation compared to placebo. These findings are contradictory to previous studies using other plant-based proteins, such as soy and oat, as an attenuated exercise-induced increase in CK levels was found compared to the placebo group [15,23]. Potential explanations, apart from the difference in plant protein source, for these discrepant outcomes, may be the higher dosage of the protein that was used (42 gr/day versus 25 gr/day [23]) and the younger age of study participants (<40 years versus >60 years) [15,23] in previous work compared to our study. Older adults are less responsive to the anabolic stimulus of a low dose of amino acid intake than younger individuals [24]. Moreover, the digestibility of protein is also age-dependent, with poorer digestibility rates at older ages [25,26,27,28]. Research on the effects of high dosage plant-based protein supplementation in active older adults would add value to this topic. Alternatively, the type of exercise intervention may have played a role since downhill running and eccentric exercise produce greater CK elevations than prolonged walking exercise [1,2,29,30]. Taken together, 13 days of pea protein supplementation at 25 g per day was insufficient to attenuate the moderate exercise-induced increase in CK levels following prolonged walking in older adults.
In contrast to the pea protein group, an attenuated exercise-induced elevation in CK concentrations was observed for the whey protein group. Whey protein supplementation is known to limit exercise-induced muscle damage [31,32] and its superior effect compared to plant-based protein may relate to differences in the essential amino acid content [33,34,35]. Plant based proteins have a relatively low leucine content (7.1 ± 0.8%) compared to animal-based proteins (8.8 ± 0.7%) [35]. Leucine is known as one of the most important factors of protein synthesis and it also inhibits protein degradation [36]. Previous studies have suggested that every protein supplement serving should contain at least 700 mg of leucine [37]. Given our standardized serving volume for every treatment arm, leucine content was lower for the pea versus whey protein supplement (900 mg versus 1150 mg, respectively). The difference of 250 mg of leucine between these supplements may have contributed to the distinct CK-response following exercise. Fortifying plant-based proteins with leucine may be a promising strategy to limit exercise-induced muscle damage to a comparable extent as is found after whey supplementation.
The digestibility of whey protein could be another important factor to explain the difference in exercise-induced elevations of CK concentrations compared to pea protein supplementation. Literature about the bio-availability of pea protein is contradictory. In vitro digestibility values are similar between whey and pea protein [38], whereas total amino acid concentrations in humans after digestion seems to be lower for pea compared to whey protein [39]. More research is needed to understand if digestion alters pea protein amino acid availability and transport compared to whey protein. A solution to meet the required amino acid composition in combination with a better digestibility could be to mix different plant-based protein sources to improve the effects [34].
Our study did not show effects of protein or placebo supplementation on changes in serum LDH concentrations, muscle strength, muscle soreness and skeletal muscle mass. The pattern of blood LDH showed a different response to the walking exercise compared to the CK response. This finding in our participants is not in line with most other literature where LDH was used as a marker for muscle damage after short periods of intense exercise (30 min–1.5 h) [40,41,42,43]. However, Rodigues et al. performed a study with fifteen endurance trained male cyclist who performed a 130 km cycling race. In their study they found a similar LDH peak pattern as our study [44]. An explanation for the differences in time of LDH peak can probably be explained by the duration of exercise, since the duration of 130 km cycling is comparable to walk 20–30 km. Most of the studies have shorter exercise bouts while our study has a prolonged relatively low intensity walking bout. The higher handgrip strength at 48 h post-exercise may partially explained by a learning effect [45], but changes over time were small and likely clinically irrelevant. Several studies with protein supplementation varying from 8 weeks to 1 years show an increase in lean body mass, muscle strength and muscle mass for both plant-based and animal-based protein sources in younger and older adults [11,46,47,48,49,50]. This indicates that the 13 days of supplementation that was adopted in our study may not have been long enough to result in changes in muscle strength and skeletal muscle mass. Besides, leg press strength did not change after the walking exercise, suggesting that we either measured the wrong muscles (hamstrings and glutes whereas calf muscles may be more affected by walking exercise), or that the observed muscle damage was not substantial enough to limit muscle strength performance. Differences in the observed muscle damage (i.e., post-exercise CK concentrations) among groups were not reflected in differences in muscle soreness, probably because the magnitude in CK release and differences across groups was only moderate.
Several limitations apply to our study. The protocol used for assessment of 1 RM for leg strength made it difficult to determine 1 RM of participants that reached the maximum of 200 kg or the last attempt. This may have hampered the possible effect of protein supplementation on leg muscle strength. Furthermore, this study also had a relatively small population, which could result in less statistical power and the supplementation period could have been too short to have impact on secondary outcomes. At last, this study had a fixed protein supplementation dose (25 g/day) which increased daily protein intake to >1.0 g/kg/day in 93% of our participants. A personalized protein supplementation dose, based on the individual lean body mass, may therefore be recommended to future studies to achieve a maximal effective dose for all study participants.

