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Effect of regular exercise training on platelet function in patients with cardiovascular disease and healthy individuals: A systematic review

  • Jacobina Kristiansen
    Affiliations
    Department of Medicine, National Hospital of the Faroe Islands, Tórshavn, Faroe Islands

    Department of Clinical Biochemistry, Aarhus University Hospital, Aarhus, Denmark

    Department of Cardiology, Aarhus University Hospital, Aarhus, Denmark

    Department of Clinical Medicine, Faculty of Health, Aarhus University, Aarhus, Denmark

    Faculty of Health, University of the Faroe Islands, Tórshavn, Faroe Islands
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  • Erik L. Grove
    Correspondence
    Corresponding author at: Department of Cardiology, Aarhus University Hospital, 8200 Aarhus N, Denmark.
    Affiliations
    Department of Cardiology, Aarhus University Hospital, Aarhus, Denmark

    Department of Clinical Medicine, Faculty of Health, Aarhus University, Aarhus, Denmark
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  • Oliver Buchhave Pedersen
    Affiliations
    Department of Clinical Biochemistry, Aarhus University Hospital, Aarhus, Denmark

    Department of Cardiology, Aarhus University Hospital, Aarhus, Denmark

    Department of Clinical Medicine, Faculty of Health, Aarhus University, Aarhus, Denmark
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  • Steen D. Kristensen
    Affiliations
    Department of Cardiology, Aarhus University Hospital, Aarhus, Denmark

    Department of Clinical Medicine, Faculty of Health, Aarhus University, Aarhus, Denmark
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  • Anne-Mette Hvas
    Affiliations
    Department of Clinical Medicine, Faculty of Health, Aarhus University, Aarhus, Denmark
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Open AccessPublished:December 30, 2022DOI:https://doi.org/10.1016/j.thromres.2022.12.017

      Abstract

      Introduction

      Regular exercise training is essential in prevention and treatment of cardiovascular disease (CVD), yet the beneficial effects of exercise remain only partly explained. Platelets play a key role in CVD and may be affected by regular exercise training. We aimed to systematically summarise studies investigating the effect of regular exercise training on platelet function in patients with CVD and in healthy individuals.

      Methods

      Studies were identified by PubMed, Embase and Web of Science May 16, 2022. We selected studies investigating markers of platelet function in relation to regular exercise training in patients with CVD and in healthy individuals. Regular exercise was defined as exercise training for four weeks or more.

      Results

      Of the included studies, 11 investigated patients with CVD and 29 were on healthy individuals. Studies were heterogeneous regarding design, study population and methodology, and the results were ambiguous. In total, 52 different markers of platelet function were investigated with platelet aggregation, soluble P-selectin, and thromboxane B2 (TXB2) as the most frequently examined. When evaluating between-group changes after regular exercise, two studies found a reduced platelet aggregation in the exercise group whilst three studies did not find a difference between groups. With respect to TXB2, three studies reported a reduction and two studies an increase in the exercise group. There were no between-group differences in the seven studies examining soluble P-selectin.

      Conclusion

      Regular exercise training has no clear impact on platelet function in patients with CVD or healthy individuals.

      Prospero registration

      CRD42022350539.

      Abbreviations:

      6-keto-PGF1α (plasma 6-keto-prostaglandin F1α), AA (arachidonic acid), ADMA (asymmetrical dimethyl arginine), ADP (adenosine diphosphate), CAD (coronary artery disease), CD40L (plasma CD40 ligand), COL (collagen), CVD (cardiovascular disease), EPI (epinephrine), L-arg (L-arginine levels), MPA (monocyte-platelet aggregates), MPV (mean platelet volume), PLT (platelet count), PCT (platelet crit (PLT × MPV / 10,000)), PDGF (platelet derived growth factor beta-1), PDW (platelet distribution width), PRISMA (preferred reporting items for systematic reviews and meta-analyses), P-sel (P-selectin), RCT (randomised controlled trial), S1P (sphingosine-1-phosphate), SA1P (sphinganine-1-phosphate), sICAM-1 (soluble intercellular adhesion molecule-1), SDMA (symmetrical dimethyl arginine), sE-sel (soluble-E-selectin), SphK (sphingosine kinase activity), sP-selectin (soluble-P-selectin), sVCAM-1 (soluble vascular cell adhesion molecule-1), TRAP (thrombin receptor activating peptide), TXA2 (thromboxane A2), TXB2 (thromboxane B2), VCAM-1 (vascular cell adhesion molecule-1), VEGF (vascular endothelial growth factor), VO2max (maximal aerobic capacity), vWf (von Willebrand factor)

      Keywords

      1. Introduction

      Cardiovascular disease (CVD) is the leading cause of death worldwide [
      World Health Organization
      Cardiovascular diseases (CVDs).
      ]. Regular exercise training has a high priority in the prevention and treatment of CVD and has been shown to reduce cardiovascular death and rehospitalisation in patients with coronary artery disease (CAD) [
      • Pelliccia A.
      • Sharma S.
      • Gati S.
      • et al.
      2020 ESC guidelines on sports cardiology and exercise in patients with cardiovascular disease.
      ,
      • Dibben G.
      • Faulkner J.
      • Oldridge N.
      • et al.
      Exercise-based cardiac rehabilitation for coronary heart disease.
      ]. In peripheral artery disease, regular exercise training is among first line treatments in order to improve limb symptoms and salvage [
      • Aboyans V.
      • Ricco J.B.
      • Bartelink M.E.L.
      • et al.
      2017 ESC guidelines on the diagnosis and treatment of peripheral arterial diseases, in collaboration with the european Society for Vascular Surgery (ESVS): document covering atherosclerotic disease of extracranial carotid and vertebral, mesenteric, renal, upper and lower extremity arteriesEndorsed by: the european stroke organization (ESO)The task force for the diagnosis and treatment of peripheral arterial diseases of the european Society of Cardiology (ESC) and of the european Society for Vascular Surgery (ESVS).
      ]. The mechanisms explaining the benefits of regular exercise training are only sparsely understood. Regular exercise training has a wide range of potential benefits on cardiovascular risk factors such as hypertension, dyslipidaemia and overweight [
      • Pelliccia A.
      • Sharma S.
      • Gati S.
      • et al.
      2020 ESC guidelines on sports cardiology and exercise in patients with cardiovascular disease.
      ,
      • Alves A.J.
      • Wu Y.
      • Lopes S.
      • et al.
      Exercise to treat hypertension: late breaking news on exercise prescriptions that FITT.
      ,
      • Doewes R.I.
      • Gharibian G.
      • Zadeh F.A.
      An updated systematic review on the effects of aerobic exercise on human blood lipid profile.
      ] and may possibly also have an impact on platelet function. Platelets play a crucial role in the process of coronary thrombus formation [
      • Freynhofer M.K.
      • Bruno V.
      • Wojta J.
      • et al.
      The role of platelets in athero-thrombotic events.
      ,
      • Gremmel T.
      • Frelinger III, A.L.
      • Michelson A.D.
      Platelet physiology.
      ] and thus CVD patients are usually treated with antithrombotic drugs [
      • Dibben G.
      • Faulkner J.
      • Oldridge N.
      • et al.
      Exercise-based cardiac rehabilitation for coronary heart disease.
      ,
      • Giannuzzi P.
      • Mezzani A.
      • Saner H.
      • et al.
      Physical activity for primary and secondary prevention. Position paper of the working group on cardiac rehabilitation and exercise physiology of the european Society of Cardiology.
      ]. Paradoxically, some studies have linked acute exercise to an increased risk of thrombosis [
      • Olsen L.N.
      • Fischer M.
      • Evans P.A.
      Does exercise influence the susceptibility to arterial thrombosis? An integrative perspective.
      ,
      • Posthuma J.J.
      • van der Meijden P.E.
      • Ten Cate H.
      Short- and Long-term exercise induced alterations in haemostasis: a review of the literature.
      ,
      • Hvas A.M.
      • Neergaard-Petersen S.
      Influence of exercise on platelet function in patients with cardiovascular disease.
      ], which may be explained by exercise-induced platelet aggregation and activation of coagulation [
      • Posthuma J.J.
      • van der Meijden P.E.
      • Ten Cate H.
      Short- and Long-term exercise induced alterations in haemostasis: a review of the literature.
      ,
      • Hvas A.M.
      • Neergaard-Petersen S.
      Influence of exercise on platelet function in patients with cardiovascular disease.
      ]. Furthermore, untrained people have a higher risk of cardiovascular events following strenuous exercise [
      • Pelliccia A.
      • Sharma S.
      • Gati S.
      • et al.
      2020 ESC guidelines on sports cardiology and exercise in patients with cardiovascular disease.
      ]. In contrast, regular exercise training may induce changes in the haemostatic system explaining its beneficial effects on cardiovascular health and mortality [
      • Dibben G.
      • Faulkner J.
      • Oldridge N.
      • et al.
      Exercise-based cardiac rehabilitation for coronary heart disease.
      ]. We aimed to systematically review the literature for studies investigating the effect of regular exercise training on platelet function in patients with CVD and in healthy individuals.

