Skip to main content

Advertisement

SpringerLink
Log in

Effects of acute mild hypoxia on cerebral blood flow in pilots

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Background

Pilots often face and need to overcome a diverse range of unfavorable conditions, of which hypoxic exposure is the most common. Studies have reported that hypoxia can induce a decrease in cerebral blood flow (CBF) in the brains of both humans and animals. Hypoxia and the associated cerebral hemodynamic changes can contribute to cognitive performance deficits that may endanger flight safety and increase the risk of accidents.

Aim

In this study, we aimed to identify region-specific alterations in CBF in male pilots after exposure to hypoxia.

Material and methods

We used 3D pseudo-continuous arterial spin labeling sequences in 35 healthy male pilots (mean age: 30.6 ± 4.82 years) under simulated hypoxic conditions with a 3.0-T magnetic resonance imaging scanner. The generated CBF maps were measured and averaged in several regions of interest.

Results

Hypoxia decreased CBF in various brain regions, including the right temporal and bilateral occipital lobes, the anterior and posterior lobes of the cerebellum, the culmen and declive, and the inferior semilunar lobule of the cerebellum.

Conclusion

These changes may impact the functional activity of the brains of pilots experiencing hypoxia in flight, but the related mechanisms require further investigation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Not applicable.

References

  1. Bouak F, Vartanian O, Hofer K, Cheung B (2018) Acute mild hypoxic hypoxia effects on cognitive and simulated aircraft pilot performance. Aerosp Med Hum Perform 89:526–535. https://doi.org/10.3357/AMHP.5022.2018

    Article  PubMed  Google Scholar 

  2. Ebmeier KP, Cavanagh JT, Moffoot AP, Glabus MF, O’Carroll RE, Goodwin GM (1997) Cerebral perfusion correlates of depressed mood. Br J Psychiatry 170:77–81. https://doi.org/10.1192/bjp.170.1.77

    Article  CAS  PubMed  Google Scholar 

  3. Coutsoumpos A, Patel S, Teruya TH, Chiriano J, Bianchi C, Abou-Zamzam AM Jr (2014) Carotid duplex ultrasound changes associated with left ventricular assist devices. Ann Vasc Surg 28:1030.e7–1030.e11. https://doi.org/10.1016/j.avsg.2013.11.013

    Article  Google Scholar 

  4. Busch KJ, Kiat H, Stephen M, Simons M, Avolio A, Morgan MK (2016) Cerebral hemodynamics and the role of transcranial Doppler applications in the assessment and management of cerebral arteriovenous malformations. J Clin Neurosci 30:24–30. https://doi.org/10.1016/j.jocn.2016.01.029

    Article  PubMed  Google Scholar 

  5. Mamalyga ML, Mamalyga LM (2017) Effect of progressive heart failure on cerebral hemodynamics and monoamine metabolism in CNS. Bull Exp Biol Med 163:307–312. https://doi.org/10.1007/s10517-017-3791-1

    Article  CAS  PubMed  Google Scholar 

  6. Jezzard P, Chappell MA, Okell TW (2018) Arterial spin labeling for the measurement of cerebral perfusion and angiography. J Cereb Blood Flow Metab 38:603–626. https://doi.org/10.1177/0271678X17743240

    Article  PubMed  Google Scholar 

  7. Telischak NA, Detre JA, Zaharchuk G (2015) Arterial spin labeling MRI: clinical applications in the brain. J Magn Reson Imaging 41:1165–1180. https://doi.org/10.1002/jmri.24751

    Article  PubMed  Google Scholar 

  8. Giani L, Lovati C, Corno S, Laganà MM, Baglio F, Mariani C (2019) Cerebral blood flow in migraine without aura: ASL-MRI case control study. Neurol Sci 40:183–184. https://doi.org/10.1007/s10072-019-03806-6

