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Effect of acute hypoxia on inspiratory muscle oxygenation during incremental inspiratory loading in healthy adults

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Abstract

Purpose

To non-invasively examine the effect of acute hypoxia and inspiratory threshold loading (ITL) on inspiratory muscles [sternocleidomastoid (SCM), scalene (SA) and parasternal (PS)] oxygenation in healthy adults using near-infrared spectroscopy (NIRS).

Methods

Twenty healthy adults (12 M/8 F) were randomly assigned to perform two ITL tests while breathing a normoxic or hypoxic (FIO2 = 15 %) gas mixture. NIRS devices were placed over the SCM, PS, SA, and a control muscle, tibialis anterior (TA), to monitor oxygenated (O2Hb), deoxygenated (HHb), total hemoglobin (tHb) and tissue saturation index (TSI). With the nose occluded, subjects breathed normally for 4 min through a mouthpiece that was connected to a weighted threshold loading device. ITL began by adding a 100-g weight to the ITL device. Then, every 2 min 50-g was added until task failure. Vital signs, ECG and ventilatory measures were monitored throughout the protocol.

Result

Participants were 31 ± 12 year and had normal spirometry. At task failure, the maximum load and ventilatory parameters did not differ between the hypoxic and normoxic ITL. At hypoxic ITL task failure, SpO2 was significantly lower, and ∆HHb increased more so in SA, SCM and PS than normoxic values. SCM ∆TSI decreased more so during hypoxic compared to normoxic ITL. ∆tHb in the inspiratory muscles (SCM, PS and SA) increased significantly compared to the decrease in TA during both hypoxic and normoxic ITL.

Conclusion

The SCM, an accessory inspiratory muscle was the most vulnerable to deoxygenation during incremental loading and this response was accentuated by acute hypoxia.

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Abbreviations

FEV1 :

Forced expiratory volume in 1 s

FEV1/FVC ratio:

Ratio of the forced expiratory volume in the first 1 s to the forced vital capacity of the lungs

FIO2 :

Fraction of inspired oxygen

FVC:

Forced vital capacity

HHb:

Deoxygenated hemoglobin

ITL:

Inspiratory threshold loading

NIRS:

Near-infrared spectroscopy

O2Hb:

Oxygenated hemoglobin

PETCO2 :

End tidal carbon dioxide partial pressure

PmPeak :

Peak mouth pressure

PS:

Parasternal

SA:

Scalene

SCM:

Sternocleidomastoid

SpO2 :

Saturation of hemoglobin with oxygen as measured by pulse oximetry

TA:

Tibialis anterior

tHb:

Total hemoglobin

TSI:

Tissue saturation index

VE :

Minute ventilation

VT :

Tidal volume

References

  • Babcock MA, Johnson BD, Pegelow DF et al (1995) Hypoxic effects on exercise-induced diaphragmatic fatigue in normal healthy humans. J Appl Physiol 78:82–92

    CAS  PubMed  Google Scholar 

  • Balady GJ, Chaitman B, Driscoll D et al (1998) Recommendations for cardiovascular screening, staffing, and emergency policies at health/fitness facilities. Circulation 97:2283–2293

    Article  CAS  PubMed  Google Scholar 

  • Borg GA (1982) Psychophysical bases of perceived exertion. Med Sci Sports Exerc 14:377–381

    CAS  PubMed  Google Scholar 

  • Campbell EJM (1955) The role of the scalene and sternomastoid muscles in breathing in normal subjects. An electromyographic study. J Anat 89:378–386

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cannon DT, Grout SL, May CA et al (2007) Recruitment of the serratus anterior as an accessory muscle of ventilation during graded exercise. J Physiol Sci 57:127–131

    Article  CAS  PubMed  Google Scholar 

  • Cvetko E, Karen P, Eržen I (2012) Myosin heavy chain composition of the human sternocleidomastoid muscle. Ann Anat 194:467–472

    Article  CAS  PubMed  Google Scholar 

  • De Bisschop C, Beloka S, Groepenhoff H et al (2014) Is there a competition for oxygen availability between respiratory and limb muscles? Respir Physiol Neurobiol 196:8–16

    Article  PubMed  Google Scholar 

  • De Troyer A, Estenne M (1984) Coordination between rib cage muscles and diaphragm during quiet breathing in humans. J Appl Physiol 57:899–906

    PubMed  Google Scholar 

  • Dubois P, Jamart J, Machiels J et al (1994) Prognosis of severely hypoxemic patients receiving long-term oxygen therapy. Chest 105:469–474

    Article  CAS  PubMed  Google Scholar 

  • Elcadi GH, Forsman M, Crenshaw AG (2011) The relationship between oxygenation and myoelectric activity in the forearm and shoulder muscles of males and females. Eur J Appl Physiol 111:647–658