6. Conclusions

Our randomized double-blind placebo-controlled trial demonstrated that 13 days with 25 g per day of pea protein suppletion did not attenuate exercise-induced muscle damage in older adults compared to placebo. In contrast, the whey protein group showed lower serum CK levels at 24 h post exercise compared to pea protein and placebo group. Furthermore, none of the applied protein supplementation strategies had effect on muscle strength, muscle soreness and skeletal muscle mass, potentially due to the relatively short supplementation period. The effects of long-term plant protein supplementation on exercise induced muscle damage and body composition should be further explored in physically active elderly. Participants may also be exposed to a higher dosage of plant-based protein, whereas the protein quality in terms of digestibility and composition should be taken into account.

Author Contributions

Conceptualization and methodology, M.S., Y.A.W.H., C.C.W.G.B., M.C.A.S. and M.T.E.H.; investigation: M.S., Y.A.W.H., C.C.W.G.B., T.M.H.E. and M.T.E.H.; formal analysis: M.S., M.C.A.S. and T.M.H.E.; writing—original draft preparation: M.S. and L.K.; writing—review and editing: M.S., L.K., Y.A.W.H., C.C.W.G.B., M.C.A.S., T.M.H.E. and M.T.E.H.; visualization: M.S. L.K.; project administration: M.S., Y.A.W.H., C.C.W.G.B. and M.T.E.H. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by NewCare (NewCare (Waalwijk, The Netherlands)).

Institutional Review Board Statement

The study conformed to the principles of the Declaration of Helsinki, was approved by the local Medical Ethical committee (Study-ID: NL77522.091.21) and registered at the Dutch trial registry (#NL9499).

Informed Consent Statement

All participants gave signed consent to participate in the research study.

Data Availability Statement

The datasets generated and/or analyzed during the current study are not publicly available due to the fact that study participants can be identified based on age, sex and finish time, but the pseudonymized dataset is available from the corresponding author upon reasonable request.

Acknowledgments

The authors greatly acknowledge the enthusiasm and dedication of the participants in this study. Furthermore, the practical assistance of colleagues and interns was greatly appreciated.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

CKCreatine Kinase
COPDChronic Obstructive Pulmonary Disease
EIMDExercise Induced Muscle Damage
LDHLactate Dehydrogenase
MPSMuscle Protein Synthesis
NRSNumeric (pain) Rating Scale
RMRepetition Maximum