      2. Methods

      2.1 Eligibility criteria

      The present review was conducted according to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines [
      • Liberati A.
      • Altman D.G.
      • Tetzlaff J.
      • et al.
      The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration.
      ]. Inclusion criteria were: 1) studies including patients with CVD or healthy individuals, 2) performance of regular exercise training (≥4 weeks), 3) evaluation of platelet function (activation, aggregation, and/or platelet turnover), 4) age ≥18 years, 5) English language, 6) randomised controlled trials, cohort, cross-sectional, or case-control studies. Exclusion criteria were: 1) Studies including individuals with risk factors without established CVD, 2) animals or in vitro studies, 3) guidelines, 4) reviews, 5) letters or editorials without original data, 6) case reports, 7) conference abstracts, 8) studies investigating the effect of pharmacotherapy on platelet function during exercise training 9) records with <10 cases that completed the study. The review was registered at PROSPERO (ID: CRD42022350539).

      2.2 Literature search and data extraction

      Literature search was performed in three different databases: PubMed, Embase and web of science. The literature search was performed on May 16th, 2022. The search string for PubMed was: (“Blood Platelets” (Mesh) OR “platelet” OR “thrombocyte” OR “Platelet Function Test” (Mesh) OR “Platelet Activation” (Mesh)) AND (“Exercise” (Mesh) OR “exercise”), Embase: (“exercise”/exp OR “exercise”) AND (“thrombocyte”/exp OR “thrombocyte”) and for web of science: ALL = (exercise) AND (ALL = (thrombocyte) OR ALL = (platelet)). The searches were without time boundaries. After duplicate screening, 30 random abstracts were independently screened by the first and last author (JK and AMH). JK made the remaining abstract screening using the Covidence systematic review software (Veritas Health Innovation, Melbourne, Australia). JK and AMH evaluated 30 random full-text records to evaluate the study selection. JK evaluated the remaining full-text records for relevance.

      2.3 Data processing

      Included records were divided by population in patients with CAD, ischaemic stroke or peripheral artery disease and healthy individuals. The exercise protocol for each study was presented with focus on weekly frequency, length of training period, and supervision status.

      3. Results

      Fig. 1 shows the flowchart of the literature searches and selection procedure. In total, 8266 records were identified. Before screening, 4178 duplicates were removed. Title and abstract screening was performed on 3312 records of which 3170 were excluded based on inclusion and exclusion criteria. The remaining 142 articles were assessed by full text of which 38 were eligible for inclusion. Furthermore, two additional records were found in the reference list of other studies. Among the included studies, 11 studies included patients with CVD and 29 studies examined healthy individuals. CVD subpopulations included CAD (n = 9) and peripheral artery disease (n = 2).

      3.1 Effect of regular exercise on platelet function in CVD patients and in healthy individuals

      Table 1, Table 2 summarise the characteristics and results of all 40 included studies. The total study population consisted of 2238 individuals: 1072 healthy individuals, 1047 patients with CAD and 119 patients with peripheral artery disease. Out of the 40 included studies, 12 were randomised controlled trials, 21 were cohort studies, 4 were cross-sectional studies and 3 were combined cohort- and cross-sectional studies. Randomised controlled studies were employed in 6 (55 %) of the studies on CVD patients and 6 (21 %) of the studies including healthy individuals. The mean age of patients with CVD was 62 years old, compared to 31 years for healthy individuals. Among studies on patients with CVD, 21 % of patients were women, whereas 33 % of healthy individuals were women. In the included studies, 52 different markers of platelet function were investigated, of which 41 were only measured in a few studies. In Table 3, changes of the 11 markers that were assessed in three or more studies are displayed. Some of the studies reported two different results for the same marker; one result on changes from baseline to after exercise training and another result from the comparison of changes in cases and controls.
      Table 1Studies investigating the effect of regular exercise on platelet function in patients with cardiovascular disease (n = 11).
      Year

      Author

      Ref
      Design

      Study population

      Number of individuals

      Age

      Females
      Exercise protocolBlood samplingPlatelet parametersResults
      2021

      Durmus et al.

      • Durmuş İ.
      • Kalaycıoğlu E.
      • Çetin M.
      • et al.
      Exercise-based cardiac rehabilitation has a strong relationship with mean platelet volume reduction.
      Cohort study

      CAD

      Cases (n = 203)

      Controls (n = 97)

      57 years

      Gender: 23 %

      Aspirin: 98 %

      P2Y12 inhib: 59 %
      5 times weekly

      1.5 months

      Supervised
      Pre

      1.5 months
      MPVCases vs controls:

      • ↓MPV
      2020

      Heber et al.

      • Heber S.
      • Fischer B.
      • Sallaberger-Lehner M.
      • et al.
      Effects of high-intensity interval training on platelet function in cardiac rehabilitation: a randomised controlled trial.
      RCT

      CAD

      Cases (n = 40)

      Controls (n = 42)

      61 years

      Gender: 0 %

      Aspirin: 100 %

      P2Y12 inhib: 100 %
      All:

      4 times weekly

      3 months

      Cases: HIIT+MICT

      Controls: MICT
      Pre

      1.5 months

      3 months
      Flow cytometry (TRAP as agonist): P-sel, CD40L, PNA, GPIIb/IIIa.

      MPV

      PLT
      Cases vs controls:

      • ↓ P-sel
      • ↔ sP-sel
      • ↔ CD40L
      • ↔ PNA
      • ↔ GPIIb/IIIa
      • ↔ MPV
      • ↔ PLT
      2013

      Keating et al.

      • Keating F.K.
      • Schneider D.J.
      • Savage P.D.
      • et al.
      Effect of exercise training and weight loss on platelet reactivity in overweight patients with coronary artery disease.
      RCT

      CAD

      Cases (n = 21)

      Controls (n = 25)

      64 years

      Gender: 24 %

      Aspirin: 98 %

      P2Y12 inhib: 0 %
      5–7 times weekly

      5 months

      Supervised and unsupervised
      Pre

      5 months
      sP-sel expression (ADP agonist)Post vs pre, cases:

      • ↓ sP-sel
      Post vs pre, controls:

      • ↔ sP-sel
      Cases vs controls:

      • ↔ sP-sel
      2006

      Lee et al.

      • Lee K.W.
      • Blann A.D.
      • Jolly K.
      • et al.
      Plasma haemostatic markers, endothelial function and ambulatory blood pressure changes with home versus hospital cardiac rehabilitation: the Birmingham rehabilitation uptake maximisation study.
      RCT

      CAD

      Cases (n = 81)

      Controls (n = 20)

      60 years

      Gender: 19 %

      Aspirin: 98 %

      P2Y12 inhib: 13 %
      2 times weekly

      3 months

      Supervised vs unsupervised
      Pre

      3 months
      sP-sel

      vWf
      Post vs pre, cases:

      • ↔ sP-sel
      • ↓ vWf
      Post vs pre, controls:

      • ↔ sP-sel
      • ↓ vWf
      Cases vs controls:

      • ↔ sP-sel
      • ↔ vWf
      2021

      Liang et al.

      • Liang G.
      • Huang X.
      • Hirsch J.
      • et al.
      Modest gains after an 8-week exercise program correlate with reductions in non-traditional markers of cardiovascular risk.
      Cohort study

      CAD

      Cases (n = 35)

      Controls (n = 17)

      67 years

      Gender: 8 %

      Aspirin: 36 %

      P2Y12 inhib: 20 %
      2 months

      Supervised vs unsupervised
      Pre

      2 months
      PDGFPost vs pre, cases:

      • ↓ PDGF
      Post vs pre, controls:

      • ↔ PDGF
      Cases vs controls:

      • ↓ PDGF
      2011, Munk et al.

      • Munk P.S.
      • Breland U.M.
      • Aukrust P.
      • et al.
      High intensity interval training reduces systemic inflammation in post-PCI patients.
      RCT

      CAD

      Cases (n = 18)

      Controls (n = 18)

      60 years

      Gender: 17 %

      Aspirin: 100 %

      P2Y12 inhib: 100 %
      3 times weekly

      6 months

      Supervised
      Pre

      6 months
      sE-sel

      VCAM-1

      vWF

      sP-sel

      CD4-Ligand
      Post vs pre, cases:

      • ↑ sE-sel
      • ↑ VCAM-1
      • ↔ vWf
      • ↔ sP-sel
      • ↔ CD40-ligand
      Post vs pre, controls:

      • ↑ E-sel
      • ↔ VCAM-1
      • ↑ vWf
      • ↔ sP-sel
      • ↔ CD4-ligand
      Cases vs controls:

      • ↔ all parameters
      1992

      Suzuki et al.

      • Suzuki T.
      • Yamauchi K.
      • Yamada Y.
      • et al.
      Blood coagulability and fibrinolytic activity before and after physical training during the recovery phase of acute myocardial infarction.
      Cohort study

      CAD

      Cases (n = 56)

      Controls (n = 30)

      60 years

      Gender: 13 %

      Aspirin: 51 %

      P2Y12 inhib: 43 %
      6 times weekly

      1 month

      Supervised
      Pre 1 monthPLT

      vWf antigen
      Post vs pre, cases:

      • ↓ PLT
      • ↓ vWf Antigen
      Post vs pre, controls:

      • ↑ PLT
      • ↔ vWf Antigen
      Cases vs controls:

      • ↓ PLT
      • ↔ vWf Antigen
      2017

      Toth-Zsamboki et al.

