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The Human Systemic and Cerebral Circulations: Contrasts in Structure and Function

Artery Research volume 26, pages 197–211 (2020)Cite this article

Abstract

Apart from peculiarities of the cerebral circulation, required to perfuse the brain with the subject erect, the principles established for function of the human systemic circulation (pulsatile flow at input and steady flow at output in capillaries) are identical to those established for other mammals. Assumption of the erect posture first as Homo erectus, then as Homo sapiens, conferred huge advantage to humans and led to command of the mammalian kingdom. But this required a circulation which could perfuse the brain securely against gravity in all positions of the body. This review covers what presently is known about the human cerebral circulation, and how such knowledge can be applied in some clinical conditions including development of dementia in older subjects, and in management of patients with elevation of intra-cranial pressure in younger subjects.

References

  1. Seymour RS, Bosiocic V, Snelling EP. Fossil skulls reveal that blood flow rate to the brain increased faster than brain volume during human evolution. R Soc Open Sci 2016;4:160305.

    Google Scholar 

  2. Nichols WW, O’Rourke MF, Vlachopoulos C. McDonald’s blood flow in arteries: Theoretical, Experimental and Clinical Principles. 6 ed., London: Arnold Hodder; 2011.

  3. O’Rourke MF, Hashimoto J. Mechanical factors in arterial aging: a clinical perspective. J Am Coll Cardiol 2007;50:1–13.

    Google Scholar 

  4. O’Rourke MF. The arterial pulse in health and disease. Am Heart J 1971;82:687–702.

    Google Scholar 

  5. Varsos GV, Richards HK, Kasprowicz M, Reinhard M, Smielewski P, Brady KM, et al. Cessation of diastolic cerebral blood flow velocity: the role of critical closing pressure. Neurocrit Care 2014;20:40–8.

    Google Scholar 

  6. O’Rourke MF. Pressure and flow in the arteries, M.D. thesis, University of Sydney, Sydney; 1966.

  7. O’Rourke MF, Safar ME. Relationship between aortic stiffening and microvascular disease in brain and kidney: cause and logic of therapy. Hypertension 2005;46:200–4.

    Google Scholar 

  8. Stone J, Johnstone DM, Mitrofanis J, O’Rourke M. The mechanical cause of age-related dementia (Alzheimer’s disease): the brain is destroyed by the pulse. J Alzheimers Dis 2015;44:355–73.

    Google Scholar 

  9. Bateman GA. Pulse-wave encephalopathy: a comparative study of the hydrodynamics of leukoaraiosis and normal-pressure hydrocephalus. Neuroradiology 2002;44:740–8.

    Google Scholar 

  10. Bateman GA. Pulse wave encephalopathy: a spectrum hypothesis incorporating Alzheimer’s disease, vascular dementia and normal pressure hydrocephalus. Med Hypotheses 2004;62:182–7.

    Google Scholar 

  11. Henry Feugeas MC, De Marco G, Peretti II, Godon-Hardy S, Fredy D, Claeys ES. Age-related cerebral white matter changes and pulse-wave encephalopathy: observations with three-dimensional MRI. Magn Reson Imaging 2005;23:929–37.

    Google Scholar 

  12. Kim MO, Li Y, Wei F, Wang J, O’Rourke MF, Adji A, et al. Normal cerebral vascular pulsations in humans: changes with age and implications for microvascular disease. J Hypertens 2017;35:2245–56.

    Google Scholar 

  13. Xing CY, Tarumi T, Meijers RL, Turner M, Repshas J, Xiong L, et al. Arterial pressure, heart rate, and cerebral hemodynamics across the adult life span. Hypertension 2017;69:712–20.

    Google Scholar 

  14. O’Rourke MF, Taylor MG. Vascular impedance of the femoral bed. Circ Res 1966;18:126–39.

    Google Scholar 

  15. Hashimoto J, Ito S. Aortic stiffness determines diastolic blood flow reversal in the descending thoracic aorta: potential implication for retrograde embolic stroke in hypertension. Hypertension 2013;62:542–9.

    Google Scholar 

  16. Kellie G. Appearance observed in the dissection of two individuals; death from cold and congestion of the brain. Trans Med Chir Soc Edinb 1824;1:84.

    Google Scholar 

  17. Monro A. Observations on structure and function of the nervous system. Edinburgh: Creech and Johnson; 1783.

  18. Kety S. Circulation of the blood: men and ideas. Bethesda: American Physiological Society; 1982.

  19. Cushing H. Concerning a definite regulatory mechanism of the vasomotor centre which controls blood pressure during cerebral compression. Bull Johns Hopkins Hosp 1901;12:290–2.