References

  1. Markus, I.; Constantini, K.; Hoffman, J.R.; Bartolomei, S.; Gepner, Y. Exercise-Induced muscle damage: Mechanism, assessment and nutritional factors to accelerate recovery. Eur. J. Appl. Physiol. 2021, 121, 969–992. [Google Scholar] [CrossRef] [PubMed]
  2. Ten Haaf, D.S.M.; Bongers, C.; Hulshof, H.G.; Eijsvogels, T.M.H.; Hopman, M.T.E. The Impact of Protein Supplementation on Exercise-Induced Muscle Damage, Soreness and Fatigue Following Prolonged Walking Exercise in Vital Older Adults: A Randomized Double-Blind Placebo-Controlled Trial. Nutrients 2020, 12, 1806. [Google Scholar] [CrossRef] [PubMed]
  3. Clifford, T.; Hayes, E.J.; Scragg, J.H.; Taylor, G.; Smith, K.; Bowden Davies, K.A.; Stevenson, E.J. The Effects of a High-Protein Diet on Markers of Muscle Damage Following Exercise in Active Older Adults: A Randomized, Controlled Trial. Int. J. Sport Nutr. Exerc. Metab. 2020, 30, 323–329. [Google Scholar] [CrossRef] [PubMed]
  4. Cruz-Jentoft, A.J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyere, O.; Cederholm, T.; Cooper, C.; Landi, F.; Rolland, Y.; Sayer, A.A.; et al. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2019, 48, 16–31. [Google Scholar] [CrossRef] [Green Version]
  5. Nieman, D.C.; Zwetsloot, K.A.; Simonson, A.J.; Hoyle, A.T.; Wang, X.; Nelson, H.K.; Lefranc-Millot, C.; Guerin-Deremaux, L. Effects of Whey and Pea Protein Supplementation on Post-Eccentric Exercise Muscle Damage: A Randomized Trial. Nutrients 2020, 12, 2382. [Google Scholar] [CrossRef]
  6. Clifford, T. Nutritional and Pharmacological Interventions to Expedite Recovery Following Muscle-Damaging Exercise in Older Adults: A Narrative Review of the Literature. J. Aging Phys. Act. 2019, 27, 914–928. [Google Scholar] [CrossRef] [PubMed]
  7. Ten Haaf, D.S.M.; Nuijten, M.A.H.; Maessen, M.F.H.; Horstman, A.M.H.; Eijsvogels, T.M.H.; Hopman, M.T.E. Effects of protein supplementation on lean body mass, muscle strength, and physical performance in nonfrail community-dwelling older adults: A systematic review and meta-analysis. Am. J. Clin. Nutr. 2018, 108, 1043–1059. [Google Scholar] [CrossRef] [Green Version]
  8. Davies, R.W.; Carson, B.P.; Jakeman, P.M. The Effect of Whey Protein Supplementation on the Temporal Recovery of Muscle Function Following Resistance Training: A Systematic Review and Meta-Analysis. Nutrients 2018, 10, 221. [Google Scholar] [CrossRef] [Green Version]
  9. Ten Haaf, D.S.M.; De Regt, M.F.; Visser, M.; Witteman, B.J.M.; de Vries, J.H.M.; Eijsvogels, T.M.H.; Hopman, M.T.E. Insufficient Protein Intakes is Highly Prevalent among Physically Active Elderly. J. Nutr. Health Aging 2018, 22, 1112–1114. [Google Scholar] [CrossRef]
  10. Aschemann-Witzel, J.; Gantriis, R.F.; Fraga, P.; Perez-Cueto, F.J.A. Plant-based food and protein trend from a business perspective: Markets, consumers, and the challenges and opportunities in the future. Crit. Rev. Food Sci. Nutr. 2021, 61, 3119–3128. [Google Scholar] [CrossRef]
  11. Babault, N.; Paizis, C.; Deley, G.; Guerin-Deremaux, L.; Saniez, M.H.; Lefranc-Millot, C.; Allaert, F.A. Pea proteins oral supplementation promotes muscle thickness gains during resistance training: A double-blind, randomized, Placebo-controlled clinical trial vs. Whey protein. J. Int. Soc. Sports Nutr. 2015, 12, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Gorissen, S.H.; Horstman, A.M.; Franssen, R.; Crombag, J.J.; Langer, H.; Bierau, J.; Respondek, F.; van Loon, L.J. Ingestion of Wheat Protein Increases In Vivo Muscle Protein Synthesis Rates in Healthy Older Men in a Randomized Trial. J. Nutr. 2016, 146, 1651–1659. [Google Scholar] [CrossRef] [Green Version]