    Article  PubMed  Google Scholar 

  • Farkas GA, McCormick KM, Gosselin LE (2007) Episodic hypoxia exacerbates respiratory muscle dysfunction in DMD(mdx) mice. Muscle Nerve 36:708–710

    Article  PubMed  Google Scholar 

  • Gorman RB, McKenzie DK, Gandevia SC (1999) Task failure, breathing discomfort and CO2 accumulation without fatigue during inspiratory resistive loading in humans. Respir Physiol 115:273–286

    Article  CAS  PubMed  Google Scholar 

  • Houssiere A, Najem B, Ciarka A et al (2005) Chemoreflex and metaboreflex control during static hypoxic exercise. Am J Physiol Heart Circ Physiol 288:H1724–H1729

    Article  CAS  PubMed  Google Scholar 

  • Hudson AL, Gandevia SC, Butler JE (2007) The effect of lung volume on the co-ordinated recruitment of scalene and sternomastoid muscles in humans. J Physiol 584:261–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain SN (1996) Regulation of ventilatory muscle blood flow. J Appl Physiol 81(4):1455–1468

  • Jardim J, Farkas G, Prefaut C et al (1981) The failing inspiratory muscles under normoxic and hypoxic conditions. Am Rev Respir Dis 124:274–279

    CAS  PubMed  Google Scholar 

  • Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 18:111–129

    Article  CAS  PubMed  Google Scholar 

  • Katayama K, Suzuki Y, Hoshikawa M et al (2015) Hypoxia exaggerates inspiratory accessory muscle deoxygenation during hyperpnoea. Resp Physiol Neurobiol 211:1–8

    Article  CAS  Google Scholar 

  • Legrand A, Schneider E, Gevenois P-A, De Troyer A (2003) Respiratory effects of the scalene and sternomastoid muscles in humans. J Appl Physiol 94:1467–1472

    Article  PubMed  Google Scholar 

  • Mal H, Armenqaud MHAM (1988) Clinical importance of inspiratory muscle fatigue in acutely ill patients. J Crit Care 3:267–274

    Article  Google Scholar 

  • Mathur S, Sheel AW, Road JD, Reid WD (2010) Delayed onset muscle soreness after inspiratory threshold loading in healthy adults. Cardiopulm Phys Ther J 21:5–12

  • Mayock DE, Standaert TA, Woodrum DE (1992) Effect of inspiratory resistive loaded breathing and hypoxemia on diaphragmatic function in the piglet. J Appl Physiol 73:1888–1893

    CAS  PubMed  Google Scholar 

  • McKenzie DK, Allen GM, Butler JE, Gandevia SC (1997) Task failure with lack of diaphragm fatigue during inspiratory resistive loading in human subjects. J Appl Physiol 82:2011–2019

    CAS  PubMed  Google Scholar 

  • Miller MR, Hankinson J, Brusasco V et al (2005) Standardisation of spirometry. Eur Respir J 26:319–338

    Article  CAS  PubMed  Google Scholar 

  • Miura H, McCully K, Nioka S, Chance B (2004) Relationship between muscle architectural features and oxygenation status determined by near infrared device. Eur J Appl Physiol 91:273–278

    Article  PubMed  Google Scholar 

  • Mizuno M, Secher NH (1989) Histochemical characteristics of human expiratory and inspiratory intercostal muscles. J Appl Physiol 67:592–598

    CAS  PubMed  Google Scholar 

  • Moalla W, Merzouk A, Costes F et al (2006) Muscle oxygenation and EMG activity during isometric exercise in children. J Sports Sci 24:1195–1201

    Article  PubMed  Google Scholar 

  • Murthy G, Hargens AR, Lehman S, Rempel DM (2001) Ischemia causes muscle fatigue. J Orthop Res 19:436–440

    Article  CAS  PubMed  Google Scholar 

  • Parthasarathy S, Jubran A, Laghi F, Tobin MJ (2007) Sternomastoid, rib cage, and expiratory muscle activity during weaning failure. J Appl Physiol 103:140–147

    Article  PubMed  Google Scholar 

  • Reid W, Yamabayashi C, Sheel AW, Shadgan B, Road JD (2013) Muscle oxygenation not maintained in sternomastoid during incremental inspiratory loading in COPD patients. Cardiopulm Phys Ther J 24(4):36

  • Robertson JCH, Foster GH, Johnson JRL (1977) The relationship of respiratory failure to the oxygen consumption of, lactate production by, and distribution of blood flow among respiratory muscles during increasing inspiratory resistance. J Clin Invest 59(1):31–42

  • Rohrbach M, Perret C, Kayser B, Boutellier U, Spengler CM (2003) Task failure from inspiratory resistive loaded breathing: a role for inspiratory muscle fatigue? Eur J Appl Physiol 90:405–410

    Article  PubMed  Google Scholar 

  • Roussos C (1985) Function and fatigue of respiratory muscles. Chest 88:124S–132S