    Google Scholar 

  20. Cushing H. The third circulation and its channels, in studies in intracranial physiology and surgery. London: Oxford University Press; 1925, pp. 1–51.

  21. Lawley JS, Petersen LG, Howden EJ, Sarma S, Cornwell WK, Zhang R, et al. Effect of gravity and microgravity on intracranial pressure. J Phys 2017;595:2115–27.

    Google Scholar 

  22. Roberts DR, Albrecht MH, Collins HR, Asemani D, Chatterjee AR, Spampinato MV, et al. Effects of spaceflight on astronaut brain structure as indicated on MRI. N Engl J Med 2017;377:1746–53.

    Google Scholar 

  23. Stepanek J, Blue RS, Parazynski S. Space medicine in the era of civilian spaceflight. N Engl J Med 2019;380:1053–60.

    Google Scholar 

  24. Franklin SS, Gustin W, Wong ND, Larson MG, Weber MA, Kannel WB, et al. Hemodynamic patterns of age-related changes in blood pressure: The Framingham Heart Study. Circulation 1997;96:308–15.

    Google Scholar 

  25. Franklin SS, Khan SA, Wong ND, Larson MG, Levy D. Is pulse pressure useful in predicting risk for coronary heart Disease? The Framingham Heart Study. Circulation 1999;100:354–60.

    Google Scholar 

  26. Franklin SS, Larson MG, Khan SA, Wong ND, Leip EP, Kannel WB, et al. Does the relation of blood pressure to coronary heart disease risk change with aging? The Framingham Heart Study. Circulation 2001;103:1245–9.

    Google Scholar 

  27. Zhang Y, Agnoletti D, Protogerou AD, Topouchian J, Wang JG, Xu Y, et al. Characteristics of pulse wave velocity in elastic and muscular arteries: a mismatch beyond age. J Hypertens 2013;31:554–9.

    Google Scholar 

  28. Thomas F, Pannier B, Danchin N, Safar ME. Wave reflections in hypertension: role of sex, metabolic, and ethnic factors. J Hypertens 2019;37:555–62.

    Google Scholar 

  29. Namasivayam M, McEniery CM, Wilkinson IB, Yasmin, Cockroft JR, McDonnell BJ, et al. Different effects of vascular aging on ischemic predisposition in healthy men and women. Hypertension 2018;72:1294–300.

    Google Scholar 

  30. Murgo JP, Westerhof N, Giolma JP, Altobelli SA. Aortic input impedance in normal man: relationship to pressure wave forms. Circulation 1980;62:105–16.

    Google Scholar 

  31. O’Rourke MF, Avolio AP. Pulsatile flow and pressure in human systemic arteries. Studies in man and in a multi-branched model of the human systemic arterial tree. Circ Res 1980;46:363–72.

    Google Scholar 

  32. Adji A, Kachenoura N, Bollache E, Avolio AP, O’Rourke MF, Mousseaux E. Magnetic resonance and applanation tonometry for noninvasive determination of left ventricular load and ventricular vascular coupling in the time and frequency domain. J Hypertens 2016;34:1099–108.

    Google Scholar 

  33. Namasivayam M, Adji A, Lin L, Hayward CS, Feneley MP, O’Rourke MF, et al. Non-invasive quantification of ventricular contractility, arterial elastic function and ventriculo-arterial coupling from a single diagnostic encounter using simultaneous arterial tonometry and magnetic resonance imaging. Cardiovasc Eng Technol 2020;11:283–94.

    Google Scholar 

  34. Benetos A, Gautier S, Labat C, Salvi P, Valbusa F, Marino F, et al. Mortality and cardiovascular events are best predicted by low central/peripheral pulse pressure amplification but not by high blood pressure levels in elderly nursing home subjects: the PARTAGE (Predictive Values of Blood Pressure and Arterial Stiffness in Institutionalized Very Aged Population) study. J Am Coll Cardiol 2012;60:1503–11.

    Google Scholar 

  35. Xu TY, Staessen JA, Wei FF, Xu J, Li FH, Fan WX, et al. Blood flow pattern in the middle cerebral artery in relation to indices of arterial stiffness in the systemic circulation. Am J Hypertens 2012;25:319–24.

    Google Scholar 

  36. Cullen KM, Kócsi Z, Stone J. Pericapillary haem-rich deposits: evidence for microhaemorrhages in aging human cerebral cortex. J Cereb Blood Flow Metab 2005;25:1656–67.