  13. Oikawa, S.Y.; Bahniwal, R.; Holloway, T.M.; Lim, C.; McLeod, J.C.; McGlory, C.; Baker, S.K.; Phillips, S.M. Potato Protein Isolate Stimulates Muscle Protein Synthesis at Rest and with Resistance Exercise in Young Women. Nutrients 2020, 12, 1235. [Google Scholar] [CrossRef] [PubMed]
  14. Maessen, M.F.; Verbeek, A.L.; Bakker, E.A.; Thompson, P.D.; Hopman, M.T.; Eijsvogels, T.M. Lifelong Exercise Patterns and Cardiovascular Health. Mayo Clin. Proc. 2016, 91, 745–754. [Google Scholar] [CrossRef]
  15. Xia, Z.; Cholewa, J.M.; Dardevet, D.; Huang, T.; Zhao, Y.; Shang, H.; Yang, Y.; Ding, X.; Zhang, C.; Wang, H.; et al. Effects of oat protein supplementation on skeletal muscle damage, inflammation and performance recovery following downhill running in untrained collegiate men. Food Funct. 2018, 9, 4720–4729. [Google Scholar] [CrossRef]
  16. Rohling, M.; McCarthy, D.; Berg, A. Continuous Protein Supplementation Reduces Acute Exercise-Induced Stress Markers in Athletes Performing Marathon. Nutrients 2021, 13, 2929. [Google Scholar] [CrossRef] [PubMed]
  17. Ten Haaf, D.S.M.; Flipsen, M.A.; Horstman, A.M.H.; Timmerman, H.; Steegers, M.A.H.; de Groot, L.; Eijsvogels, T.M.H.; Hopman, M.T.E. The Effect of Protein Supplementation versus Carbohydrate Supplementation on Muscle Damage Markers and Soreness Following a 15-km Road Race: A Double-Blind Randomized Controlled Trial. Nutrients 2021, 13, 858. [Google Scholar] [CrossRef]
  18. Hjermstad, M.J.; Fayers, P.M.; Haugen, D.F.; Caraceni, A.; Hanks, G.W.; Loge, J.H.; Fainsinger, R.; Aass, N.; Kaasa, S.; European Palliative Care Research, C. Studies comparing Numerical Rating Scales, Verbal Rating Scales, and Visual Analogue Scales for assessment of pain intensity in adults: A systematic literature review. J. Pain Symptom Manag. 2011, 41, 1073–1093. [Google Scholar] [CrossRef]
  19. Boonstra, A.M.; Stewart, R.E.; Koke, A.J.; Oosterwijk, R.F.; Swaan, J.L.; Schreurs, K.M.; Schiphorst Preuper, H.R. Cut-Off Points for Mild, Moderate, and Severe Pain on the Numeric Rating Scale for Pain in Patients with Chronic Musculoskeletal Pain: Variability and Influence of Sex and Catastrophizing. Front. Psychol 2016, 7, 1466. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Ocke, M.; Dinnissen, C.; Stafleu, A.; de Vries, J.; van Rossum, C. Relative Validity of MijnEetmeter: A Food Diary App for Self-Monitoring of Dietary Intake. Nutrients 2021, 13, 1135. [Google Scholar] [CrossRef] [PubMed]
  21. Ottestad, I.; Lovstad, A.T.; Gjevestad, G.O.; Hamarsland, H.; Saltyte Benth, J.; Andersen, L.F.; Bye, A.; Biong, A.S.; Retterstol, K.; Iversen, P.O.; et al. Intake of a Protein-Enriched Milk and Effects on Muscle Mass and Strength. A 12-Week Randomized Placebo Controlled Trial among Community-Dwelling Older Adults. J. Nutr. Health Aging 2017, 21, 1160–1169. [Google Scholar] [CrossRef] [PubMed]
  22. Brewer, G.J.; Blue, M.N.M.; Hirsch, K.R.; Saylor, H.E.; Gould, L.M.; Nelson, A.G.; Smith-Ryan, A.E. Validation of InBody 770 bioelectrical impedance analysis compared to a four-compartment model criterion in young adults. Clin. Physiol. Funct. Imaging 2021, 41, 317–325. [Google Scholar] [CrossRef]
  23. Shenoy, S.; Dhawan, M.; Singh Sandhu, J. Four Weeks of Supplementation With Isolated Soy Protein Attenuates Exercise-Induced Muscle Damage and Enhances Muscle Recovery in Well Trained Athletes: A Randomized Trial. Asian J. Sports Med. 2016, 7, e33528. [Google Scholar] [CrossRef] [Green Version]
  24. Baum, J.I.; Kim, I.Y.; Wolfe, R.R. Protein Consumption and the Elderly: What Is the Optimal Level of Intake? Nutrients 2016, 8, 359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Gorissen, S.H.M.; Trommelen, J.; Kouw, I.W.K.; Holwerda, A.M.; Pennings, B.; Groen, B.B.L.; Wall, B.T.; Churchward-Venne, T.A.; Horstman, A.M.H.; Koopman, R.; et al. Protein Type, Protein Dose, and Age Modulate Dietary Protein Digestion and Phenylalanine Absorption Kinetics and Plasma Phenylalanine Availability in Humans. J. Nutr. 2020, 150, 2041–2050. [Google Scholar] [CrossRef] [Green Version]
