Deleterious effects of short-term, high-intensity exercise on immune function: Evidence from leucocyte mitochondrial alterations and apoptosis

Ta Chuan Tuan, T. G. Hsu, Man Cai Fong, C. F. Hsu, K. K C Tsai, C. Y. Lee, C. W. Kong

Research output: Contribution to journalArticle

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Abstract

Background: Although moderate exercise can benefit health, acute and vigorous exercise may have the opposite effect. Strenuous exercise can induce alterations in the physiology and viability of circulating leucocytes, which have a causal relationship with exercise-induced immune distress. Objectives: To investigate the use of mitochondrial transmembrane potential (MTP), a functional marker of the energy and viability status of leucocytes, for monitoring the immunomodulating effects of short-term, high-intensity exercise. Methods: 12 healthy volunteers with a mean VO2MAX of 70.4 ml/kg/min carried out 3 consecutive days of high-intensity exercise (85% of VO 2MAX for 30 min every day). Blood samples were collected at multiple time points immediately before and after each exercise session and at 24 and 72 h after the completion of exercise. Leucocyte MTP, apoptosis and circulatory inflammation markers were measured by flow cytometry and enzyme-linked immunosorbent assays. Results: MTP of peripheral blood leucocytes had declined immediately after the first exercise session and remained subnormal 24 h later. It did not normalise until 72 h after exercise. The sequential changes in MTP were consistent among the three leucocyte subpopulations (polymorphonuclear neutrophils, lymphocytes and monocytes) and were significant (p<0.05). Leucocytes displayed a gradual and incremental change in their propensity for apoptosis during and after exercise. Similarly, plasma concentrations of tumour necrosis factor-α and soluble Fas ligand were raised during the exercise sessions and had not normalised by 72 h after the completion of exercise. Correlation between changes in leucocyte MTP and plasma concentrations of tumour necrosis factor-α and soluble Fas ligand was variable, but significant for polymorphonuclear neutrophils and lymphocytes (p<0.05). Conclusions: Short-term, high-intensity exercise can lead to a significant and prolonged dysfunction of the mitochondrial energy status of peripheral blood leucocytes, which is accompanied by an increased propensity for apoptosis and raised pro-inflammatory mediators. These results support the immunosuppressive effects of excessive exercise and suggest that MTP is a useful marker of these effects.

Original languageEnglish
Pages (from-to)11-15
Number of pages5
JournalBritish Journal of Sports Medicine
Volume42
Issue number1
DOIs
Publication statusPublished - Jan 2008

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Leukocytes
Exercise
Apoptosis
Membrane Potentials
Neutrophils
Fas Ligand Protein
Tumor Necrosis Factor-alpha
Lymphocytes
Insurance Benefits
Immunosuppressive Agents
Monocytes
Healthy Volunteers
Flow Cytometry
Enzyme-Linked Immunosorbent Assay
Inflammation

ASJC Scopus subject areas

  • Public Health, Environmental and Occupational Health
  • Orthopedics and Sports Medicine

Cite this

Deleterious effects of short-term, high-intensity exercise on immune function : Evidence from leucocyte mitochondrial alterations and apoptosis. / Tuan, Ta Chuan; Hsu, T. G.; Fong, Man Cai; Hsu, C. F.; Tsai, K. K C; Lee, C. Y.; Kong, C. W.

In: British Journal of Sports Medicine, Vol. 42, No. 1, 01.2008, p. 11-15.

Research output: Contribution to journalArticle

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abstract = "Background: Although moderate exercise can benefit health, acute and vigorous exercise may have the opposite effect. Strenuous exercise can induce alterations in the physiology and viability of circulating leucocytes, which have a causal relationship with exercise-induced immune distress. Objectives: To investigate the use of mitochondrial transmembrane potential (MTP), a functional marker of the energy and viability status of leucocytes, for monitoring the immunomodulating effects of short-term, high-intensity exercise. Methods: 12 healthy volunteers with a mean VO2MAX of 70.4 ml/kg/min carried out 3 consecutive days of high-intensity exercise (85{\%} of VO 2MAX for 30 min every day). Blood samples were collected at multiple time points immediately before and after each exercise session and at 24 and 72 h after the completion of exercise. Leucocyte MTP, apoptosis and circulatory inflammation markers were measured by flow cytometry and enzyme-linked immunosorbent assays. Results: MTP of peripheral blood leucocytes had declined immediately after the first exercise session and remained subnormal 24 h later. It did not normalise until 72 h after exercise. The sequential changes in MTP were consistent among the three leucocyte subpopulations (polymorphonuclear neutrophils, lymphocytes and monocytes) and were significant (p<0.05). Leucocytes displayed a gradual and incremental change in their propensity for apoptosis during and after exercise. Similarly, plasma concentrations of tumour necrosis factor-α and soluble Fas ligand were raised during the exercise sessions and had not normalised by 72 h after the completion of exercise. Correlation between changes in leucocyte MTP and plasma concentrations of tumour necrosis factor-α and soluble Fas ligand was variable, but significant for polymorphonuclear neutrophils and lymphocytes (p<0.05). Conclusions: Short-term, high-intensity exercise can lead to a significant and prolonged dysfunction of the mitochondrial energy status of peripheral blood leucocytes, which is accompanied by an increased propensity for apoptosis and raised pro-inflammatory mediators. These results support the immunosuppressive effects of excessive exercise and suggest that MTP is a useful marker of these effects.",
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AU - Tuan, Ta Chuan

AU - Hsu, T. G.

AU - Fong, Man Cai

AU - Hsu, C. F.

AU - Tsai, K. K C

AU - Lee, C. Y.

AU - Kong, C. W.

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N2 - Background: Although moderate exercise can benefit health, acute and vigorous exercise may have the opposite effect. Strenuous exercise can induce alterations in the physiology and viability of circulating leucocytes, which have a causal relationship with exercise-induced immune distress. Objectives: To investigate the use of mitochondrial transmembrane potential (MTP), a functional marker of the energy and viability status of leucocytes, for monitoring the immunomodulating effects of short-term, high-intensity exercise. Methods: 12 healthy volunteers with a mean VO2MAX of 70.4 ml/kg/min carried out 3 consecutive days of high-intensity exercise (85% of VO 2MAX for 30 min every day). Blood samples were collected at multiple time points immediately before and after each exercise session and at 24 and 72 h after the completion of exercise. Leucocyte MTP, apoptosis and circulatory inflammation markers were measured by flow cytometry and enzyme-linked immunosorbent assays. Results: MTP of peripheral blood leucocytes had declined immediately after the first exercise session and remained subnormal 24 h later. It did not normalise until 72 h after exercise. The sequential changes in MTP were consistent among the three leucocyte subpopulations (polymorphonuclear neutrophils, lymphocytes and monocytes) and were significant (p<0.05). Leucocytes displayed a gradual and incremental change in their propensity for apoptosis during and after exercise. Similarly, plasma concentrations of tumour necrosis factor-α and soluble Fas ligand were raised during the exercise sessions and had not normalised by 72 h after the completion of exercise. Correlation between changes in leucocyte MTP and plasma concentrations of tumour necrosis factor-α and soluble Fas ligand was variable, but significant for polymorphonuclear neutrophils and lymphocytes (p<0.05). Conclusions: Short-term, high-intensity exercise can lead to a significant and prolonged dysfunction of the mitochondrial energy status of peripheral blood leucocytes, which is accompanied by an increased propensity for apoptosis and raised pro-inflammatory mediators. These results support the immunosuppressive effects of excessive exercise and suggest that MTP is a useful marker of these effects.

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