    Google Scholar 

  37. Cullen KM, Kócsi Z, Stone J. Microvascular pathology in the aging human brain: evidence that senile plaques are sites of microhaemorrhages. Neurobiol Aging 2006;27:1786–96.

    Google Scholar 

  38. Evensen KB, Eide PK. Measuring intracranial pressure by invasive, less invasive or non-invasive means: limitations and avenues for improvement. Fluids Barriers CNS 2020;17:34.

    Google Scholar 

  39. Robba C, Bacigaluppi S, Cardim D, Donnelly J, Bertuccio A, Czosnyka M. Non-invasive assessment of intracranial pressure. Acta Neurol Scand 2016;134:4–21.

    Google Scholar 

  40. Kim MO, Adji A, O’Rourke MF, Avolio AP, Smielewski P, Pickard JD, et al. Principles of cerebral hemodynamics when intracranial pressure is raised: lessons from the peripheral circulation. J Hypertens 2015;33:1233–41.

    Google Scholar 

  41. Kim MO, Adji A, O’Rourke MF, Avolio AP, Smielewski P, Pickard JD, Change in pulsatile cerebral arterial pressure and flow waves as a therapeutic strategy? Acta Neurochir Suppl 2016;122:167–70.

  42. Kim MO, Eide PK, O’Rourke MF, Adji A, Avolio AP. Intracranial pressure waveforms are more closely related to central aortic than radial pressure waveforms: implications for pathophysiology and therapy. Acta Neurochir Suppl 2016;122:61–4.

    Google Scholar 

  43. Lim SS, Adji A, Agharazii M, O’Rourke M. MP-09 Can contour of the arterial pressure waveform be used to assess brain death in potential organ transplant donors? Pulse 2016;4:116–17.

  44. O’Rourke MF. A non-invasive method of estimating intracranial pressure. USA; 2016 (patent application no 15/614232).

  45. O’Rourke MF, Taylor MG. Vascular impedance of the femoral bed. Circ Res 1966;18:126–39.

    Google Scholar 

  46. Avolio AP, Chen SG, Wang RP, Zhang CL, Li MF, et al. Effects of aging on changing arterial compliance and left ventricular load in a northern Chinese urban community. Circulation 1983;68:50–8.

    Google Scholar 

  47. Avolio AP, Deng FQ, Li WQ, Luo YF, Huang ZD, Xing LF, et al. Effects of aging on arterial distensibility in populations with high and low prevalence of hypertension: comparison between urban and rural communities in China. Circulation 1985;71:202–10.

    Google Scholar 

  48. Castellani G, Zweifel C, Kim DJ, Carrera E, Radolovich DK, Smielewski P, et al. Plateau waves in head injured patients requiring neurocritical care. Neurocrit Care 2009;11:143–50.

    Google Scholar 

  49. Alexandrov AV. Cerebrovascular ultrasound in stroke prevention and treatment. Oxford: Wiley Blackwell Publishing; 2011, p. 83.

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Author information

Authors and Affiliations

  1. St Vincent’s Hospital/Clinic, UNSW Medicine, Sydney, Australia

    Michael O’Rourke & Audrey Adji

  2. Bosch Institute, Sydney University, Sydney, Australia

    Jonathan Stone

  3. Department of Cardiology, Victor Chang Cardiac Research Institute, Sydney, Australia

    Audrey Adji

  4. Faculty of Medicine, Health and Human Sciences, Macquarie University, Sydney, Australia

    Audrey Adji, Mi Ok Kim & Alberto Avolio

  5. The Shanghai Institute of Hypertension, Ruijin Hospital, Shanghai Jiaotong University of Medicine, Shanghai, China

    Yan Li & Ji Guang Wang

  6. Department of Neurosurgery, Oslo University Hospital - Rikshospitalet, Oslo, Norway

    Per Kristian Eide

  7. Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway

    Per Kristian Eide

  8. Cambridge Neuroscience, Addenbrooks Hospital, Cambridge, UK

    Marek Czosnyka

Authors
  1. Michael O’Rourke
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  2. Jonathan Stone
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  3. Audrey Adji
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  4. Mi Ok Kim
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  8. Per Kristian Eide
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  9. Marek Czosnyka
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Corresponding author

Correspondence to Michael O’Rourke.

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Peer review under responsibility of the Association for Research into Arterial Structure and Physiology

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O’Rourke, M., Stone, J., Adji, A. et al. The Human Systemic and Cerebral Circulations: Contrasts in Structure and Function. Artery Res 26, 197–211 (2020). https://doi.org/10.2991/artres.k.200704.001

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  • DOI: https://doi.org/10.2991/artres.k.200704.001

Keywords

Artery Research

ISSN: 1876-4401

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