  26. Deutz, N.E.; Bauer, J.M.; Barazzoni, R.; Biolo, G.; Boirie, Y.; Bosy-Westphal, A.; Cederholm, T.; Cruz-Jentoft, A.; Krznaric, Z.; Nair, K.S.; et al. Protein intake and exercise for optimal muscle function with aging: Recommendations from the ESPEN Expert Group. Clin. Nutr. 2014, 33, 929–936. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Koopman, R.; van Loon, L.J. Aging, exercise, and muscle protein metabolism. J. Appl. Physiol. 2009, 106, 2040–2048. [Google Scholar] [CrossRef] [PubMed]
  28. Wall, B.T.; Gorissen, S.H.; Pennings, B.; Koopman, R.; Groen, B.B.; Verdijk, L.B.; van Loon, L.J. Aging Is Accompanied by a Blunted Muscle Protein Synthetic Response to Protein Ingestion. PLoS ONE 2015, 10, e0140903. [Google Scholar] [CrossRef] [PubMed]
  29. Schoenfeld, B.J. Does exercise-induced muscle damage play a role in skeletal muscle hypertrophy? J. Strength Cond. Res. 2012, 26, 1441–1453. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Brancaccio, P.; Maffulli, N.; Limongelli, F.M. Creatine kinase monitoring in sport medicine. Br. Med. Bull. 2007, 81–82, 209–230. [Google Scholar] [CrossRef]
  31. Cooke, M.B.; Rybalka, E.; Stathis, C.G.; Cribb, P.J.; Hayes, A. Whey protein isolate attenuates strength decline after eccentrically-induced muscle damage in healthy individuals. J. Int. Soc. Sports Nutr. 2010, 7, 30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Buckley, J.D.; Thomson, R.L.; Coates, A.M.; Howe, P.R.; DeNichilo, M.O.; Rowney, M.K. Supplementation with a whey protein hydrolysate enhances recovery of muscle force-generating capacity following eccentric exercise. J. Sci. Med. Sport 2010, 13, 178–181. [Google Scholar] [CrossRef] [PubMed]
  33. Kerksick, C.M.; Jagim, A.; Hagele, A.; Jager, R. Plant Proteins and Exercise: What Role Can Plant Proteins Have in Promoting Adaptations to Exercise? Nutrients 2021, 13, 1962. [Google Scholar] [CrossRef]
  34. van Vliet, S.; Burd, N.A.; van Loon, L.J. The Skeletal Muscle Anabolic Response to Plant- versus Animal-Based Protein Consumption. J. Nutr. 2015, 145, 1981–1991. [Google Scholar] [CrossRef] [Green Version]
  35. Gorissen, S.H.M.; Crombag, J.J.R.; Senden, J.M.G.; Waterval, W.A.H.; Bierau, J.; Verdijk, L.B.; van Loon, L.J.C. Protein content and amino acid composition of commercially available plant-based protein isolates. Amino Acids 2018, 50, 1685–1695. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Duan, Y.; Li, F.; Li, Y.; Tang, Y.; Kong, X.; Feng, Z.; Anthony, T.G.; Watford, M.; Hou, Y.; Wu, G.; et al. The role of leucine and its metabolites in protein and energy metabolism. Amino Acids 2016, 48, 41–51. [Google Scholar] [CrossRef]
  37. Jager, R.; Kerksick, C.M.; Campbell, B.I.; Cribb, P.J.; Wells, S.D.; Skwiat, T.M.; Purpura, M.; Ziegenfuss, T.N.; Ferrando, A.A.; Arent, S.M.; et al. International Society of Sports Nutrition Position Stand: Protein and exercise. J. Int. Soc. Sports Nutr. 2017, 14, 20. [Google Scholar] [CrossRef] [Green Version]
  38. Corgneau, M.; Gaiani, C.; Petit, J.; Nikolova, Y.; Banon, S.; Ritié-Pertusa, L.; Le, D.T.L.; Scher, J. Nutritional quality evaluation of commercial protein supplements. Int. J. Food Sci. Technol. 2019, 54, 2586–2594. [Google Scholar] [CrossRef]
  39. Liu, J.; Klebach, M.; Visser, M.; Hofman, Z. Amino Acid Availability of a Dairy and Vegetable Protein Blend Compared to Single Casein, Whey, Soy, and Pea Proteins: A Double-Blind, Cross-Over Trial. Nutrients 2019, 11, 2613. [Google Scholar] [CrossRef] [Green Version]