    Article  PubMed  Google Scholar 

  9. Yadav SK, Kumar R, Macey PM, Richardson HL, Wang DJ, Woo MA, Harper RM (2013) Regional cerebral blood flow alterations in obstructive sleep apnea. Neurosci Lett 555:159–164. https://doi.org/10.1016/j.neulet.2013.09.033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Liu W, Liu J, Lou X, Zheng D, Wu B, Wang DJ, Ma L (2017) A longitudinal study of cerebral blood flow under hypoxia at high altitude using 3D pseudo-continuous arterial spin labeling. Sci Rep 7:43246. https://doi.org/10.1038/srep43246

    Article  PubMed  PubMed Central  Google Scholar 

  11. Villien M, Bouzat P, Rupp T, Robach P, Lamalle L, Troprès I, Estève F, Krainik A, Lévy P, Warnking JM, Verges S (2013) Changes in cerebral blood flow and vasoreactivity to CO2 measured by arterial spin labeling after 6 days at 4350 m. Neuroimage 15:272–279. https://doi.org/10.1016/j.neuroimage.2013.01.066

    Article  Google Scholar 

  12. Harris AD, Murphy K, Diaz CM, Saxena N, Hall JE, Liu TT, Wise RG (2013) Cerebral blood flow response to acute hypoxic hypoxia. NMR Biomed 26:1844–1852. https://doi.org/10.1002/nbm.3026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lawley JS, Macdonald JH, Oliver SJ, Mullins PG (2017) Unexpected reductions in regional cerebral perfusion during prolonged hypoxia. J Physiol 595:935–947. https://doi.org/10.1113/JP272557

    Article  CAS  PubMed  Google Scholar 

  14. Kasai N, Kojima C, Goto K (2018) Metabolic and performance responses to sprint exercise under hypoxia among female athletes. Sports Med Int Open 2:E71–E78. https://doi.org/10.1055/a-0628-6100

    Article  PubMed  PubMed Central  Google Scholar 

  15. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98:676–682. https://doi.org/10.1073/pnas.98.2.676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62:782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015

    Article  PubMed  Google Scholar 

  17. Friston KJ, Holmes AP, Worsley KJ, Firth J-P CD, Frackowiak RSJ (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210. https://doi.org/10.1002/hbm.460020402

    Article  Google Scholar 

  18. Nel J, Franconi F, Joudiou N, Saulnier P, Gallez B, Lemaire L (2019) Lipid nanocapsules as in vivo oxygen sensors using magnetic resonance imaging. Mater Sci Eng C Mater Biol Appl 101:396–403. https://doi.org/10.1016/j.msec.2019.03.104

    Article  CAS  PubMed  Google Scholar 

  19. Sumiyoshi A, Suzuki H, Shimokawa H, Kawashima R (2012) Neurovascular uncoupling under mild hypoxic hypoxia: an EEG–fMRI study in rats. J Cereb Blood Flow Metab 32:1853–1858. https://doi.org/10.1038/jcbfm.2012.111

    Article  PubMed  PubMed Central  Google Scholar 

  20. Alisauskaite N, Wang-Leandro A, Dennler M, Kantyka M, Ringer SK, Steffen F, Beckmann K (2019) Conventional and functional magnetic resonance imaging features of late subacute cortical laminar necrosis in a dog. J Vet Intern Med 33:1759–1765. https://doi.org/10.1111/jvim.15526

    Article  PubMed  PubMed Central  Google Scholar 

  21. Cahill LS, Zhou YQ, Seed M, Macgowan CK, Sled JG (2014) Brain sparing in fetal mice: BOLD MRI and Doppler ultrasound show blood redistribution during hypoxia. J Cereb Blood Flow Metab 34:1082–1088. https://doi.org/10.1038/jcbfm.2014.62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Temme LA, Still DL, Acromite MT (2010) Hypoxia and flight performance of military instructor pilots in a flight simulator. Aviat Space Environ Med 81:654–659. https://doi.org/10.3357/asem.2690.2010