      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      Cohort study

      CAD

      Cases (n = 84)

      Controls (n = 51)

      61 years

      Gender: 22 %

      Aspirin: 33 %

      P2Y12 inhib: 20 %
      5 times weekly

      3 months

      Supervised vs unsupervised
      Pre

      3 months
      PLT

      MPV

      Platelet aggregation (COL, ADP, EPI and AA as agonists)

      PDGF

      Platelet micro particles
      Post vs pre, cases:

      • ↑ PLT
      • ↔ MPV
      • ↓ Platelet aggregation (COL, ADP, EPI)
      • ↔ Platelet aggregation (AA)
      • ↓ PDGF
      • ↓ Platelet micro particles
      Post vs pre, controls:

      • ↑ PLT
      • ↔ MPV
      • ↔ Platelet aggregation (COL, ADP, AA)
      • ↓ Platelet aggregation (EPI)
      • ↔ PDGF
      • ↔ Platelet micro particles
      2009

      Vona et al.

      • Vona M.
      • Codeluppi G.M.
      • Iannino T.
      • et al.
      Effects of different types of exercise training followed by detraining on endothelium-dependent dilation in patients with recent myocardial infarction.
      RCT

      CAD

      Cases (n = 159)

      Controls (n = 50)

      57 years

      Gender: 26 %

      Aspirin: 100 %

      P2Y12 inhib: NR
      4 times weekly

      1 month

      Supervised
      Pre

      1 month
      vWfPost vs pre, cases:

      • ↓ vWf
      Post vs pre, controls:

      • ↔ vWf
      2017

      Januszek et al.

      • Januszek R.
      • Mika P.
      • Nowobilski R.
      • et al.
      Soluble endoglin as a prognostic factor of the claudication distance improvement in patients with peripheral artery disease undergoing supervised treadmill training program.
      Cohort study

      Intermittent claudication (n = 66)

      65 years

      Gender: 38 %

      Aspirin: NR

      P2Y12 inhib: NR
      3 months

      Supervised
      Pre

      3 months
      PDGF AA

      PDGF AB/BB
      Post vs pre:

      • ↔ PDGF AA
      • ↔ PDGF AB/BB
      2012

      Schlager et al.

      • Schlager O.
      • Hammer A.
      • Giurgea A.
      Impact of exercise training on inflammation and platelet activation in patients with intermittent claudication.
      RCT

      Intermittent claudication: cases (n = 27)

      Controls (n = 26)

      70 years

      Gender: 38 %

      Aspirin: 85 %

      P2Y12 inhib: 40 %
      2 times weekly

      6 months

      Supervised
      Pre

      3 months

      6 months

      12 months
      sP-sel

      MPA
      Post vs pre, cases:

      • ↔ sP-sel
      • ↔ MPA
      Post vs pre, controls:

      • ↔ sP-sel
      • ↔ MPA
      Cases vs controls:

      • ↔ sP-sel
      • ↔ MPA
      Studies evaluating two or more subgroups were labelled as cases and controls. Cases were defined as the group who exercised. If both groups exercised, the population termed cases exercised more than controls and we only presented the exercise protocol for the case group.
      Abbreviations: AA: arachidonic acid, ADP: adenosine 5′diphosphate, CAD: coronary artery disease, COL: collagen, EPI: epinephrine, Inhib: inhibitor, HIIT: high-intensity interval training, MICT: moderate-intensity continuous training, MPA: monocyte-platelet aggregates, MPV: mean platelet volume, PDGF: platelet derived growth factor beta-1, PLT: platelet count, PNA: platelet–neutrophil aggregates, P-sel: P-selectin, RCT: Randomised controlled trial, sE-sel: soluble E-selectin, sP-sel: soluble P-selectin, VCAM-1: vascular cell adhesion molecule-1, vWf: von Willebrand factor.
      Table 2Studies investigating the effect of regular exercise on platelet function in healthy individuals (n = 29).
      Year, author

      Ref.
      Design

      Study population

      Number of patients

      Age

      Gender (%females)
      Exercise protocolBlood samplingPlatelet analysisResults
      1991, Ågren et al.

      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      RCT

      Cases (n = 27)

      Controls (n = 23)

      21 years

      Gender: 100 %
      3 times weekly

      3.5 months

      Unsupervised
      Pre

      3.5 months
      Platelet aggregation (ADP as agonist)

      TXB2

      6-Keto-PGF
      Post vs pre, cases:

      • ↔ Platelet aggregation (ADP), TXB2, 6-keto-PGF
      Post vs pre, controls:

      • ↔ Platelet aggregation (ADP), TXB2, 6-keto-PGF
      Cases vs controls:

      • ↔ Platelet aggregation (ADP), TXB2, 6-keto-PGF
      2017, Bachero-Mena et al.

      • Bachero-Mena B.
      • Pareja-Blanco F.
      • Gonzalez-Badillo J.J.
      Enhanced strength and sprint levels, and changes in blood parameters during a complete athletics season in 800m high-level athletes.
      Cohort study

      Active (n = 13)

      23 years

      Gender 0 %
      Daily

      8 months

      NR
      Pre

      4 months

      8 months
      PLT

      MPV
      8 months vs pre:

      • ↑ MPV
      • ↔ PLT
      8 months vs 4 months:

      • ↑ MPV
      • ↔ PLT
      4 months vs pre:

      • ↔ MPV
      • ↔ PLT
      2017, Bittencourt et al.

      • Bittencourt C.R.O.
      • Izar M.C.O.
      • França C.N.
      • et al.
      Effects of chronic exercise on endothelial progenitor cells and microparticles in professional runners.
      Cross-sectional study

      Cases (n = 25)

      Controls (n = 24)

      NR

      NR
      Daily

      NR
      Single time pointPlatelet micro particlesCases vs controls:

      • ↔ Platelet micro particles
      2019, Boyali et al.

      • Boyali E.
      • Sevindi T.
      • Yuksel M.F.
      • et al.
      The effects of preparation period exercises on the hematological parameters of the taekwondo athletes.
      Cohort study

      Active (n = 21)

      20 years

      Gender: 57 %
      5 times weekly

      2 months

      NR
      Pre

      2 months
      PLT

      MPV

      PCT

      PDW
      Post vs pre:

      • ↔ PLT
      • ↓ MPV
      • ↓ PCT
      • ↔ PDW
      1996, Burri et al.

      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      Cohort study

      Inactive (n = 10)

      28 years

      Gender: 100 %
      6 times weekly

      3 months

      Supervised
      Pre

      1.5 months

      3 months
      PLT

      Platelet aggregation (ADP, COL and EPI as agonists)
      1.5 months vs pre:

      • ↔ PLT
      • ↓ Platelet aggregation (COL)
      • ↔ Platelet aggregation (ADP, EPI)
      3 months vs 1.5 months:

      • ↔ PLT
      • ↑ Platelet aggregation (ADP, COL)
      • ↔ Platelet aggregation (EPI)
      3 months vs pre:

      • ↓ PLT
      • ↔ Platelet aggregation (ADP, EPI)
      • ↓ Platelet aggregation (COL)
      2004, Coppola et al.

      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      Cohort study

      Cases (n = 15)

      Controls (n = 15)

      43 years

      Gender: 27 %
      3 times weekly for 3 months

      Supervised
      Pre

      3 months
      PLT

      Platelet aggregation (ADP as agonist)
      Post vs pre, cases:

      • ↔ PLT
      • ↓ Platelet aggregation (ADP)
      Cases vs controls:

      • ↔ PLT
      • ↔ Platelet aggregation (ADP)
      2004, Di Massimo et al.

      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      Cohort study

      Inactive (n = 12)

      25 years

      Gender: 0 %
      3 times weekly 5 months

      Supervised
      Pre

      5 months
      Platelet aggregation (ADP and COL as agonists)

      NOx level
      Post vs pre:

      • ↓ Platelet aggregation (ADP)
      • ↓ Platelet aggregation (COL)
      • ↑ NOx
      2020, Erdogan et al.

      • Erdogan R.
      Effects of endurance workouts on thyroid hormone metabolism and biochemical markers in athletes.
      Cohort study

      Active (n = 16)

      NR

      Gender: 0 %
      3 times weekly for 3 months

      Supervised
      Pre

      3 months
      PLT

      PCT

      MPV

      PDW
      Post vs pre:

      • ↔ PLT
      • ↔ PCT
      • ↑ MPV
      • ↑ PDW
      2018, Haynes et al.

      • Haynes A.
      • Linden M.D.
      • Robey E.
      Beneficial impacts of regular exercise on platelet function in sedentary older adults: evidence from a randomized 6-mo walking trial.
      RCT

      Cases (n = 14)

      Controls (n = 13)

      60 years

      Gender: 82 %
      3 times weekly for 6 months

      Supervised
      Pre

      6 months
      MPA (ADP, TRAP, AA as agonists)6 months vs pre, cases:

      • ↔ MPA (ADP, TRAP, AA)
      6 months vs pre, controls:

      • ↑ MPA (ADP)
      • ↔ MPA (TRAP, AA)
      Cases vs controls:

      • ↓ MPA (ADP)
      • ↔ MPA (TRAP, AA)
      2016, Heber et al.