  40. Minahan, C.L.; Poke, D.P.; Morrison, J.; Bellinger, P.M. Muscle Damage and Metabolic Responses to Repeated-Sprint Running With and Without Deceleration. J. Strength Cond. Res. 2020, 34, 3423–3430. [Google Scholar] [CrossRef]
  41. Callegari, G.A.; Novaes, J.S.; Neto, G.R.; Dias, I.; Garrido, N.D.; Dani, C. Creatine Kinase and Lactate Dehydrogenase Responses after Different Resistance and Aerobic Exercise Protocols. J. Hum. Kinet. 2017, 58, 65–72. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Chapman, D.W.; Newton, M.J.; Zainuddin, Z.; Sacco, P.; Nosaka, K. Work and peak torque during eccentric exercise do not predict changes in markers of muscle damage. Br. J. Sports Med. 2008, 42, 585–591. [Google Scholar] [CrossRef] [PubMed]
  43. Ispirlidis, I.; Fatouros, I.G.; Jamurtas, A.Z.; Nikolaidis, M.G.; Michailidis, I.; Douroudos, I.; Margonis, K.; Chatzinikolaou, A.; Kalistratos, E.; Katrabasas, I.; et al. Time-course of changes in inflammatory and performance responses following a soccer game. Clin. J. Sport Med. 2008, 18, 423–431. [Google Scholar] [CrossRef]
  44. Rodrigues, P.; Wassmansdorf, R.; Salgueirosa, F.M.; Hernandez, S.G.; Nascimento, V.B.; Daros, L.B.; Lee, W.; Ousicki, R. Time-course of changes in indirect markers of muscle damage responses following a 130-km cycling race. Rev. Bras. CIneantropom Hum. 2016, 18, 322–331. [Google Scholar] [CrossRef] [Green Version]
  45. Mehmet, H.; Yang, A.W.H.; Robinson, S.R. Measurement of hand grip strength in the elderly: A scoping review with recommendations. J. Bodyw. Mov. Ther. 2020, 24, 235–243. [Google Scholar] [CrossRef]
  46. Joy, J.M.; Lowery, R.P.; Wilson, J.M.; Purpura, M.; De Souza, E.O.; Wilson, S.M.; Kalman, D.S.; Dudeck, J.E.; Jager, R. The effects of 8 weeks of whey or rice protein supplementation on body composition and exercise performance. Nutr. J. 2013, 12, 86. [Google Scholar] [CrossRef] [Green Version]
  47. Kim, J.E.; O’Connor, L.E.; Sands, L.P.; Slebodnik, M.B.; Campbell, W.W. Effects of dietary protein intake on body composition changes after weight loss in older adults: A systematic review and meta-analysis. Nutr. Rev. 2016, 74, 210–224. [Google Scholar] [CrossRef] [Green Version]
  48. Morton, R.W.; Murphy, K.T.; McKellar, S.R.; Schoenfeld, B.J.; Henselmans, M.; Helms, E.; Aragon, A.A.; Devries, M.C.; Banfield, L.; Krieger, J.W.; et al. A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults. Br. J. Sports Med. 2018, 52, 376–384. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Nakayama, K.; Saito, Y.; Sanbongi, C.; Murata, K.; Urashima, T. Effects of low-dose milk protein supplementation following low-to-moderate intensity exercise training on muscle mass in healthy older adults: A randomized placebo-controlled trial. Eur. J. Nutr. 2021, 60, 917–928. [Google Scholar] [CrossRef]
  50. Tieland, M.; Dirks, M.L.; van der Zwaluw, N.; Verdijk, L.B.; van de Rest, O.; de Groot, L.C.; van Loon, L.J. Protein supplementation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly people: A randomized, double-blind, placebo-controlled trial. J. Am. Med. Dir. Assoc. 2012, 13, 713–719. [Google Scholar] [CrossRef]
Nutrients 15 00342 g001 550
Figure 1. Overview of study timeline and measurements. #1–5 means visit 1–5.
Figure 1. Overview of study timeline and measurements. #1–5 means visit 1–5.
Nutrients 15 00342 g001
Nutrients 15 00342 g002 550
Figure 2. Change in Creatine kinase (CK) (A) and Lactate Dehydrogenase (LDH) (B) concentrations. Data is presented as mean with Standard Error of the Mean (SEM), while statistical analyses were performed on the logarithmic transformed data with the pre-exercise values as a covariate. * p < 0.05 indicates significant group differences at the respective time-point.
