European Journal of Applied Physiology

, Volume 114, Issue 9, pp 1955–1961 | Cite as

High intensity cycling before SCUBA diving reduces post-decompression microparticle production and neutrophil activation

  • Dennis Madden
  • Stephen R. Thom
  • Ming Yang
  • Veena M. Bhopale
  • Marko Ljubkovic
  • Zeljko DujicEmail author
Original Article



Venous gas emboli (VGE) have traditionally served as a marker for decompression stress after SCUBA diving and a reduction in bubble loads is a target for precondition procedures. However, VGE can be observed in large quantities with no negative clinical consequences. The effect of exercise before diving on VGE has been evaluated with mixed results. Microparticle (MP) counts and sub-type expression serve as indicators of vascular inflammation and DCS in mice. The goal of the present study is to evaluate the effect of anaerobic cycling (AC) on VGE and MP following SCUBA diving.


Ten male divers performed two dives to 18 m for 41 min, one dive (AC) was preceded by a repeated-Wingate cycling protocol; a control dive (CON) was completed without exercise. VGE were analyzed at 15, 40, 80, and 120 min post-diving. Blood for MP analysis was collected before exercise (AC only), before diving, 15 and 120 min after surfacing.


VGE were significantly lower 15 min post-diving in the AC group, with no difference in the remaining measurements. MPs were elevated by exercise and diving, however, post-diving elevations were attenuated in the AC dive. Some markers of neutrophil elevation (CD18, CD41) were increased in the CON compared to the AC dive.


The repeated-Wingate protocol resulted in an attenuation of MP counts and sub-types that have been related to vascular injury and DCS-like symptoms in mice. Further studies are needed to determine if MPs represent a risk factor or marker for DCS in humans.


SCUBA diving Exercise Microparticles Neutrophil activation High intensity 



Anaerobic cycling


Analysis of variance


Body mass index


Bubble score






Decompression sickness


High intensity training


Heart rate






Nitric oxide


Self-contained underwater breathing apparatus


Standard deviation


Venous gas emboli


Maximal volume of oxygen uptake



The research leading to these results has received funding from the People Program (Marie Curie Actions) of the European Union’s Seventh Framework Program FRP/2007-2013/under REA grant agreement n° 264816, the Croatian Ministry of Science, Education and Sports (Grant No. 216-2160133-0130 to ZD) and the Office of Naval Research: ONR grant (Microparticle production with decompression stress - N00014-13-10614).

Conflict of interest

The authors declare no conflict of interest.


  1. Anderson HC, Mulhall D, Garimella R (2010) Role of extracellular membrane vesicles in the pathogenesis of various diseases, including cancer, renal diseases, atherosclerosis, and arthritis. Lab Invest 90(11):1549–1557PubMedCrossRefGoogle Scholar
  2. Blatteau JE, Gempp E, Galland FM, Pontier JM, Sainty JM, Robinet C (2005) Aerobic exercise 2 hours before a dive to 30 msw decreases bubble formation after decompression. Aviat Space Environ Med 76(7):666–669PubMedGoogle Scholar
  3. Blatteau JE, Boussuges A, Gempp E, Pontier JM, Castagna O, Robinet C, Galland FM, Bourdon L (2007) Haemodynamic changes induced by submaximal exercise before a dive and its consequences on bubble formation. Br J Sports Med 41(6):375–379PubMedCentralPubMedCrossRefGoogle Scholar
  4. Blatteau JE, Gempp E, Balestra C, Mets T, Germonpre P (2008) Predive sauna and venous gas bubbles upon decompression from 400 kPa. Aviat Space Environ Med 79(12):1100–1105PubMedCrossRefGoogle Scholar
  5. Burger D, Schock S, Thompson CS, Montezano AC, Hakim AM, Touyz RM (2013) Microparticles: biomarkers and beyond. Clin Sci 124(7):423–441PubMedCrossRefGoogle Scholar
  6. Castagna O, Brisswalter J, Vallee N, Blatteau JE (2011) Endurance exercise immediately before sea diving reduces bubble formation in scuba divers. Eur J Appl Physiol 111(6):1047–1054PubMedCrossRefGoogle Scholar
  7. Chaar V, Romana M, Tripette J, Broquere C, Huisse MG, Hue O, Hardy-Dessources MD, Connes P (2011) Effect of strenuous physical exercise on circulating cell-derived microparticles. Clin Hemorheol Microcirc 47(1):15–25PubMedGoogle Scholar
  8. Cocks M, Shaw CS, Shepherd SO, Fisher JP, Ranasinghe AM, Barker TA, Tipton KD, Wagenmakers AJ (2013) Sprint interval and endurance training are equally effective in increasing muscle microvascular density and eNOS content in sedentary males. J Physiol 591(Pt 3):641–656PubMedCentralPubMedCrossRefGoogle Scholar
  9. Distler JH, Akhmetshina A, Dees C, Jungel A, Sturzl M, Gay S, Pisetsky DS, Schett G, Distler O (2011) Induction of apoptosis in circulating angiogenic cells by microparticles. Arthritis Rheum 63(7):2067–2077. doi: 10.1002/art.30361 PubMedCrossRefGoogle Scholar
  10. Dujic Z, Duplancic D, Marinovic-Terzic I, Bakovic D, Ivancev V, Valic Z, Eterovic D, Petri NM, Wisloff U, Brubakk AO (2004) Aerobic exercise before diving reduces venous gas bubble formation in humans. J Physiol 555(Pt 3):637–642PubMedCentralPubMedCrossRefGoogle Scholar
  11. Dujic Z, Valic Z, Brubakk AO (2008) Beneficial role of exercise on scuba diving. Exerc Sport Sci Rev 36(1):38–42. doi: 10.1097/jes.0b013e31815ddb02 PubMedCrossRefGoogle Scholar
  12. Eckenhoff RG, Olstad CS, Carrod G (1990) Human dose-response relationship for decompression and endogenous bubble formation. J Appl Physiol (1985) 69(3):914–918Google Scholar
  13. Enoksen E, Shalfawi SA, Tonnessen E (2011) The effect of high- vs low-intensity training on aerobic capacity in well-trained male middle-distance runners. J Strength Cond Res 25(3):812–818PubMedCrossRefGoogle Scholar
  14. Gennser M, Jurd KM, Blogg SL (2012) Pre-dive exercise and post-dive evolution of venous gas emboli. Aviat Space Environ Med 83(1):30–34PubMedCrossRefGoogle Scholar
  15. Germonpre P, Pontier JM, Gempp E, Blatteau JE, Deneweth S, Lafere P, Marroni A, Balestra C (2009) Pre-dive vibration effect on bubble formation after a 30-m dive requiring a decompression stop. Aviat Space Environ Med 80(12):1044–1048PubMedCrossRefGoogle Scholar
  16. Jurd KM, Thacker JC, Seddon FM, Gennser M, Loveman GA (2011) The effect of pre-dive exercise timing, intensity and mode on post-decompression venous gas emboli. Diving Hyperb Med 41(4):183–188PubMedGoogle Scholar
  17. Kessler HS, Sisson SB, Short KR (2012) The potential for high-intensity interval training to reduce cardiometabolic disease risk. Sports Med 42(6):489–509PubMedCrossRefGoogle Scholar
  18. Ljubkovic M, Zanchi J, Breskovic T, Marinovic J, Lojpur M, Dujic Z (2012) Determinants of arterial gas embolism after scuba diving. J Appl Physiol (1985) 112(1):91–95. doi: 10.1152/japplphysiol.00943.2011 CrossRefGoogle Scholar
  19. Madden D, Thom SR, Milovanova TN, Yang M, Bhopale VM, Ljubkovic M, Dujic Z (2014) Exercise before SCUBA diving ameliorates decompression-induced neutrophil activation. Med Sci Sports ExercGoogle Scholar
  20. Marinovic J, Ljubkovic M, Breskovic T, Gunjaca G, Obad A, Modun D, Bilopavlovic N, Tsikas D, Dujic Z (2012) Effects of successive air and nitrox dives on human vascular function. Eur J Appl Physiol 112(6):2131–2137PubMedCrossRefGoogle Scholar
  21. Medby C, Bye A, Wisloff U, Brubakk AO (2008) Heat shock increases survival in rats exposed to hyperbaric pressure. Diving Hyperb Med 38(4):189–193PubMedGoogle Scholar
  22. Mollerlokken A, Breskovic T, Palada I, Valic Z, Dujic Z, Brubakk AO (2011) Observation of increased venous gas emboli after wet dives compared to dry dives. Diving Hyperb Med 41(3):124–128PubMedGoogle Scholar
  23. Thom SR, Yang M, Bhopale VM, Huang S, Milovanova TN (2011) Microparticles initiate decompression-induced neutrophil activation and subsequent vascular injuries. J Appl Physiol 110(2):340–351PubMedCrossRefGoogle Scholar
  24. Thom SR, Milovanova TN, Bogush M, Bhopale VM, Yang M, Bushmann K, Pollock NW, Ljubkovic M, Denoble P, Dujic Z (2012) Microparticle production, neutrophil activation, and intravascular bubbles following open-water SCUBA diving. J Appl Physiol 112(8):1268–1278. doi: 10.1152/japplphysiol.01305.2011 PubMedCrossRefGoogle Scholar
  25. Thom SR, Milovanova TN, Bogush M, Yang M, Bhopale VM, Pollock NW, Ljubkovic M, Denoble PJ, Madden D, Lozo M, Dujic Z (2013) Bubbles, microparticles and neutrophil activation: changes with exercise level and breathing gas during open-water SCUBA diving. J Appl Physiol 114(10):1396–1405PubMedCrossRefGoogle Scholar
  26. Trappenburg MC, van Schilfgaarde M, Frerichs FC, Spronk HM, ten Cate H, de Fijter CW, Terpstra WE, Leyte A (2012) Chronic renal failure is accompanied by endothelial activation and a large increase in microparticle numbers with reduced procoagulant capacity. Nephrol Dial Transplant 27(4):1446–1453PubMedCrossRefGoogle Scholar
  27. Wisloff U, Brubakk AO (2001) Aerobic endurance training reduces bubble formation and increases survival in rats exposed to hyperbaric pressure. J Physiol 537(Pt 2):607–611PubMedCentralPubMedCrossRefGoogle Scholar
  28. Yang M, Milovanova TN, Bogush M, Uzun G, Bhopale VM, Thom SR (2012a) Microparticle enlargement and altered surface proteins after air decompression are associated with inflammatory vascular injuries. J Appl Physiol 112(1):204–211PubMedCentralPubMedCrossRefGoogle Scholar
  29. Yang M, Milovanova TN, Bogush M, Uzun G, Bhopale VM, Thom SR (2012b) Microparticle enlargement and altered surface proteins after air decompression are associated with inflammatory vascular injuries. J Appl Physiol (1985) 112(1):204–211CrossRefGoogle Scholar
  30. Zielinska M, Koniarek W, Goch JH, Cebula B, Tybura M, Robak T, Smolewski P (2005) Circulating endothelial microparticles in patients with acute myocardial infarction. Kardiologia Polska 62(6):531–542 discussion 543–534PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Dennis Madden
    • 1
  • Stephen R. Thom
    • 2
  • Ming Yang
    • 2
  • Veena M. Bhopale
    • 2
  • Marko Ljubkovic
    • 1
  • Zeljko Dujic
    • 1
    Email author
  1. 1.Department of PhysiologyUniversity of Split School of MedicineSplitCroatia
  2. 2.Department of Emergency MedicineUniversity of MarylandBaltimoreUSA

Personalised recommendations