    Article  CAS  PubMed  Google Scholar 

  • Saboisky JP, Gorman RB, De Troyer A et al (2007) Differential activation among five human inspiratory motoneuron pools during tidal breathing. J Appl Physiol 102:772–780

    Article  PubMed  Google Scholar 

  • Sayli O, Akin A, Cotuk H et al (2014) Correlation analysis between surface electromyography and continuous wave near infrared spectroscopy parameters during isometric exercise to volitional fatigue. Turk J Electr Eng Comput Sci 22:780–793

    Article  Google Scholar 

  • Segizbaeva MO, Donina ZA, Timofeev NN et al (2013) EMG analysis of human inspiratory muscle resistance to fatigue during exercise. Adv Exp Med Biol 788:197–205

    Article  CAS  PubMed  Google Scholar 

  • Shadgan B, Guenette JA, Sheel AW, Reid WD (2011) Sternocleidomastoid muscle deoxygenation in response to incremental inspiratory threshold loading measured by near infrared spectroscopy. Respir Physiol Neurobiol 178:202–209

    Article  PubMed  Google Scholar 

  • Sheel AW, Derchak PA, Morgan BJ et al (2001) Fatiguing inspiratory muscle work causes reflex reduction in resting leg blood flow in humans. J Physiol 537:277–289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taelman J, Vanderhaegen J, Robijns M et al (2011) Estimation of muscle fatigue using surface electromyography and near-infrared spectroscopy. Adv Exp Med Biol. pp 353–359

  • Verges S, Bachasson D, Wuyam B (2010) Effect of acute hypoxia on respiratory muscle fatigue in healthy humans. Respir Res 11:109

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogiatzis I, Georgiadou O, Koskolou M et al (2007) Effects of hypoxia on diaphragmatic fatigue in highly trained athletes. J Physiol 581:299–308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogiatzis I, Athanasopoulos D, Habazettl H et al (2009) Intercostal muscle blood flow limitation in athletes during maximal exercise. J Physiol 587:3665–3677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wahr JA, Tremper KK, Samra S, Delpy DT (1996) Near-infrared spectroscopy: theory and applications. J Cardiothorac Vasc Anesth 10:406–418

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Yoshikawa T, Hara T et al (2006) Which common NIRS variable reflects muscle estimated lactate threshold most closely? Appl Physiol Nutr Metab 31:612–620

    Article  CAS  PubMed  Google Scholar 

  • Yamada E, Kusaka T, Arima N et al (2008) Relationship between muscle oxygenation and electromyography activity during sustained isometric contraction. Clin Physiol Funct Imaging 28:216–221

    Article  PubMed  Google Scholar 

  • Yamamoto Y, Hoshikawa Y, Miyashita M (1996) Effects of acute exposure to simulated altitude on heart rate variability during exercise. J Appl Physiol 81(3):1223–1229

    CAS  PubMed  Google Scholar 

  • Zattara-Hartmann MC, Jammes Y (1996) Cardiorespiratory response to progressive leg exercise under acute normobaric hypoxia. Arch Physiol Biochem 104:272–281

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank all subjects for their participation. We are also very appreciative of the valuable assistance given by Carmen Ma during data collection and Dr. Salem Bahubeshi for ECG monitoring. This study was supported by a grant and scholarship funding from Princess Nora bint Abdul Rahman University.

Author information

Authors and Affiliations

  1. Department of Physical Therapy, University of British Columbia (UBC), Vancouver, Canada

    Nada Basoudan & Jordan A. Guenette

  2. College of Health and Rehabilitation Sciences, Princess Nora Bint Abdul Rahman University, Riyadh, Saudi Arabia

    Nada Basoudan

  3. International Collaboration on Repair Discoveries, Vancouver, Canada

    Babak Shadgan

  4. Centre for Heart Lung Innovation, UBC and St. Paul’s Hospital, Vancouver, Canada

    Jordan A. Guenette

  5. Division of Respiratory Medicine, Department of Medicine, UBC, Vancouver, Canada

    Jeremy Road

  6. Physical Therapy Department, University of Toronto, Toronto, Canada

    W. Darlene Reid

Authors
  1. Nada Basoudan
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  2. Babak Shadgan
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  3. Jordan A. Guenette
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  4. Jeremy Road
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  5. W. Darlene Reid
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Corresponding author

Correspondence to Nada Basoudan.

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The authors declare that they have no conflict of interest.

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Communicated by Jean-René Lacour.

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Basoudan, N., Shadgan, B., Guenette, J.A. et al. Effect of acute hypoxia on inspiratory muscle oxygenation during incremental inspiratory loading in healthy adults. Eur J Appl Physiol 116, 841–850 (2016). https://doi.org/10.1007/s00421-016-3334-x

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  • DOI: https://doi.org/10.1007/s00421-016-3334-x

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