Figure 2. Change in Creatine kinase (CK) (A) and Lactate Dehydrogenase (LDH) (B) concentrations. Data is presented as mean with Standard Error of the Mean (SEM), while statistical analyses were performed on the logarithmic transformed data with the pre-exercise values as a covariate. * p < 0.05 indicates significant group differences at the respective time-point.
Nutrients 15 00342 g002
Nutrients 15 00342 g003 550
Figure 3. Muscle parameters. Changes in handgrip strength (A), leg strength (B), skeletal muscle mass (C) and muscle soreness (D) over time. Data is presented as mean with Standard Error of the Mean (SEM). BW = body weight.
Figure 3. Muscle parameters. Changes in handgrip strength (A), leg strength (B), skeletal muscle mass (C) and muscle soreness (D) over time. Data is presented as mean with Standard Error of the Mean (SEM). BW = body weight.
Nutrients 15 00342 g003
Table
Table 1. Nutritional composition of whey, pea and placebo supplements.
Table 1. Nutritional composition of whey, pea and placebo supplements.
NutrientWhey ProteinPea ProteinPlacebo (Maltodextrin with Lemon Flavor)
Energy (kcal/100 g)390382385
Fat (g/100 g)890
Carbohydrate (g/100 g)63.894.8
Of which lactose (g/100 g)600
Protein (g/100)81820
Amino Acid content (g/100 g)
Alanine4.13.60
Arginine2.47.20
Aspartanic Acid9.29.20
Cystine1.90.80
Glutamic Acid12.313.20
Glycine1.73.20
Histidine1.52.00
Isoleucine **4.44.00
Leucine **9.27.20
Lysine7.36.40
Methionine2.10.80
Phenylalanine2.84.80
Proline5.13.60
Serine3.94.40
Threonine4.63.20
Tryptofaan1.20.80
Tyrosine2.43.20
Valine **4.54.40
** Branches Chain Amino Acids (BCAA’s).
Table
Table 2. Baseline characteristics of the total group and specified for the whey-, pea- and placebo supplemented group.
Table 2. Baseline characteristics of the total group and specified for the whey-, pea- and placebo supplemented group.
Total Group
n = 45		Whey Protein
n = 15		Pea Protein
n = 15		Placebo
n = 15
Demographics
Age (years)70 ± 672 ± 569 ± 669 ± 6
Male n (%)36 (80)12 (80)12 (80)12 (80)
Anthropometrics
Body weight (kg)75.4 ± 13.973.9 ± 10.175.8 ± 16.376.4 ± 15.4
Height (m)1.76 ± 0.091.76 ± 0.071.75 ± 0.101.76 ± 0.10
BMI (kg/m2)24.2 ± 2.823.7 ± 2.224.6 ± 3.324.4 ± 2.9
Waist-hip ratio0.97 ± 0.060.98 ± 0.070.97 ± 0.050.97 ± 0.07
Skeletal muscle mass (%)42.5 ± 3.342.6 ± 3.941.5 ± 3.243.4 ± 3.3
Dietary intake
Energy intake (kcal)2078 ± 5282153 ± 5291960 ± 4962123 ± 570
Protein intake (g/kg/d)1.13 ± 0.331.16 ± 0.391.09 ± 0.311.15 ± 0.31
Protein intake (en%)22.0 ± 4.721.8 ± 5.322.1 ± 3.922.0 ± 5.1
Number of participants with a protein intake below 1.0 g/kg/d (n (%))18 (40)5 (33)7 (47)6 (40)
Walking activity
Cumulative walking distance last year (km)645 [1074]800 [1784]280 [520]820 [988]
Walking bout distance (km)24.3 ± 4.923.8 ± 5.423.0 ± 4.426.1 ± 4.8
Walking bout duration bout (h)5.2 ± 1.15.2 ± 1.34.8 ± 1.05.4 ± 1.0
Data are presented as number (with percentage between brackets) of participants, mean ± SD for parametric data or median with the IQR between square brackets for non-parametric data. Body Mass Index (BMI). Thepercentage skeletal muscle mass was calculated by (skeletal muscle mass/the participant’s bodyweight) × 100. (kg = kilogram; m = meter; m2 = square meter; g = gram, d = day; en% = energy percentage).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Spoelder, M.; Koopmans, L.; Hartman, Y.A.W.; Bongers, C.C.W.G.; Schoofs, M.C.A.; Eijsvogels, T.M.H.; Hopman, M.T.E. Supplementation with Whey Protein, but Not Pea Protein, Reduces Muscle Damage Following Long-Distance Walking in Older Adults. Nutrients 2023, 15, 342. https://doi.org/10.3390/nu15020342