      • Heber S.
      • Assinger A.
      • Pokan R.
      • et al.
      Correlation between cardiorespiratory fitness and platelet function in healthy women.
      • A:
        Cross-sectional study
        • Cases (n = 28)
        • Controls (n = 34)
        • 23 years
        • Gender: 100 %
      • B:
        Cohort study
        • Cases (n = 17)
        • Controls (n = 17)
        • NR
        • Gender: 100 %
      • A:
        NR, based on VO2max at inclusion
      • B:
        3 times weekly
        2 months
        Supervised
      • A:
        Single time point
      • B:
        Pre
        2 months
      Flow cytometry (P-sel, CD40L, ROS) [unstimulated and TRAP as agonist]
      • A:
        Cases vs control
        • ↓ P-sel (unstimulated)
        • ↑ P-sel (TRAP)
        • ↔ CD40L (unstimulated)
        • ↑ CD40L (TRAP)
        • ↑ ROS (TRAP)
      • B:
        Post vs pre, cases
        • ↓ P-sel (unstimulated)
        • ↑ P-sel (TRAP)
        • ↔ CD40L (unstimulated)
        • ↓ CD40L (TRAP)
        • ↔ ROS (TRAP)
      • C:
        Post vs pre, controls
        • ↔ P-sel (unstimulated, TRAP)
        • ↔ CD40L (unstimulated, TRAP)
        • ↔ ROS (TRAP)
      2000, Hilberg et al.

      • Hilberg T.
      • Nowacki P.E.
      • Müller-Berghaus G.
      • et al.
      Changes in blood coagulation and fibrinolysis associated with maximal exercise and physical conditioning in women taking low dose oral contraceptives.
      Cohort study

      Cases (n = 24)

      Controls (n = 10)

      22–38 years

      Gender: 100 %
      2 times weekly

      3 months

      NR
      Pre

      3 months
      vWfPost vs pre, cases

      • ↔ vWf
      Cases vs controls

      • ↔ vWf
      1997, Kauffman et al.

      • Kauffman R.D.
      • Sforzo G.S.
      • Frost B.
      • et al.
      The effects of exercise training on resting prostacyclin and thromboxane A(2) in older adults.
      Cohort study

      Cases (n = 10)

      Controls (n = 6)

      66 years

      Gender: 50 %
      3 times weekly

      4 months

      Supervised
      Pre

      4 months
      6-Keto-PGF

      TXB2
      Post vs pre, cases

      • ↓ 6-Keto-PGF
      • ↔ TXB2
      Post vs pre, controls

      • ↓ 6-Keto-PGF
      • ↔ TXB2
      Cases vs controls

      • ↔ 6-Keto-PGF
      • ↑ TXB2
      2018, Książek et al.

      • Książek M.
      • Charmas M.
      • Klusiewicz A.
      • et al.
      Endurance training selectively increases high-density lipoprotein-bound sphingosine-1-phosphate in the plasma.
      Cohort study

      Inactive (n = 17)

      20 years

      Gender: 0 %
      3 times weekly

      2 months

      Supervised
      Pre

      2 months
      Sphingosine

      Sphinganine

      S1P

      SA1P

      Ceramide

      SphK

      PLT
      Post vs pre

      • ↑ Sphingosine
      • ↑ Sphinganine
      • ↔ S1P
      • ↑ SA1P
      • ↔ Ceramide
      • ↑ Sphingosine kinase activity
      • ↔ PLT
      2006, Lippi et al.

      • Lippi G.
      • Montagnana M.
      • Salvagno G.L.
      • et al.
      Comparison of platelet function between sedentary individuals and competitive athletes at rest.
      Cross-sectional study

      Cases (n = 89)

      Controls (n = 43)

      28 years

      Gender: 0 %
      Daily

      NR
      Single time pointPlatelet aggregation (COL-ADP and COL-EPI as agonist)

      vWf
      Cases vs controls:

      • ↓ Platelet aggregation (COL-ADP)
      • ↔ Platelet aggregation (COL-EPI)
      • ↔ vWf
      2018, Lundberg Slingsby et al.

      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      Cross-sectional study

      Cases (n = 14)

      Controls (n = 13)

      52 years

      Gender: 0 %
      2–4 h weekly

      >15 years

      Unsupervised
      Single time pointPlatelet aggregation (AA, ADP, COL, EPI, TRAP, TXA2 as agonists)

      6-Keto PGF
      Cases vs controls:

      • ↓ Platelet aggregation (COL, EPI)
      • ↔ Platelet aggregation (AA, ADP, TRAP6, TXA2)
      • ↔ 6-Keto PGF1α
      2017, Lundberg Slingsby et al.

      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      Cohort study

      Inactive (n = 49)

      51 years

      Gender: 100 %
      3 times weekly

      3 months

      Supervised
      Pre

      3 months
      Platelet aggregation (ADP, EPI, TRAP, TXA2 and COL as agonists)

      6-Keto PGF

      PLT

      MPV
      Post vs pre

      • ↔ 6-Keto PGF
      • ↔ PLT
      • ↔ MPV
      • ↔ Platelet aggregation (ADP, EPI, TRAP, TXA2 and COL)
      2021, Medvedev et al.

      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      The functional characteristics of the organism of physically inactive students who have started regular physical training.
      • A:
        Cross-sectional study
        • Cases (n = 46)
        • Controls (n = 42)
        • 21 years
        • Gender: 0 %
      • B:
        Cohort study
        • Inactive (n = 42)
        • 22 years
        • Gender: 0 %
      • A:
        3 times weekly
        NR
      • B:
        3 times weekly
        6 months
        Unsupervised
      • A:
        Single time point
      • B:
        Pre
        3 months
        6 months
      TXB2

      6-Keto-PGF
      • A:
        Cases vs controls
        • ↓ TXB2
        • ↑ 6-Keto-PGF
      • B:
        3 months vs pre
        • ↔ TXB2
        • ↔ 6-Keto-PGF
      • C:
        6 months vs pre
        • ↓ TXB2
        • ↑ 6-Keto-PGF
      2021, Medvedev et al.

      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      Hematological parameters in mature age men who have begun regular sports walking.
      • A:
        Cross-sectional study
        Cases (n = 35)
        Controls (n = 38)
        48 years
        Gender: 0 %
      • B:
        Cohort study
        Inactive (n = 38)
        48 years
        Gender: 0 %
      • A:
        4 times weekly
        NR
      • B:
        4 times weekly
        6 months
        Unsupervised
      • A:
        Single time point
      • B:
        Pre
        3 months
        6 months
      TXB2

      6-Keto-PGF
      • A:
        Cases vs controls
        • ↓ TXB2
        • ↑ 6-Keto-PGF
      • B:
        3 months vs pre
        • ↔ TXB2
        • ↔ 6-Keto-PGF
      • C:
        6 months vs pre
        • ↓ TXB2
        • ↑ 6-Keto-PGF
      2007, Murakami et al.

      • Murakami T.
      • Horigome H.
      • Tanaka K.
      • et al.
      Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity.
      RCT

      Cases (n = 28)

      Controls (n = 21)

      52 years

      Gender: 48 %
      3 times weekly

      3 months

      Supervised
      Pre

      3 months
      Platelet microparticles3 months vs pre, cases:

      • ↓ Platelet microparticles
      3 months vs pre, controls:

      • ↓ Platelet microparticles
      Cases vs controls:

      • ↔ Platelet microparticles
      2017, Podgórska et al.

      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      Cross-sectional study

      Cases (n = 25)

      Controls (n = 54)

      25 years

      Gender: 0 %
      Daily

      Supervised
      Single time pointPlatelet aggregation (AA and ADP as agonists)

      6-Keto-PGF TXB2

      Soluble markers (sP-Sel, VEGF, sICAM-1, sVCAM-1, sE-Sel, ADMA, SDMA, L-arg, Serpin E1)
      Cases vs controls:

      • ↔ Platelet aggregation (AA and ADP)
      • ↓ TXB2
      • ↔ 6-Keto-PGF
      • ↓ sICAM-1
      • ↔ sP-Sel, VEGF, sVCAM-1, sE-Sel, ADMA, SDMA, L-arg, Serpin E1
      1993, Ponjee et al.

      • Ponjee G.A.
      • Janssen E.M.
      • van Wersch J.W.
      Prolonged physical conditioning and blood platelet release markers: a longitudinal study.
      Cohort study

      Inactive (n = 34)

      37 years

      Gender: 41 %
      3 times weekly

      9 months

      Supervised
      Pre

      6 months

      9 months
      Platelet factor 4

      β-Thrombo-globulin
      6 months vs pre:

      • ↑ Plasma platelet factor 4
      • ↔ β-Thromboglobulin
      9 months vs pre

      • ↑ Plasma platelet factor 4
      • ↔ β-Thromboglobulin
      2013, Santilli et al.

      • Santilli F.
      • Vazzana N.
      • Iodice P.
      • et al.
      Effects of high-amount-high-intensity exercise on in vivo platelet activation: modulation by lipid peroxidation and AGE/RAGE axis.
      Cohort study

      Inactive (n = 22)

      51 years

      Gender: 32 %
      2 times weekly

      2 months

      Supervised
      Pre

      2 months
      8-iso-PGF TXB2

      sCD40L

      sP-sel
      2 months vs pre

      • ↓8-iso-PGF
      • ↓ TXB2
      • ↓ sCD40L
      • ↓ s-P-sel
      2018 Tagawa et al.

      • Tagawa K.
      • Ra S.G.
      • Kumagai H.
      • et al.
      Resistance training-induced decreases in central arterial compliance is associated with increases in serum thromboxane B-2 concentrations in young men.
      Cohort study

      Cases (n = 17)

      Controls (n = 7)

      25 years

      Gender: 0 %
      3 times weekly 1 month

      Supervised
      Pre

      1 month
      TXB2Post vs pre, cases:

      • ↑ TXB2
      Post vs pre, controls:

      • ↔ TXB2
      Cases vs controls:

      • ↑ TXB2 in cases
      2011 Trenerry et al.

      • Trenerry M.K.
      • Della Gatta P.A.
      • Larsen A.E.
      • et al.
      Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men.
      Cohort study

      Active (n = 13)

      19 years

      Gender: 0 %
      3 times weekly 3 months

      Supervised
      Pre

      3 months
      VEGFPost vs pre:

      • ↔ VEGF
      2004 Wang et al.

      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      Cohort study

      Inactive (n = 10)

      22 years

      Gender: 0 %
      5 times weekly 2 months

      Supervised
      Pre

      2 months
      PLT

      Platelet aggregation (ADP as agonist)

      Platelet [Ca2+]I (unstimulated and ADP)
      Post vs pre:

      • ↔ PLT
      • ↓ Platelet aggregation (ADP)
      • ↓ [Ca2+]I (unstimulated, ADP)
      1997 Wang et al.

      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      RCT

      Cases (n = 8)

      Controls (n = 8)

      22 years

      Gender: 100 %
      5 times weekly 2 months

      Supervised
      Pre

      2 months
      Platelet adhesiveness

      Platelet aggregation (ADP as agonist)

      Platelet [Ca2+]I (unstimulated and ADP)

      Platelet cGMP
      Post vs pre, cases:

      • ↓ Platelet adhesiveness
      • ↓ Platelet aggregation (ADP)
      • ↓ [Ca2+]I (unstimulated, ADP)
      • ↑ cGMP
      Post vs pre, controls:

      • ↔ Platelet adhesiveness
      • ↔ Platelet aggregation (ADP)
      • ↔ [Ca2+]I (unstimulated, ADP)
      • ↔ cGMP
      Cases vs controls:

      • ↓ Platelet adhesiveness
      • ↓ Platelet aggregation (ADP)
      • ↓ [Ca2+]I (unstimulated, ADP)
      • ↑ cGMP
      1995 Wang et al.

      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      RCT

      Cases (n = 11)

      Controls (n = 12)

      21 years

      Gender: 0 %
      5 times weekly 2 months

      Supervised
      Pre

      2 months
      Platelet adhesiveness

      Platelet aggregation (ADP as agonist)
      Post vs pre, cases:

      • ↓ Platelet adhesiveness
      • ↓ Platelet aggregation (ADP)
      Post vs pre, controls:

      • ↔ Platelet adhesiveness
      • ↔ Platelet aggregation (ADP)
      Cases vs controls:

      • ↓ Platelet adhesiveness
      • ↔ Platelet aggregation (ADP)
      2005 Wang et al.

      • Wang J.S.
      • Li Y.S.
      • Chen J.C.
      • et al.
      Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men.
      RCT

      Cases (n = 15)

      Controls (n = 15)

      24 years

      Gender: 0 %
      5 times weekly 2 months

      Supervised
      Pre

      2 months
      Platelet aggregation (induced by shear stress)

      sP-sel

      vWf
      Post vs pre, cases:

      • ↓ Platelet aggregation
      • ↓ vWf
      • ↔ sP-sel
      Post vs pre, controls:

      • ↔ Platelet aggregation
      • ↔ vWf
      • ↔ sP-sel
      Cases vs controls:

      • ↓ Platelet aggregation
      • ↓ vWf
      • ↔ sP-sel
      2010 Zoladz et al.

      • Zoladz J.A.
      • Majerczak J.
      • Duda K.
      • et al.
      Endurance training increases exercise-induced prostacyclin release in young, healthy men - relationship with VO2max.
      Cohort study

      Inactive (n = 12)

      23 years

      Gender: 0 %
      4 times weekly 1 month

      Supervised
      Pre

      1 month
      6-Keto-PGFPost vs pre:

      • ↔ 6-Keto-PGF
      Cohort studies investigating one group only were labelled active or inactive describing their level of physical activity at inclusion. Studies evaluating two or more subgroups were labelled as cases and controls. Cases were defined as the group who exercised. If both groups exercised, the population termed cases exercised more than controls and we only presented the exercise protocol for the case group.
      Abbreviations: 6-keto-PGF: plasma 6-keto-prostaglandin F, AA: arachidonic acid, ADMA: asymmetrical dimethyl arginine, ADP: adenosine 5′diphosphate, CD40L: plasma CD40 ligand, COL: collagen, EPI: epinephrine, L-arg: L-arginine levels, MPA: monocyte-platelet aggregates, MPV: mean platelet volume, NR: not reported, PLT: platelet count, PCT: platelet crit (PLT × MPV / 10,000), PDW: platelet distribution width, RCT: randomised controlled trial, S1P: sphingosine-1-phosphate, SA1P: sphinganine-1-phosphate, sICAM-1: soluble intercellular adhesion molecule-1, SDMA: symmetrical dimethyl arginine, sE-sel: soluble-E-selectin, SphK: sphingosine kinase activity, sP-selectin: soluble-P-selectin, sVCAM-1: soluble vascular cell adhesion molecule-1, TRAP: thrombin receptor activating peptide, TXA2: thromboxane A2, TXB2: thromboxane B2, VEGF: vascular endothelial growth factor, VO2max: maximal aerobic capacity, vWf: von Willebrand factor.
      Table 3Alteration in platelet function following regular exercise training from baseline to after exercise intervention (within-group) and comparing cases and controls (between-group).
      MarkerHealthy individualsCardiovascular disease
      Within-groupBetween-groupWithin-groupBetween-group
      Platelet aggregation (ADP)
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.


      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.


      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      Platelet aggregation (COL)
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.


      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      Platelet aggregation (EPI)
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      TXB2
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      The functional characteristics of the organism of physically inactive students who have started regular physical training.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      Hematological parameters in mature age men who have begun regular sports walking.
      ,
      • Santilli F.
      • Vazzana N.
      • Iodice P.
      • et al.
      Effects of high-amount-high-intensity exercise on in vivo platelet activation: modulation by lipid peroxidation and AGE/RAGE axis.


      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Kauffman R.D.
      • Sforzo G.S.
      • Frost B.
      • et al.
      The effects of exercise training on resting prostacyclin and thromboxane A(2) in older adults.


      • Tagawa K.
      • Ra S.G.
      • Kumagai H.
      • et al.
      Resistance training-induced decreases in central arterial compliance is associated with increases in serum thromboxane B-2 concentrations in young men.
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      The functional characteristics of the organism of physically inactive students who have started regular physical training.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      Hematological parameters in mature age men who have begun regular sports walking.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.


      • Kauffman R.D.
      • Sforzo G.S.
      • Frost B.
      • et al.
      The effects of exercise training on resting prostacyclin and thromboxane A(2) in older adults.
      ,
      • Tagawa K.
      • Ra S.G.
      • Kumagai H.
      • et al.
      Resistance training-induced decreases in central arterial compliance is associated with increases in serum thromboxane B-2 concentrations in young men.
      6-Keto-PGF
      • Kauffman R.D.
      • Sforzo G.S.
      • Frost B.
      • et al.
      The effects of exercise training on resting prostacyclin and thromboxane A(2) in older adults.


      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ,
      • Zoladz J.A.
      • Majerczak J.
      • Duda K.
      • et al.
      Endurance training increases exercise-induced prostacyclin release in young, healthy men - relationship with VO2max.


      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      The functional characteristics of the organism of physically inactive students who have started regular physical training.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      Hematological parameters in mature age men who have begun regular sports walking.
      • Kauffman R.D.
      • Sforzo G.S.
      • Frost B.
      • et al.
      The effects of exercise training on resting prostacyclin and thromboxane A(2) in older adults.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.


      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      The functional characteristics of the organism of physically inactive students who have started regular physical training.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      Hematological parameters in mature age men who have begun regular sports walking.
      Mean platelet volume
      • Boyali E.
      • Sevindi T.
      • Yuksel M.F.
      • et al.
      The effects of preparation period exercises on the hematological parameters of the taekwondo athletes.


      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.


      • Bachero-Mena B.
      • Pareja-Blanco F.
      • Gonzalez-Badillo J.J.
      Enhanced strength and sprint levels, and changes in blood parameters during a complete athletics season in 800m high-level athletes.
      ,
      • Erdogan R.
      Effects of endurance workouts on thyroid hormone metabolism and biochemical markers in athletes.
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      • Durmuş İ.
      • Kalaycıoğlu E.
      • Çetin M.
      • et al.
      Exercise-based cardiac rehabilitation has a strong relationship with mean platelet volume reduction.


      • Heber S.
      • Fischer B.
      • Sallaberger-Lehner M.
      • et al.
      Effects of high-intensity interval training on platelet function in cardiac rehabilitation: a randomised controlled trial.
      Platelet count
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.


      • Bachero-Mena B.
      • Pareja-Blanco F.
      • Gonzalez-Badillo J.J.
      Enhanced strength and sprint levels, and changes in blood parameters during a complete athletics season in 800m high-level athletes.
      ,
      • Boyali E.
      • Sevindi T.
      • Yuksel M.F.
      • et al.
      The effects of preparation period exercises on the hematological parameters of the taekwondo athletes.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Erdogan R.
      Effects of endurance workouts on thyroid hormone metabolism and biochemical markers in athletes.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      • Suzuki T.
      • Yamauchi K.
      • Yamada Y.
      • et al.
      Blood coagulability and fibrinolytic activity before and after physical training during the recovery phase of acute myocardial infarction.


      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      • Suzuki T.
      • Yamauchi K.
      • Yamada Y.
      • et al.
      Blood coagulability and fibrinolytic activity before and after physical training during the recovery phase of acute myocardial infarction.


      • Heber S.
      • Fischer B.
      • Sallaberger-Lehner M.
      • et al.
      Effects of high-intensity interval training on platelet function in cardiac rehabilitation: a randomised controlled trial.
      Micro particles
      • Murakami T.
      • Horigome H.
      • Tanaka K.
      • et al.
      Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity.
      • Bittencourt C.R.O.
      • Izar M.C.O.
      • França C.N.
      • et al.
      Effects of chronic exercise on endothelial progenitor cells and microparticles in professional runners.
      ,
      • Murakami T.
      • Horigome H.
      • Tanaka K.
      • et al.
      Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity.
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      vWf
      • Wang J.S.
      • Li Y.S.
      • Chen J.C.
      • et al.
      Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men.


      • Hilberg T.
      • Nowacki P.E.
      • Müller-Berghaus G.
      • et al.
      Changes in blood coagulation and fibrinolysis associated with maximal exercise and physical conditioning in women taking low dose oral contraceptives.
      • Wang J.S.
      • Li Y.S.
      • Chen J.C.
      • et al.
      Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men.


      • Hilberg T.
      • Nowacki P.E.
      • Müller-Berghaus G.
      • et al.
      Changes in blood coagulation and fibrinolysis associated with maximal exercise and physical conditioning in women taking low dose oral contraceptives.
      ,
      • Lippi G.
      • Montagnana M.
      • Salvagno G.L.
      • et al.
      Comparison of platelet function between sedentary individuals and competitive athletes at rest.
      • Lee K.W.
      • Blann A.D.
      • Jolly K.
      • et al.
      Plasma haemostatic markers, endothelial function and ambulatory blood pressure changes with home versus hospital cardiac rehabilitation: the Birmingham rehabilitation uptake maximisation study.
      ,
      • Suzuki T.
      • Yamauchi K.
      • Yamada Y.
      • et al.
      Blood coagulability and fibrinolytic activity before and after physical training during the recovery phase of acute myocardial infarction.
      ,
      • Vona M.
      • Codeluppi G.M.
      • Iannino T.
      • et al.
      Effects of different types of exercise training followed by detraining on endothelium-dependent dilation in patients with recent myocardial infarction.


      • Munk P.S.
      • Breland U.M.
      • Aukrust P.
      • et al.
      High intensity interval training reduces systemic inflammation in post-PCI patients.
      • Lee K.W.
      • Blann A.D.
      • Jolly K.
      • et al.
      Plasma haemostatic markers, endothelial function and ambulatory blood pressure changes with home versus hospital cardiac rehabilitation: the Birmingham rehabilitation uptake maximisation study.
      ,
      • Munk P.S.
      • Breland U.M.
      • Aukrust P.
      • et al.
      High intensity interval training reduces systemic inflammation in post-PCI patients.
      ,
      • Suzuki T.
      • Yamauchi K.
      • Yamada Y.
      • et al.
      Blood coagulability and fibrinolytic activity before and after physical training during the recovery phase of acute myocardial infarction.
      sP-selectin
      • Santilli F.
      • Vazzana N.
      • Iodice P.
      • et al.
      Effects of high-amount-high-intensity exercise on in vivo platelet activation: modulation by lipid peroxidation and AGE/RAGE axis.


      • Wang J.S.
      • Li Y.S.
      • Chen J.C.
      • et al.
      Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men.
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      ,
      • Wang J.S.
      • Li Y.S.
      • Chen J.C.
      • et al.
      Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men.
      • Keating F.K.
      • Schneider D.J.
      • Savage P.D.
      • et al.
      Effect of exercise training and weight loss on platelet reactivity in overweight patients with coronary artery disease.


      • Lee K.W.
      • Blann A.D.
      • Jolly K.
      • et al.
      Plasma haemostatic markers, endothelial function and ambulatory blood pressure changes with home versus hospital cardiac rehabilitation: the Birmingham rehabilitation uptake maximisation study.
      ,
      • Munk P.S.
      • Breland U.M.
      • Aukrust P.
      • et al.
      High intensity interval training reduces systemic inflammation in post-PCI patients.
      ,
      • Schlager O.
      • Hammer A.
      • Giurgea A.
      Impact of exercise training on inflammation and platelet activation in patients with intermittent claudication.
      • Keating F.K.
      • Schneider D.J.
      • Savage P.D.
      • et al.
      Effect of exercise training and weight loss on platelet reactivity in overweight patients with coronary artery disease.
      ,
      • Lee K.W.
      • Blann A.D.
      • Jolly K.
      • et al.
      Plasma haemostatic markers, endothelial function and ambulatory blood pressure changes with home versus hospital cardiac rehabilitation: the Birmingham rehabilitation uptake maximisation study.
      ,
      • Munk P.S.
      • Breland U.M.
      • Aukrust P.
      • et al.
      High intensity interval training reduces systemic inflammation in post-PCI patients.
      ,
      • Schlager O.
      • Hammer A.
      • Giurgea A.
      Impact of exercise training on inflammation and platelet activation in patients with intermittent claudication.
      ,
      • Heber S.
      • Fischer B.
      • Sallaberger-Lehner M.
      • et al.
      Effects of high-intensity interval training on platelet function in cardiac rehabilitation: a randomised controlled trial.
      PDGF
      • Liang G.
      • Huang X.
      • Hirsch J.
      • et al.
      Modest gains after an 8-week exercise program correlate with reductions in non-traditional markers of cardiovascular risk.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.


      • Januszek R.
      • Mika P.
      • Nowobilski R.
      • et al.
      Soluble endoglin as a prognostic factor of the claudication distance improvement in patients with peripheral artery disease undergoing supervised treadmill training program.
      • Liang G.
      • Huang X.
      • Hirsch J.
      • et al.
      Modest gains after an 8-week exercise program correlate with reductions in non-traditional markers of cardiovascular risk.
      Only platelet activity and aggregation markers examined in at least three studies across study populations are presented.
      ↑: Higher after exercise or higher in exercise group (cases) than controls.
      ↓: Lower after exercise or lower in exercise group (cases) than controls.
      ↔: Unchanged after exercise or no difference between exercise group (cases) and controls.
      If markers were measured more than twice during the intervention, we only included comparison between baseline and post intervention blood samples in this table.
      Abbreviations: ADP: adenosine diphosphate, COL: collagen, EPI: epinephrine, PDGF: platelet derived growth factor beta, TXB2: thromboxane B2, vWf: von Willebrand factor.

      3.2 Exercise intervention characteristics

      The included studies were homogeneous concerning the type of exercise intervention. In 38 (95 %) of the studies, aerobic exercise was performed (supervised, unsupervised or retrospectively) [
      • Hilberg T.
      • Nowacki P.E.
      • Müller-Berghaus G.
      • et al.
      Changes in blood coagulation and fibrinolysis associated with maximal exercise and physical conditioning in women taking low dose oral contraceptives.
      ,
      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Bachero-Mena B.
      • Pareja-Blanco F.
      • Gonzalez-Badillo J.J.
      Enhanced strength and sprint levels, and changes in blood parameters during a complete athletics season in 800m high-level athletes.
      ,
      • Bittencourt C.R.O.
      • Izar M.C.O.
      • França C.N.
      • et al.
      Effects of chronic exercise on endothelial progenitor cells and microparticles in professional runners.
      ,
      • Boyali E.
      • Sevindi T.
      • Yuksel M.F.
      • et al.
      The effects of preparation period exercises on the hematological parameters of the taekwondo athletes.
      ,
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Erdogan R.
      Effects of endurance workouts on thyroid hormone metabolism and biochemical markers in athletes.
      ,
      • Haynes A.
      • Linden M.D.
      • Robey E.
      Beneficial impacts of regular exercise on platelet function in sedentary older adults: evidence from a randomized 6-mo walking trial.
      ,
      • Heber S.
      • Assinger A.
      • Pokan R.
      • et al.
      Correlation between cardiorespiratory fitness and platelet function in healthy women.
      ,
      • Kauffman R.D.
      • Sforzo G.S.
      • Frost B.
      • et al.
      The effects of exercise training on resting prostacyclin and thromboxane A(2) in older adults.
      ,
      • Książek M.
      • Charmas M.
      • Klusiewicz A.
      • et al.
      Endurance training selectively increases high-density lipoprotein-bound sphingosine-1-phosphate in the plasma.
      ,
      • Lippi G.
      • Montagnana M.
      • Salvagno G.L.
      • et al.
      Comparison of platelet function between sedentary individuals and competitive athletes at rest.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      The functional characteristics of the organism of physically inactive students who have started regular physical training.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      Hematological parameters in mature age men who have begun regular sports walking.
      ,
      • Murakami T.
      • Horigome H.
      • Tanaka K.
      • et al.
      Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      ,
      • Ponjee G.A.
      • Janssen E.M.
      • van Wersch J.W.
      Prolonged physical conditioning and blood platelet release markers: a longitudinal study.
      ,
      • Santilli F.
      • Vazzana N.
      • Iodice P.
      • et al.
      Effects of high-amount-high-intensity exercise on in vivo platelet activation: modulation by lipid peroxidation and AGE/RAGE axis.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ,
      • Wang J.S.
      • Li Y.S.
      • Chen J.C.
      • et al.
      Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men.
      ,
      • Zoladz J.A.
      • Majerczak J.
      • Duda K.
      • et al.
      Endurance training increases exercise-induced prostacyclin release in young, healthy men - relationship with VO2max.
      ,
      • Durmuş İ.
      • Kalaycıoğlu E.
      • Çetin M.
      • et al.
      Exercise-based cardiac rehabilitation has a strong relationship with mean platelet volume reduction.
      ,
      • Keating F.K.
      • Schneider D.J.
      • Savage P.D.
      • et al.
      Effect of exercise training and weight loss on platelet reactivity in overweight patients with coronary artery disease.
      ,
      • Lee K.W.
      • Blann A.D.
      • Jolly K.
      • et al.
      Plasma haemostatic markers, endothelial function and ambulatory blood pressure changes with home versus hospital cardiac rehabilitation: the Birmingham rehabilitation uptake maximisation study.
      ,
      • Liang G.
      • Huang X.
      • Hirsch J.
      • et al.
      Modest gains after an 8-week exercise program correlate with reductions in non-traditional markers of cardiovascular risk.
      ,
      • Munk P.S.
      • Breland U.M.
      • Aukrust P.
      • et al.
      High intensity interval training reduces systemic inflammation in post-PCI patients.
      ,
      • Suzuki T.
      • Yamauchi K.
      • Yamada Y.
      • et al.
      Blood coagulability and fibrinolytic activity before and after physical training during the recovery phase of acute myocardial infarction.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ,
      • Vona M.
      • Codeluppi G.M.
      • Iannino T.
      • et al.
      Effects of different types of exercise training followed by detraining on endothelium-dependent dilation in patients with recent myocardial infarction.
      ,
      • Januszek R.
      • Mika P.
      • Nowobilski R.
      • et al.
      Soluble endoglin as a prognostic factor of the claudication distance improvement in patients with peripheral artery disease undergoing supervised treadmill training program.
      ,
      • Schlager O.
      • Hammer A.
      • Giurgea A.
      Impact of exercise training on inflammation and platelet activation in patients with intermittent claudication.
      ,
      • Heber S.
      • Fischer B.
      • Sallaberger-Lehner M.
      • et al.
      Effects of high-intensity interval training on platelet function in cardiac rehabilitation: a randomised controlled trial.
      ] whilst 2 (5 %) studies performed a resistance training program [
      • Tagawa K.
      • Ra S.G.
      • Kumagai H.
      • et al.
      Resistance training-induced decreases in central arterial compliance is associated with increases in serum thromboxane B-2 concentrations in young men.
      ,
      • Trenerry M.K.
      • Della Gatta P.A.
      • Larsen A.E.
      • et al.
      Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men.
      ]. Twenty-nine studies (73 %) performed supervised exercise training [
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Erdogan R.
      Effects of endurance workouts on thyroid hormone metabolism and biochemical markers in athletes.
      ,
      • Haynes A.
      • Linden M.D.
      • Robey E.
      Beneficial impacts of regular exercise on platelet function in sedentary older adults: evidence from a randomized 6-mo walking trial.
      ,
      • Heber S.
      • Assinger A.
      • Pokan R.
      • et al.
      Correlation between cardiorespiratory fitness and platelet function in healthy women.
      ,
      • Kauffman R.D.
      • Sforzo G.S.
      • Frost B.
      • et al.
      The effects of exercise training on resting prostacyclin and thromboxane A(2) in older adults.
      ,
      • Książek M.
      • Charmas M.
      • Klusiewicz A.
      • et al.
      Endurance training selectively increases high-density lipoprotein-bound sphingosine-1-phosphate in the plasma.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ,
      • Murakami T.
      • Horigome H.
      • Tanaka K.
      • et al.
      Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      ,
      • Ponjee G.A.
      • Janssen E.M.
      • van Wersch J.W.
      Prolonged physical conditioning and blood platelet release markers: a longitudinal study.
      ,
      • Santilli F.
      • Vazzana N.
      • Iodice P.
      • et al.
      Effects of high-amount-high-intensity exercise on in vivo platelet activation: modulation by lipid peroxidation and AGE/RAGE axis.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ,
      • Wang J.S.
      • Li Y.S.
      • Chen J.C.
      • et al.
      Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men.
      ,
      • Zoladz J.A.
      • Majerczak J.
      • Duda K.
      • et al.
      Endurance training increases exercise-induced prostacyclin release in young, healthy men - relationship with VO2max.
      ,
      • Durmuş İ.
      • Kalaycıoğlu E.
      • Çetin M.
      • et al.
      Exercise-based cardiac rehabilitation has a strong relationship with mean platelet volume reduction.
      ,
      • Lee K.W.
      • Blann A.D.
      • Jolly K.
      • et al.
      Plasma haemostatic markers, endothelial function and ambulatory blood pressure changes with home versus hospital cardiac rehabilitation: the Birmingham rehabilitation uptake maximisation study.
      ,
      • Munk P.S.
      • Breland U.M.
      • Aukrust P.
      • et al.
      High intensity interval training reduces systemic inflammation in post-PCI patients.
      ,
      • Suzuki T.
      • Yamauchi K.
      • Yamada Y.
      • et al.
      Blood coagulability and fibrinolytic activity before and after physical training during the recovery phase of acute myocardial infarction.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ,
      • Vona M.
      • Codeluppi G.M.
      • Iannino T.
      • et al.
      Effects of different types of exercise training followed by detraining on endothelium-dependent dilation in patients with recent myocardial infarction.
      ,
      • Januszek R.
      • Mika P.
      • Nowobilski R.
      • et al.
      Soluble endoglin as a prognostic factor of the claudication distance improvement in patients with peripheral artery disease undergoing supervised treadmill training program.
      ,
      • Schlager O.
      • Hammer A.
      • Giurgea A.
      Impact of exercise training on inflammation and platelet activation in patients with intermittent claudication.
      ,
      • Heber S.
      • Fischer B.
      • Sallaberger-Lehner M.
      • et al.
      Effects of high-intensity interval training on platelet function in cardiac rehabilitation: a randomised controlled trial.
      ,
      • Tagawa K.
      • Ra S.G.
      • Kumagai H.
      • et al.
      Resistance training-induced decreases in central arterial compliance is associated with increases in serum thromboxane B-2 concentrations in young men.
      ,
      • Trenerry M.K.
      • Della Gatta P.A.
      • Larsen A.E.
      • et al.
      Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men.
      ], 6 studies (15 %) did not report supervision status [
      • Hilberg T.
      • Nowacki P.E.
      • Müller-Berghaus G.
      • et al.
      Changes in blood coagulation and fibrinolysis associated with maximal exercise and physical conditioning in women taking low dose oral contraceptives.
      ,
      • Bachero-Mena B.
      • Pareja-Blanco F.
      • Gonzalez-Badillo J.J.
      Enhanced strength and sprint levels, and changes in blood parameters during a complete athletics season in 800m high-level athletes.
      ,
      • Bittencourt C.R.O.
      • Izar M.C.O.
      • França C.N.
      • et al.
      Effects of chronic exercise on endothelial progenitor cells and microparticles in professional runners.
      ,
      • Boyali E.
      • Sevindi T.
      • Yuksel M.F.
      • et al.
      The effects of preparation period exercises on the hematological parameters of the taekwondo athletes.
      ,
      • Lippi G.
      • Montagnana M.
      • Salvagno G.L.
      • et al.
      Comparison of platelet function between sedentary individuals and competitive athletes at rest.
      ,
      • Liang G.
      • Huang X.
      • Hirsch J.
      • et al.
      Modest gains after an 8-week exercise program correlate with reductions in non-traditional markers of cardiovascular risk.
      ] and 5 (13 %) studies performed unsupervised exercise [
      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      The functional characteristics of the organism of physically inactive students who have started regular physical training.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      Hematological parameters in mature age men who have begun regular sports walking.
      ,
      • Keating F.K.
      • Schneider D.J.
      • Savage P.D.
      • et al.
      Effect of exercise training and weight loss on platelet reactivity in overweight patients with coronary artery disease.
      ]. The length of the exercise intervention was varying from 1 to 9 months. Twenty-six studies (65 %) performed exercise interventions for ≤3 months [
      • Hilberg T.
      • Nowacki P.E.
      • Müller-Berghaus G.
      • et al.
      Changes in blood coagulation and fibrinolysis associated with maximal exercise and physical conditioning in women taking low dose oral contraceptives.
      ,
      • Boyali E.
      • Sevindi T.
      • Yuksel M.F.
      • et al.
      The effects of preparation period exercises on the hematological parameters of the taekwondo athletes.
      ,
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Erdogan R.
      Effects of endurance workouts on thyroid hormone metabolism and biochemical markers in athletes.
      ,
      • Heber S.
      • Assinger A.
      • Pokan R.
      • et al.
      Correlation between cardiorespiratory fitness and platelet function in healthy women.
      ,
      • Książek M.
      • Charmas M.
      • Klusiewicz A.
      • et al.
      Endurance training selectively increases high-density lipoprotein-bound sphingosine-1-phosphate in the plasma.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ,
      • Murakami T.
      • Horigome H.
      • Tanaka K.
      • et al.
      Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity.
      ,
      • Santilli F.
      • Vazzana N.
      • Iodice P.
      • et al.
      Effects of high-amount-high-intensity exercise on in vivo platelet activation: modulation by lipid peroxidation and AGE/RAGE axis.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ,
      • Wang J.S.
      • Li Y.S.
      • Chen J.C.
      • et al.
      Effects of exercise training and deconditioning on platelet aggregation induced by alternating shear stress in men.
      ,
      • Zoladz J.A.
      • Majerczak J.
      • Duda K.
      • et al.
      Endurance training increases exercise-induced prostacyclin release in young, healthy men - relationship with VO2max.
      ,
      • Durmuş İ.
      • Kalaycıoğlu E.
      • Çetin M.
      • et al.
      Exercise-based cardiac rehabilitation has a strong relationship with mean platelet volume reduction.
      ,
      • Lee K.W.
      • Blann A.D.
      • Jolly K.
      • et al.
      Plasma haemostatic markers, endothelial function and ambulatory blood pressure changes with home versus hospital cardiac rehabilitation: the Birmingham rehabilitation uptake maximisation study.
      ,
      • Liang G.
      • Huang X.
      • Hirsch J.
      • et al.
      Modest gains after an 8-week exercise program correlate with reductions in non-traditional markers of cardiovascular risk.
      ,
      • Suzuki T.
      • Yamauchi K.
      • Yamada Y.
      • et al.
      Blood coagulability and fibrinolytic activity before and after physical training during the recovery phase of acute myocardial infarction.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ,
      • Vona M.
      • Codeluppi G.M.
      • Iannino T.
      • et al.
      Effects of different types of exercise training followed by detraining on endothelium-dependent dilation in patients with recent myocardial infarction.
      ,
      • Januszek R.
      • Mika P.
      • Nowobilski R.
      • et al.
      Soluble endoglin as a prognostic factor of the claudication distance improvement in patients with peripheral artery disease undergoing supervised treadmill training program.
      ,
      • Heber S.
      • Fischer B.
      • Sallaberger-Lehner M.
      • et al.
      Effects of high-intensity interval training on platelet function in cardiac rehabilitation: a randomised controlled trial.
      ,
      • Tagawa K.
      • Ra S.G.
      • Kumagai H.
      • et al.
      Resistance training-induced decreases in central arterial compliance is associated with increases in serum thromboxane B-2 concentrations in young men.
      ,
      • Trenerry M.K.
      • Della Gatta P.A.
      • Larsen A.E.
      • et al.
      Impact of resistance exercise training on interleukin-6 and JAK/STAT in young men.
      ], and in 14 studies (35 %) the exercise period lasted for >3 months [
      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Bachero-Mena B.
      • Pareja-Blanco F.
      • Gonzalez-Badillo J.J.
      Enhanced strength and sprint levels, and changes in blood parameters during a complete athletics season in 800m high-level athletes.
      ,
      • Bittencourt C.R.O.
      • Izar M.C.O.
      • França C.N.
      • et al.
      Effects of chronic exercise on endothelial progenitor cells and microparticles in professional runners.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Haynes A.
      • Linden M.D.
      • Robey E.
      Beneficial impacts of regular exercise on platelet function in sedentary older adults: evidence from a randomized 6-mo walking trial.
      ,
      • Kauffman R.D.
      • Sforzo G.S.
      • Frost B.
      • et al.
      The effects of exercise training on resting prostacyclin and thromboxane A(2) in older adults.
      ,
      • Lippi G.
      • Montagnana M.
      • Salvagno G.L.
      • et al.
      Comparison of platelet function between sedentary individuals and competitive athletes at rest.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      The functional characteristics of the organism of physically inactive students who have started regular physical training.
      ,
      • Medvedev I.N.
      • Karpov V.Y.
      • Eremin M.V.
      • et al.
      Hematological parameters in mature age men who have begun regular sports walking.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      ,
      • Ponjee G.A.
      • Janssen E.M.
      • van Wersch J.W.
      Prolonged physical conditioning and blood platelet release markers: a longitudinal study.
      ,
      • Keating F.K.
      • Schneider D.J.
      • Savage P.D.
      • et al.
      Effect of exercise training and weight loss on platelet reactivity in overweight patients with coronary artery disease.
      ,
      • Munk P.S.
      • Breland U.M.
      • Aukrust P.
      • et al.
      High intensity interval training reduces systemic inflammation in post-PCI patients.
      ,
      • Schlager O.
      • Hammer A.
      • Giurgea A.
      Impact of exercise training on inflammation and platelet activation in patients with intermittent claudication.
      ]. Changes in platelet function markers following exercise did not differ between studies with ≤3 months' exercise compared with studies with >3 months of exercise training (data not shown).

      3.3 Platelet aggregation

      Eight studies measured platelet aggregation using light transmittance aggregometry [
      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ]. Overall, eight studies reported a reduction [
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ] and seven studies reported no changes in platelet aggregation following exercise training [
      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ]. The most frequently measured marker was ADP-induced platelet aggregation. When comparing changes from baseline to after the exercise intervention, six studies showed a decline [
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ], whilst three reported no changes in ADP-induced platelet aggregation (Table 3) [
      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ]. When changes in the exercise groups were compared with changes in the control group, one study reported a decrease [
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ] and four studies found no differences between the two groups [
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ]. When comparing studies that reported a decrease and studies reporting no change in ADP-induced platelet aggregation following an exercise intervention, age (33 years and 34 years) and body mass index (24 in both) were similar in both groups of studies. On the contrary, there was a noticeable variation in the gender distribution across the groups, with a greater proportion of females (44 % vs 27 %) in the group that did not find any alterations in ADP-induced platelet aggregation (χ2 (1, n = 443) = 13.4, p = 0.0003). COL-induced platelet aggregation was reduced after exercise training in four studies [
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ], whereas one study did not show any changes [
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ]. Regarding results on EPI-induced platelet aggregation; two studies reported a reduced aggregation [
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ] and two studies did not find any changes after regular exercise training [
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ]. All studies on platelet aggregation, with the exception of one [
      • Toth-Zsamboki E.
      • Horvath Z.
      • Hajtman L.
      • et al.
      Cardiac rehabilitation programme as a non-pharmacological platelet inhibitory tool in acute coronary syndrome survivors.
      ], comprised healthy individuals [
      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Di Massimo C.
      • Scarpelli P.
      • Penco M.
      • et al.
      Possible involvement of plasma antioxidant defences in training-associated decrease of platelet responsiveness in humans.
      ,
      • Lundberg Slingsby M.H.
      • Nyberg M.
      • Egelund J.
      • et al.
      Aerobic exercise training lowers platelet reactivity and improves platelet sensitivity to prostacyclin in pre- and postmenopausal women.
      ,
      • Lundberg Slingsby M.H.
      • Gliemann L.
      • Thrane M.
      • et al.
      Platelet responses to pharmacological and physiological interventions in middle-aged men with different habitual physical activity levels.
      ,
      • Podgórska K.
      • Derkacz A.
      • Szahidewicz-Krupska E.
      • et al.
      Effect of regular aerobic activity in young healthy athletes on profile of endothelial function and platelet activity.
      ,
      • Wang J.S.
      • Chow S.E.
      Effects of exercise training and detraining on oxidized low-density lipoprotein-potentiated platelet function in men.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of chronic exercise and deconditioning on platelet function in women.
      ,
      • Wang J.S.
      • Jen C.J.
      • Chen H.I.
      Effects of exercise training and deconditioning on platelet function in men.
      ].

      3.4 Platelet activation and endothelial activation linked to platelet function

      Eight different markers of endothelial and platelet activation were measured in three or more studies and are presented in Table 3 [
      • Hilberg T.
      • Nowacki P.E.
      • Müller-Berghaus G.
      • et al.
      Changes in blood coagulation and fibrinolysis associated with maximal exercise and physical conditioning in women taking low dose oral contraceptives.
      ,
      • Agren J.J.
      • Pekkarinen H.
      • Litmanen H.
      • et al.
      Fish diet and physical fitness in relation to membrane and serum lipids, prostanoid metabolism and platelet aggregation in female students.
      ,
      • Bachero-Mena B.
      • Pareja-Blanco F.
      • Gonzalez-Badillo J.J.
      Enhanced strength and sprint levels, and changes in blood parameters during a complete athletics season in 800m high-level athletes.
      ,
      • Bittencourt C.R.O.
      • Izar M.C.O.
      • França C.N.
      • et al.
      Effects of chronic exercise on endothelial progenitor cells and microparticles in professional runners.
      ,
      • Boyali E.
      • Sevindi T.
      • Yuksel M.F.
      • et al.
      The effects of preparation period exercises on the hematological parameters of the taekwondo athletes.
      ,
      • Burri B.J.
      • Van Loan M.
      • Keim N.L.
      Moderate exercise training and low-energy diets are associated with small changes in indices of platelet aggregation and blood coagulation in overweight women.
      ,
      • Coppola L.
      • Grassia A.
      • Coppola A.
      • et al.
      Effects of a moderate-intensity aerobic program on blood viscosity, platelet aggregation and fibrinolytic balance in young and middle-aged sedentary subjects.
      ,
      • Erdogan R.
      Effects of endurance workouts on thyroid hormone metabolism and biochemical markers in athletes.