    Article  PubMed  Google Scholar 

  23. Dormanesh B, Vosouqhi K, Akhoundi FH, Mehrpour M, Fereshtehnejad SM, Esmaeili S, Sabet AS (2016) Carotid duplex ultrasound and transcranial Doppler findings in commercial divers and pilots. Neurol Sci 37:1911–1916. https://doi.org/10.1007/s10072-016-2674-y

    Article  PubMed  Google Scholar 

  24. Poulin MJ, Liang PJ, Robbins P (1985) Dynamics of the cerebral blood flow response to step changes in end-tidal PCO2 and PO2 in humans. J Appl Physiol 81:1084–1095. https://doi.org/10.1152/jappl.1996.81.3.1084

    Article  Google Scholar 

  25. Lee SM, Kwon S, Lee YJ (2019) Diagnostic usefulness of arterial spin labeling in MR negative children with new onset seizures. Seizure 65:151–158. https://doi.org/10.1016/j.seizure.2019.01.024

    Article  PubMed  Google Scholar 

  26. Keil VC, Hartkamp NS, Connolly DJA, Morana G, Dremmen MHG, Mutsaerts HJMM, Lequin MH (2019) Added value of arterial spin labeling magnetic resonance imaging in pediatric neuroradiology: pitfalls and applications. Pediatr Radiol 49:245–253. https://doi.org/10.1007/s00247-018-4269-7

    Article  PubMed  Google Scholar 

  27. Ho ML (2018) Arterial spin labeling: clinical applications. J Neuroradiol 45:276–289. https://doi.org/10.1016/j.neurad.2018.06.003

    Article  PubMed  Google Scholar 

  28. Austin BP, Nair VA, Meier TB, Xu G, Rowley HA, Carlsson CM, Johnson SC, Prabhakaran V (2011) Effects of hypoperfusion in Alzheimer’s disease. J Alzheimers Dis 26:123–133. https://doi.org/10.3233/JAD-2011-0010

    Article  PubMed  PubMed Central  Google Scholar 

  29. Duong TQ (2007) Cerebral blood flow and BOLD fMRI responses to hypoxia in awake and anesthetized rats. Brain Res 1135:186–194. https://doi.org/10.1016/j.brainres.2006.11.097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ainslie PN, Poulin MJ (2014) Ventilatory, cerebrovascular, and cardiovascular interactions in acute hypoxia: regulation by carbon dioxide. J Appl Physiol 97:149–159. https://doi.org/10.1152/japplphysiol.01385.2003

    Article  Google Scholar 

  31. Cohen PJ, Alexander SC, Smith TC, Reivich M, Wollman H (1967) Effects of hypoxia and normocarbia on cerebral blood flow and metabolism in conscious man. J Appl Physiol 23:183–189. https://doi.org/10.1152/jappl.1967.23.2.183

    Article  CAS  PubMed  Google Scholar 

  32. Poulin MJ, Fatemian M, Tansley JG, O'Connor DF, Robbins PA (2002) Changes in cerebral blood flow during and after 48 h of both isocapnic and poikilocapnic hypoxia in humans. Exp Physiol 87:633–642. https://doi.org/10.1113/eph8702437

    Article  PubMed  Google Scholar 

  33. Curtelin D, Morales-Alamo D, Torres-Peralta R, Rasmussen P, Martin-Rincon M, Perez-Valera M, Siebenmann C, Pérez-Suárez I, Cherouveim E, Sheel AW, Lundby C, Calbert JA (2018) Cerebral blood flow, frontal lobe oxygenation and intra-arterial blood pressure during sprint exercise in normoxia and severe acute hypoxia in humans. J Cereb Blood Flow Metab 38:136–150. https://doi.org/10.1177/0271678X17691986

    Article  PubMed  Google Scholar 

  34. Sicard KM, Duong TQ (2005) Effects of hypoxia, hyperoxia, and hypercapnia on baseline and stimulus-evoked BOLD, CBF, and CMRO2 in spontaneously breathing animals. Neuroimage 25:850–858. https://doi.org/10.1016/j.neuroimage.2004.12.010

    Article  PubMed  Google Scholar 

  35. Alosco ML, Gunstad J, Jerskey BA, Xu X, Clark US, Hassenstab J, Cote DM, Walsh EG, Labbe DR, Hoge R, Cohen RA, Sweet LH (2013) The adverse effects of reduced cerebral perfusion on cognition and brain structure in older adults with cardiovascular disease. Brain Behav 3:626–636. https://doi.org/10.1002/brb3.171

    Article  PubMed  PubMed Central  Google Scholar 

  36. Caldwell JA Jr, Lewis JA (1995) The feasibility of collecting in-flight EEG data from helicopter pilots. Aviat Space Environ Med 66:883–889

    PubMed  Google Scholar 

  37. Bangen KJ, Werhane ML, Weigand AJ, Edmonds EC, Wood LD, Thomas KR, Nation DA, Evangelista ND, Clark AL, Liu TT, Bondi MW (2018) Reduced regional cerebral blood flow relates to poorer cognition in older adults with type 2 diabetes. Front Aging Neurosci 10:270. https://doi.org/10.3389/fnagi.2018.00270

    Article  PubMed  PubMed Central  Google Scholar 

  38. Gainotti G (2014) Why are the right and left hemisphere conceptual representations different? Behav Neurol 2014:603134–603110. https://doi.org/10.1155/2014/603134

    Article  PubMed  PubMed Central  Google Scholar 

  39. Shulman GL, Pope DLW, Astafiev SV, McAvoy MP, Snyder AZ, Corbetta M (2010) Right hemisphere dominance during spatial selective attention and target detection occurs outside the dorsal frontoparietal network. J Neurosci 30:3640–3651. https://doi.org/10.1523/JNEUROSCI.4085-09.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Causse M, Chua ZK, Rémy F (2019) Influences of age, mental workload, and flight experience on cognitive performance and prefrontal activity in private pilots: a fNIRS study. Sci Rep 9:7688. https://doi.org/10.1038/s41598-019-44082-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors would like to thank GE Healthcare China in Beijing for support and Yu Tian, Mingyang Ding, and Ling Fang for the assistance in the data collection. We would like to thank Editage (www.editage.cn) for the English language editing.

Author information

Authors and Affiliations

  1. Department of MRI, The First Affiliated Hospital of Zhengzhou University, No.1 Jianshe Dong Road, Erqi District, Zhengzhou, Henan Province, China

    Jie Liu, Shujian Li, Yong Zhang & Jingliang Cheng

  2. GE Healthcare China, Floor 1, Yongchang North Road, Beijing Economic and Technological Development Zone, Beijing, China

    Long Qian

  3. Department of Air Duty, The Air Force General Hospital in Beijing, No. 30 Fucheng Road, Haidian District, Beijing, West Diaoyutai, China

    Xianrong Xu

  4. Department of Radiology, The Air Force General Hospital in Beijing, No. 30 Fucheng Road, Haidian District, Beijing, West Diaoyutai, China

    Wanshi Zhang

Authors
  1. Jie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shujian Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Long Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianrong Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jingliang Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wanshi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Jie Liu: data curation, formal analysis, investigation, methodology, and writing—original draft; Shujian Li: formal analysis and writing—review and editing; Long Qian: data curation, formal analysis, software, and validation; Xianrong Xu: conceptualization and resources; Yong Zhang: writing—review and editing; Jingliang: project administration and writing—review and editing; Wanshi Zhang: conceptualization, investigation, methodology, and writing—review and editing.

Corresponding author

Correspondence to Jingliang Cheng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

All procedures were conducted in accordance with the tenets of the Declaration of Helsinki and were approved by the Institutional Review Board of the First Affiliated Hospital of Zhengzhou University.

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Consent for publication

Not applicable.

Code availability

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, J., Li, S., Qian, L. et al. Effects of acute mild hypoxia on cerebral blood flow in pilots. Neurol Sci 42, 673–680 (2021). https://doi.org/10.1007/s10072-020-04567-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-020-04567-3

Keywords

Search

Navigation