Influence of pistachios on performance and exercise-induced inflammation, oxidative stress, immune dysfunction, and metabolite shifts in cyclists: a randomized, crossover trial

David C Nieman, Johannes Scherr, Beibei Luo, Mary Pat Meaney, Didier Dréau, Wei Sha, Dustin A Dew, Dru A Henson, Kirk L Pappan, David C Nieman, Johannes Scherr, Beibei Luo, Mary Pat Meaney, Didier Dréau, Wei Sha, Dustin A Dew, Dru A Henson, Kirk L Pappan

Abstract

Objectives: Pistachio nut ingestion (3 oz./d, two weeks) was tested for effects on exercise performance and 21-h post-exercise recovery from inflammation, oxidative stress, immune dysfunction, and metabolite shifts.

Methods: Using a randomized, crossover approach, cyclists (N = 19) engaged in two 75-km time trials after 2-weeks pistachio or no pistachio supplementation, with a 2-week washout period. Subjects came to the lab in an overnight fasted state, and ingested water only or 3 oz. pistachios with water before and during exercise. Blood samples were collected 45 min pre-exercise, and immediately post-, 1.5-h post-, and 21-h post-exercise, and analyzed for plasma cytokines, C-reactive protein (CRP), F2-isoprostanes (F2-IsoP), granulocyte phagocytosis (GPHAG) and oxidative burst activity (GOBA), and shifts in metabolites.

Results: Performance time for the 75-km time trial was 4.8% slower under pistachio conditions (2.84 ± 0.11 and 2.71 ± 0.07 h, respectively, P = 0.034). Significant time effects were shown for plasma cytokines, CRP, F2-IsoP, GPHAG, and GOBA, with few group differences. Metabolomics analysis revealed 423 detectable compounds of known identity, with significant interaction effects for 19 metabolites, especially raffinose, (12Z)-9,10-Dihydroxyoctadec-12-enoate (9,10-DiHOME), and sucrose. Dietary intake of raffinose was 2.19 ± 0.15 and 0.35 ± 0.08 mg/d during the pistachio and no pistachio periods, and metabolomics revealed that colon raffinose and sucrose translocated to the circulation during exercise due to increased gut permeability. The post-exercise increase in plasma raffinose correlated significantly with 9,10-DiHOME and other oxidative stress metabolites.

Conclusions: In summary, 2-weeks pistachio nut ingestion was associated with reduced 75-km cycling time trial performance and increased post-exercise plasma levels of raffinose, sucrose, and metabolites related to leukotoxic effects and oxidative stress.

Trial registration: ClinicalTrials.gov NCT01821820.

Conflict of interest statement

Competing Interests: The authors confirm that funding through the American Pistachio Growers did not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

Figures

Figure 1. Subject flow diagram.
Figure 1. Subject flow diagram.
Figure 2. Performance time for the 75-km…
Figure 2. Performance time for the 75-km trial under pistachio compared to water-only conditions (mean±SE).
*  =  Q-value 2-way ANOVA contrasts

Figure 3. Plasma raffinose in pistachio and…

Figure 3. Plasma raffinose in pistachio and water conditions (interaction effect, Q

* =…

Figure 3. Plasma raffinose in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts

Figure 4. Plasma sucrose in pistachio and…

Figure 4. Plasma sucrose in pistachio and water conditions (interaction effect, Q

* =…

Figure 4. Plasma sucrose in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts

Figure 5. Plasma 9,10 DiHOME in pistachio…

Figure 5. Plasma 9,10 DiHOME in pistachio and water conditions (interaction effect, Q

*…

Figure 5. Plasma 9,10 DiHOME in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts
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Serum Branched-Chain Amino Acid Metabolites Increase in Males When Aerobic Exercise Is Initiated with Low Muscle Glycogen.
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References
Nieman DC (1997) Immune response to heavy exertion. J Appl Physiol 82: 1385–1394. - PubMed Nieman DC (2008) Immunonutrition support for athletes. Nutr Rev 66: 310–320. - PubMed Walsh NP, Gleeson M, Pyne DB, Nieman DC, Dhabhar FS, et al. (2011) Position statement. Part two: Maintaining immune health. Exerc Immunol Rev 17: 64–103. - PubMed Nieman DC, Gillitt ND, Henson DA, Sha W, Shanely RA, et al. (2012) Bananas as an energy source during exercise: a metabolomics approach. PLoS One 7(5): e37479. - PMC - PubMed Nieman DC, Henson DA, Gojanovich G, Davis JM, Murphy EA, et al. (2006) Influence of carbohydrate on immune function following 2 h cycling. Res Sports Med 14: 225–237. - PubMed
Show all 37 references
Publication types
Randomized Controlled Trial
Research Support, Non-U.S. Gov't
MeSH terms
C-Reactive Protein / analysis
Intestinal Mucosa / metabolism
Mitochondria / drug effects
Oxidative Stress* / drug effects
Permeability / drug effects
Phagocytosis / drug effects
Associated data
ClinicalTrials.gov/NCT01821820
Grant support
This work was supported by American Pistachio Growers. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[x]
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The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

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Figure 3. Plasma raffinose in pistachio and…
Figure 3. Plasma raffinose in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts

Figure 4. Plasma sucrose in pistachio and…

Figure 4. Plasma sucrose in pistachio and water conditions (interaction effect, Q

* =…

Figure 4. Plasma sucrose in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts

Figure 5. Plasma 9,10 DiHOME in pistachio…

Figure 5. Plasma 9,10 DiHOME in pistachio and water conditions (interaction effect, Q

*…

Figure 5. Plasma 9,10 DiHOME in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts
Similar articles
Metabolomics approach to assessing plasma 13- and 9-hydroxy-octadecadienoic acid and linoleic acid metabolite responses to 75-km cycling.
Nieman DC, Shanely RA, Luo B, Meaney MP, Dew DA, Pappan KL. Nieman DC, et al. Am J Physiol Regul Integr Comp Physiol. 2014 Jul 1;307(1):R68-74. doi: 10.1152/ajpregu.00092.2014. Epub 2014 Apr 23. Am J Physiol Regul Integr Comp Physiol. 2014. PMID: 24760997
Influence of a polyphenol-enriched protein powder on exercise-induced inflammation and oxidative stress in athletes: a randomized trial using a metabolomics approach.
Nieman DC, Gillitt ND, Knab AM, Shanely RA, Pappan KL, Jin F, Lila MA. Nieman DC, et al. PLoS One. 2013 Aug 15;8(8):e72215. doi: 10.1371/journal.pone.0072215. eCollection 2013. PLoS One. 2013. PMID: 23967286 Free PMC article. Clinical Trial.
Bananas as an energy source during exercise: a metabolomics approach.
Nieman DC, Gillitt ND, Henson DA, Sha W, Shanely RA, Knab AM, Cialdella-Kam L, Jin F. Nieman DC, et al. PLoS One. 2012;7(5):e37479. doi: 10.1371/journal.pone.0037479. Epub 2012 May 17. PLoS One. 2012. PMID: 22616015 Free PMC article. Clinical Trial.
Influence of red pepper spice and turmeric on inflammation and oxidative stress biomarkers in overweight females: a metabolomics approach.
Nieman DC, Cialdella-Kam L, Knab AM, Shanely RA. Nieman DC, et al. Plant Foods Hum Nutr. 2012 Dec;67(4):415-21. doi: 10.1007/s11130-012-0325-x. Plant Foods Hum Nutr. 2012. PMID: 23150126 Clinical Trial.
Potential Impact of Nutrition on Immune System Recovery from Heavy Exertion: A Metabolomics Perspective.
Nieman DC, Mitmesser SH. Nieman DC, et al. Nutrients. 2017 May 18;9(5):513. doi: 10.3390/nu9050513. Nutrients. 2017. PMID: 28524103 Free PMC article. Review.
Cited by
Single and Joined Behaviour of Circulating Biomarkers and Metabolic Parameters in High-Fit and Low-Fit Healthy Females.
Janssen JJE, Lagerwaard B, Nieuwenhuizen AG, Escoté X, Canela N, Del Bas JM, de Boer VCJ, Keijer J. Janssen JJE, et al. Int J Mol Sci. 2023 Feb 20;24(4):4202. doi: 10.3390/ijms24044202. Int J Mol Sci. 2023. PMID: 36835625 Free PMC article.
Almond intake alters the acute plasma dihydroxy-octadecenoic acid (DiHOME) response to eccentric exercise.
Nieman DC, Omar AM, Kay CD, Kasote DM, Sakaguchi CA, Lkhagva A, Weldemariam MM, Zhang Q. Nieman DC, et al. Front Nutr. 2023 Jan 9;9:1042719. doi: 10.3389/fnut.2022.1042719. eCollection 2022. Front Nutr. 2023. PMID: 36698469 Free PMC article.
Influence of pistachios on force production, subjective ratings of pain, and oxidative stress following exercise-induced muscle damage in moderately trained athletes: A randomized, crossover trial.
Rayo VU, Thayer I, Galloway SDR, Hong MY, Hooshmand S, Liu C, North E, Okamoto L, O'Neal T, Philpott J, Witard OC, Kern M. Rayo VU, et al. Metabol Open. 2022 Oct 21;16:100215. doi: 10.1016/j.metop.2022.100215. eCollection 2022 Dec. Metabol Open. 2022. PMID: 36325128 Free PMC article.
Serum Branched-Chain Amino Acid Metabolites Increase in Males When Aerobic Exercise Is Initiated with Low Muscle Glycogen.
Margolis LM, Karl JP, Wilson MA, Coleman JL, Whitney CC, Pasiakos SM. Margolis LM, et al. Metabolites. 2021 Nov 30;11(12):828. doi: 10.3390/metabo11120828. Metabolites. 2021. PMID: 34940586 Free PMC article.
The Importance of Lipidomic Approach for Mapping and Exploring the Molecular Networks Underlying Physical Exercise: A Systematic Review.
Latino F, Cataldi S, Carvutto R, De Candia M, D'Elia F, Patti A, Bonavolontà V, Fischetti F. Latino F, et al. Int J Mol Sci. 2021 Aug 13;22(16):8734. doi: 10.3390/ijms22168734. Int J Mol Sci. 2021. PMID: 34445440 Free PMC article. Review.
References
Nieman DC (1997) Immune response to heavy exertion. J Appl Physiol 82: 1385–1394. - PubMed Nieman DC (2008) Immunonutrition support for athletes. Nutr Rev 66: 310–320. - PubMed Walsh NP, Gleeson M, Pyne DB, Nieman DC, Dhabhar FS, et al. (2011) Position statement. Part two: Maintaining immune health. Exerc Immunol Rev 17: 64–103. - PubMed Nieman DC, Gillitt ND, Henson DA, Sha W, Shanely RA, et al. (2012) Bananas as an energy source during exercise: a metabolomics approach. PLoS One 7(5): e37479. - PMC - PubMed Nieman DC, Henson DA, Gojanovich G, Davis JM, Murphy EA, et al. (2006) Influence of carbohydrate on immune function following 2 h cycling. Res Sports Med 14: 225–237. - PubMed
Show all 37 references
Publication types
Randomized Controlled Trial
Research Support, Non-U.S. Gov't
MeSH terms
C-Reactive Protein / analysis
Intestinal Mucosa / metabolism
Mitochondria / drug effects
Oxidative Stress* / drug effects
Permeability / drug effects
Phagocytosis / drug effects
Associated data
ClinicalTrials.gov/NCT01821820
Grant support
This work was supported by American Pistachio Growers. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Figure 4. Plasma sucrose in pistachio and…
Figure 4. Plasma sucrose in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts

Figure 5. Plasma 9,10 DiHOME in pistachio…

Figure 5. Plasma 9,10 DiHOME in pistachio and water conditions (interaction effect, Q

*…

Figure 5. Plasma 9,10 DiHOME in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts
Similar articles
Metabolomics approach to assessing plasma 13- and 9-hydroxy-octadecadienoic acid and linoleic acid metabolite responses to 75-km cycling.
Nieman DC, Shanely RA, Luo B, Meaney MP, Dew DA, Pappan KL. Nieman DC, et al. Am J Physiol Regul Integr Comp Physiol. 2014 Jul 1;307(1):R68-74. doi: 10.1152/ajpregu.00092.2014. Epub 2014 Apr 23. Am J Physiol Regul Integr Comp Physiol. 2014. PMID: 24760997
Influence of a polyphenol-enriched protein powder on exercise-induced inflammation and oxidative stress in athletes: a randomized trial using a metabolomics approach.
Nieman DC, Gillitt ND, Knab AM, Shanely RA, Pappan KL, Jin F, Lila MA. Nieman DC, et al. PLoS One. 2013 Aug 15;8(8):e72215. doi: 10.1371/journal.pone.0072215. eCollection 2013. PLoS One. 2013. PMID: 23967286 Free PMC article. Clinical Trial.
Bananas as an energy source during exercise: a metabolomics approach.
Nieman DC, Gillitt ND, Henson DA, Sha W, Shanely RA, Knab AM, Cialdella-Kam L, Jin F. Nieman DC, et al. PLoS One. 2012;7(5):e37479. doi: 10.1371/journal.pone.0037479. Epub 2012 May 17. PLoS One. 2012. PMID: 22616015 Free PMC article. Clinical Trial.
Influence of red pepper spice and turmeric on inflammation and oxidative stress biomarkers in overweight females: a metabolomics approach.
Nieman DC, Cialdella-Kam L, Knab AM, Shanely RA. Nieman DC, et al. Plant Foods Hum Nutr. 2012 Dec;67(4):415-21. doi: 10.1007/s11130-012-0325-x. Plant Foods Hum Nutr. 2012. PMID: 23150126 Clinical Trial.
Potential Impact of Nutrition on Immune System Recovery from Heavy Exertion: A Metabolomics Perspective.
Nieman DC, Mitmesser SH. Nieman DC, et al. Nutrients. 2017 May 18;9(5):513. doi: 10.3390/nu9050513. Nutrients. 2017. PMID: 28524103 Free PMC article. Review.
Cited by
Single and Joined Behaviour of Circulating Biomarkers and Metabolic Parameters in High-Fit and Low-Fit Healthy Females.
Janssen JJE, Lagerwaard B, Nieuwenhuizen AG, Escoté X, Canela N, Del Bas JM, de Boer VCJ, Keijer J. Janssen JJE, et al. Int J Mol Sci. 2023 Feb 20;24(4):4202. doi: 10.3390/ijms24044202. Int J Mol Sci. 2023. PMID: 36835625 Free PMC article.
Almond intake alters the acute plasma dihydroxy-octadecenoic acid (DiHOME) response to eccentric exercise.
Nieman DC, Omar AM, Kay CD, Kasote DM, Sakaguchi CA, Lkhagva A, Weldemariam MM, Zhang Q. Nieman DC, et al. Front Nutr. 2023 Jan 9;9:1042719. doi: 10.3389/fnut.2022.1042719. eCollection 2022. Front Nutr. 2023. PMID: 36698469 Free PMC article.
Influence of pistachios on force production, subjective ratings of pain, and oxidative stress following exercise-induced muscle damage in moderately trained athletes: A randomized, crossover trial.
Rayo VU, Thayer I, Galloway SDR, Hong MY, Hooshmand S, Liu C, North E, Okamoto L, O'Neal T, Philpott J, Witard OC, Kern M. Rayo VU, et al. Metabol Open. 2022 Oct 21;16:100215. doi: 10.1016/j.metop.2022.100215. eCollection 2022 Dec. Metabol Open. 2022. PMID: 36325128 Free PMC article.
Serum Branched-Chain Amino Acid Metabolites Increase in Males When Aerobic Exercise Is Initiated with Low Muscle Glycogen.
Margolis LM, Karl JP, Wilson MA, Coleman JL, Whitney CC, Pasiakos SM. Margolis LM, et al. Metabolites. 2021 Nov 30;11(12):828. doi: 10.3390/metabo11120828. Metabolites. 2021. PMID: 34940586 Free PMC article.
The Importance of Lipidomic Approach for Mapping and Exploring the Molecular Networks Underlying Physical Exercise: A Systematic Review.
Latino F, Cataldi S, Carvutto R, De Candia M, D'Elia F, Patti A, Bonavolontà V, Fischetti F. Latino F, et al. Int J Mol Sci. 2021 Aug 13;22(16):8734. doi: 10.3390/ijms22168734. Int J Mol Sci. 2021. PMID: 34445440 Free PMC article. Review.
References
Nieman DC (1997) Immune response to heavy exertion. J Appl Physiol 82: 1385–1394. - PubMed Nieman DC (2008) Immunonutrition support for athletes. Nutr Rev 66: 310–320. - PubMed Walsh NP, Gleeson M, Pyne DB, Nieman DC, Dhabhar FS, et al. (2011) Position statement. Part two: Maintaining immune health. Exerc Immunol Rev 17: 64–103. - PubMed Nieman DC, Gillitt ND, Henson DA, Sha W, Shanely RA, et al. (2012) Bananas as an energy source during exercise: a metabolomics approach. PLoS One 7(5): e37479. - PMC - PubMed Nieman DC, Henson DA, Gojanovich G, Davis JM, Murphy EA, et al. (2006) Influence of carbohydrate on immune function following 2 h cycling. Res Sports Med 14: 225–237. - PubMed
Show all 37 references
Publication types
Randomized Controlled Trial
Research Support, Non-U.S. Gov't
MeSH terms
C-Reactive Protein / analysis
Intestinal Mucosa / metabolism
Mitochondria / drug effects
Oxidative Stress* / drug effects
Permeability / drug effects
Phagocytosis / drug effects
Associated data
ClinicalTrials.gov/NCT01821820
Grant support
This work was supported by American Pistachio Growers. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Figure 5. Plasma 9,10 DiHOME in pistachio…
Figure 5. Plasma 9,10 DiHOME in pistachio and water conditions (interaction effect, Q
*  =  Q-value 2-way ANOVA contrasts

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Source: PubMed

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