AMA Style

Spoelder M, Koopmans L, Hartman YAW, Bongers CCWG, Schoofs MCA, Eijsvogels TMH, Hopman MTE. Supplementation with Whey Protein, but Not Pea Protein, Reduces Muscle Damage Following Long-Distance Walking in Older Adults. Nutrients. 2023; 15(2):342. https://doi.org/10.3390/nu15020342

Chicago/Turabian Style

Spoelder, Marcia, Lotte Koopmans, Yvonne A. W. Hartman, Coen C. W. G. Bongers, Merle C. A. Schoofs, Thijs M. H. Eijsvogels, and Maria T. E. Hopman. 2023. "Supplementation with Whey Protein, but Not Pea Protein, Reduces Muscle Damage Following Long-Distance Walking in Older Adults" Nutrients 15, no. 2: 342. https://doi.org/10.3390/nu15020342

APA Style

Spoelder, M., Koopmans, L., Hartman, Y. A. W., Bongers, C. C. W. G., Schoofs, M. C. A., Eijsvogels, T. M. H., & Hopman, M. T. E. (2023). Supplementation with Whey Protein, but Not Pea Protein, Reduces Muscle Damage Following Long-Distance Walking in Older Adults. Nutrients, 15(2), 342. https://doi.org/10.3390/nu15020342

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop