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Physiology of Human Hemorrhage and Compensation

Victor A. Convertino, Natalie J. Koons, Mithun R. Suresh

10.1002/cphy.c200016

Source: Volume 11, Issue 2, April 2021

Published online: February 2021

Full Article on Wiley Online Library



Abstract

Hemorrhage is a leading cause of death following traumatic injuries in the United States. Much of the previous work in assessing the physiology and pathophysiology underlying blood loss has focused on descriptive measures of hemodynamic responses such as blood pressure, cardiac output, stroke volume, heart rate, and vascular resistance as indicators of changes in organ perfusion. More recent work has shifted the focus toward understanding mechanisms of compensation for reduced systemic delivery and cellular utilization of oxygen as a more comprehensive approach to understanding the complex physiologic changes that occur following and during blood loss. In this article, we begin with applying dimensional analysis for comparison of animal models, and progress to descriptions of various physiological consequences of hemorrhage. We then introduce the complementary side of compensation by detailing the complexity and integration of various compensatory mechanisms that are activated from the initiation of hemorrhage and serve to maintain adequate vital organ perfusion and hemodynamic stability in the scenario of reduced systemic delivery of oxygen until the onset of hemodynamic decompensation. New data are introduced that challenge legacy concepts related to mechanisms that underlie baroreflex functions and provide novel insights into the measurement of the integrated response of compensation to central hypovolemia known as the compensatory reserve. The impact of demographic and environmental factors on tolerance to hemorrhage is also reviewed. Finally, we describe how understanding the physiology of compensation can be translated to applications for early assessment of the clinical status and accurate triage of hypovolemic and hypotensive patients. © 2021 American Physiological Society. Compr Physiol 11:1531‐1574, 2021.

Figure 1. Figure 1. Relationship between reductions in central venous pressure and stroke volume during progressive reductions in central blood volume induced by lower body negative pressure in a group of healthy human subjects. Reused, with permission, from Mack GW, et al., 1993 290.
Figure 2. Figure 2. The response of right atrial pressure (A), cardiac output (B), heart rate (C), total peripheral resistance (D), and blood pressure (E) following voluntary blood loss (venesection) causing fainting in a human subject. Redrawn from Barcroft H, et al., 1944 12.
Figure 3. Figure 3. Comparisons of mean arterial blood pressures in rats (closed circles, solid lines) and humans (open circles, broken lines) during progressive lower body negative pressure (A) and controlled hemorrhage (B). LBNP and hemorrhage data for rats were extracted from Tipton CM, et al., 1982 431. LBNP data for humans were extracted from Rickards CA, et al., 2011 350, and hemorrhage data for humans were extracted from Convertino VA, et al., 2015 79.
Figure 4. Figure 4. Average stroke volume reductions as percent change (%Δ) from baseline in 14 baboons during four steps of progressive controlled hemorrhage (red circles and lines) and LBNP (black circles and lines) compared with 117 humans (green circles and lines). Calculated slope predicts a 2% reduction in stroke volume for every 1% reduction in blood volume. Modified, with permission, from Hinojosa‐Laborde C, et al., 2014 208.
Figure 5. Figure 5. Responses of heart rate (broken line) and mean arterial pressure (solid line) during graded LBNP in a single subject demonstrating the onset of severe hypotension and bradycardia with hemodynamic decompensation. Reproduced, with permission, from Convertino VA, 1993 67.
Figure 6. Figure 6. Conceptual diagram of the relationship between oxygen delivery (DO2) and the consumption of oxygen (Vo2) during hemorrhage. OER, oxygen extraction ratio; SvO2, mixed venous oxygen saturation; DO2crit, level of DO2 at which anaerobic metabolism begins. Reproduced, with permission, from Convertino VA and Koons NJ, 2020 80.
Figure 7. Figure 7. Kaplan‐Meier survival curves demonstrating differences in tolerance times to hemodynamic decompensation in human subjects classified as “low” and “high” tolerance to progressive hemorrhage simulated by LBNP. Modified, with permission, from Schiller AM, et al., 2017 387.
Figure 8. Figure 8. Recording of the temporal relationship of repeating oscillatory pattern between arterial blood pressure (BP) and muscle sympathetic nerve activity (MSNA) obtained from a healthy human during simulated hemorrhage of an estimated 25% blood loss induced by 70 mmHg LBNP.
Figure 9. Figure 9. Illustration of the traditionally viewed concept of cerebral autoregulation (black line) compared to the pressure‐dependent relationship of cerebrovascular control (red line). Redrawn, with permission, from Lucas SJE, et al., 2010 286.
Figure 10. Figure 10. Time course of systemic peripheral vascular resistance (A), heart rate (B), mean arterial pressure (C), sympathetic nerve activity (D), and cardiac baroreflex sensitivity (E) during progressive LBNP in individuals with low tolerance (LT, n = 59, open triangle, broken lines) and high tolerance (HT, n = 113, closed circle, solid lines). Onset of hemodynamic decompensation with pronounced hypotension is marked by the vertical red broken lines for the LT group (line 1) and HT group (line 2). Data, with permission, extracted from Xiang L, et al., 2018 473.
Figure 11. Figure 11. Illustration of changes in features of an integrated arterial waveform when progressing from a normal blood volume to a state of central hypovolemia such as hemorrhage. The red line indicates the integrated waveform that would be clinically observed and recorded. Modified, with permission, from Convertino VA and Schiller, 2017 96 and Convertino VA, et al., 2016 100.
Figure 12. Figure 12. Kaplan‐Meier survival curves analysis used to compare population tolerance times to hemodynamic decompensation in males and females who underwent progressive reductions in central hypovolemia. Modified, with permission, from Schiller AM, et al., 2017 387.
Figure 13. Figure 13. Relationship between maximal oxygen uptake (Vo2max) and LBNP tolerance in a group of five habitual runners (open circles) and five sedentary nonrunners (closed circles). Broken line represents best fit of linear regression. Data extracted from Luft UC, et al., 1976 288.
Figure 14. Figure 14. Relationship between blood volume and maximal oxygen uptake (Vo2max) in a group of six aerobically fit subjects (closed circles) and five unfit subjects (open circles). Broken line represents best fit of linear regression. Redrawn, with permission, from Mack GW, et al., 1987 291.
Figure 15. Figure 15. Conceptual illustration of the Frank‐Starling relationship between end‐diastolic volume and stroke volume in endurance athletes (EA) and nonathletes (NA). Figure depicts how the same reduction (Δ moving to the left) in end‐diastolic volume (EDV; vertical red broken lines) translates to a greater reduction in stroke volume in EA (ΔSV1) compared to the smaller reduction in stroke volume in NA (ΔSV2). Redrawn, with permission, from Levine B, 1993 262.
Figure 16. Figure 16. Kaplan‐Meier survival curves analysis used to compare tolerance times to hemodynamic decompensation in humans who underwent progressive reductions in central hypovolemia induced by LBNP in a thermoneutral state (gray line) and heat stress designed to cause a 1 °C elevation in core temperature (black broken line). Reproduced, with permission, from Schlader ZJ, et al., 2016 390.
Figure 17. Figure 17. Relationship between plasma volume and stroke volume during conditions of normal hydration (circles), dehydration (triangles), and hyperhydration (squares) during exposure to −50 mmHg LBNP in eight highly fit (HF; closed figures) and eight age‐matched low fit (LF; open figures) subjects. Figures are mean and lines are standard errors. Modified, with permission, from Convertino VA, 1993 67.
Figure 18. Figure 18. Average response of the compensatory reserve during progressive reductions in central blood volume induced by lower body negative pressure (LBNP) that elicited hemodynamic decompensation in normal (open circles) compared to elevated (closed circles) core temperature. Data demonstrate a significant reduction in tolerance associated with a more rapid depletion of the compensatory reserve with hyperthermia. Revised, with permission, from Gagnon D, et al., 2016 168.
Figure 19. Figure 19. Individual compensatory reserve responses for two subjects before and during stepwise withdrawal of blood volume (in mL, black circles) and after reinfusion of total amount of withdrawn blood volume (red circles). Linear regression relationships are shown as dashed lines. Data extracted, with permission, from Convertino VA, et al., 2015 79.
Figure 20. Figure 20. Relationship that depicts a greater rate of reduction in compensatory reserve is associated with a greater hypotension during central hypovolemia induced in seven men by LBNP (red circles and broken line). Breathing with application of intrathoracic pressure regulation (IPR) therapy (green circles) in the same subjects slows the rate of compensatory reserve reduction and restores blood pressure. Data extracted from Poh Y, et al., 2014 330.
Figure 21. Figure 21. Summary illustration of the continuum of physiological events initiated by hemorrhage. Hypovolemic stimuli are translated through direct effects (blue broken arrows) or afferent nerve activation (blue solid lines). Compensatory responses are activated through cell metabolism, efferent nerve transmission (pink solid lines), or motor nerves innervating respiratory muscles and the diaphragm (orange solid line).


Figure 1. Relationship between reductions in central venous pressure and stroke volume during progressive reductions in central blood volume induced by lower body negative pressure in a group of healthy human subjects. Reused, with permission, from Mack GW, et al., 1993 290.


Figure 2. The response of right atrial pressure (A), cardiac output (B), heart rate (C), total peripheral resistance (D), and blood pressure (E) following voluntary blood loss (venesection) causing fainting in a human subject. Redrawn from Barcroft H, et al., 1944 12.


Figure 3. Comparisons of mean arterial blood pressures in rats (closed circles, solid lines) and humans (open circles, broken lines) during progressive lower body negative pressure (A) and controlled hemorrhage (B). LBNP and hemorrhage data for rats were extracted from Tipton CM, et al., 1982 431. LBNP data for humans were extracted from Rickards CA, et al., 2011 350, and hemorrhage data for humans were extracted from Convertino VA, et al., 2015 79.


Figure 4. Average stroke volume reductions as percent change (%Δ) from baseline in 14 baboons during four steps of progressive controlled hemorrhage (red circles and lines) and LBNP (black circles and lines) compared with 117 humans (green circles and lines). Calculated slope predicts a 2% reduction in stroke volume for every 1% reduction in blood volume. Modified, with permission, from Hinojosa‐Laborde C, et al., 2014 208.


Figure 5. Responses of heart rate (broken line) and mean arterial pressure (solid line) during graded LBNP in a single subject demonstrating the onset of severe hypotension and bradycardia with hemodynamic decompensation. Reproduced, with permission, from Convertino VA, 1993 67.


Figure 6. Conceptual diagram of the relationship between oxygen delivery (DO2) and the consumption of oxygen (Vo2) during hemorrhage. OER, oxygen extraction ratio; SvO2, mixed venous oxygen saturation; DO2crit, level of DO2 at which anaerobic metabolism begins. Reproduced, with permission, from Convertino VA and Koons NJ, 2020 80.


Figure 7. Kaplan‐Meier survival curves demonstrating differences in tolerance times to hemodynamic decompensation in human subjects classified as “low” and “high” tolerance to progressive hemorrhage simulated by LBNP. Modified, with permission, from Schiller AM, et al., 2017 387.


Figure 8. Recording of the temporal relationship of repeating oscillatory pattern between arterial blood pressure (BP) and muscle sympathetic nerve activity (MSNA) obtained from a healthy human during simulated hemorrhage of an estimated 25% blood loss induced by 70 mmHg LBNP.


Figure 9. Illustration of the traditionally viewed concept of cerebral autoregulation (black line) compared to the pressure‐dependent relationship of cerebrovascular control (red line). Redrawn, with permission, from Lucas SJE, et al., 2010 286.


Figure 10. Time course of systemic peripheral vascular resistance (A), heart rate (B), mean arterial pressure (C), sympathetic nerve activity (D), and cardiac baroreflex sensitivity (E) during progressive LBNP in individuals with low tolerance (LT, n = 59, open triangle, broken lines) and high tolerance (HT, n = 113, closed circle, solid lines). Onset of hemodynamic decompensation with pronounced hypotension is marked by the vertical red broken lines for the LT group (line 1) and HT group (line 2). Data, with permission, extracted from Xiang L, et al., 2018 473.


Figure 11. Illustration of changes in features of an integrated arterial waveform when progressing from a normal blood volume to a state of central hypovolemia such as hemorrhage. The red line indicates the integrated waveform that would be clinically observed and recorded. Modified, with permission, from Convertino VA and Schiller, 2017 96 and Convertino VA, et al., 2016 100.


Figure 12. Kaplan‐Meier survival curves analysis used to compare population tolerance times to hemodynamic decompensation in males and females who underwent progressive reductions in central hypovolemia. Modified, with permission, from Schiller AM, et al., 2017 387.


Figure 13. Relationship between maximal oxygen uptake (Vo2max) and LBNP tolerance in a group of five habitual runners (open circles) and five sedentary nonrunners (closed circles). Broken line represents best fit of linear regression. Data extracted from Luft UC, et al., 1976 288.


Figure 14. Relationship between blood volume and maximal oxygen uptake (Vo2max) in a group of six aerobically fit subjects (closed circles) and five unfit subjects (open circles). Broken line represents best fit of linear regression. Redrawn, with permission, from Mack GW, et al., 1987 291.


Figure 15. Conceptual illustration of the Frank‐Starling relationship between end‐diastolic volume and stroke volume in endurance athletes (EA) and nonathletes (NA). Figure depicts how the same reduction (Δ moving to the left) in end‐diastolic volume (EDV; vertical red broken lines) translates to a greater reduction in stroke volume in EA (ΔSV1) compared to the smaller reduction in stroke volume in NA (ΔSV2). Redrawn, with permission, from Levine B, 1993 262.


Figure 16. Kaplan‐Meier survival curves analysis used to compare tolerance times to hemodynamic decompensation in humans who underwent progressive reductions in central hypovolemia induced by LBNP in a thermoneutral state (gray line) and heat stress designed to cause a 1 °C elevation in core temperature (black broken line). Reproduced, with permission, from Schlader ZJ, et al., 2016 390.


Figure 17. Relationship between plasma volume and stroke volume during conditions of normal hydration (circles), dehydration (triangles), and hyperhydration (squares) during exposure to −50 mmHg LBNP in eight highly fit (HF; closed figures) and eight age‐matched low fit (LF; open figures) subjects. Figures are mean and lines are standard errors. Modified, with permission, from Convertino VA, 1993 67.


Figure 18. Average response of the compensatory reserve during progressive reductions in central blood volume induced by lower body negative pressure (LBNP) that elicited hemodynamic decompensation in normal (open circles) compared to elevated (closed circles) core temperature. Data demonstrate a significant reduction in tolerance associated with a more rapid depletion of the compensatory reserve with hyperthermia. Revised, with permission, from Gagnon D, et al., 2016 168.


Figure 19. Individual compensatory reserve responses for two subjects before and during stepwise withdrawal of blood volume (in mL, black circles) and after reinfusion of total amount of withdrawn blood volume (red circles). Linear regression relationships are shown as dashed lines. Data extracted, with permission, from Convertino VA, et al., 2015 79.


Figure 20. Relationship that depicts a greater rate of reduction in compensatory reserve is associated with a greater hypotension during central hypovolemia induced in seven men by LBNP (red circles and broken line). Breathing with application of intrathoracic pressure regulation (IPR) therapy (green circles) in the same subjects slows the rate of compensatory reserve reduction and restores blood pressure. Data extracted from Poh Y, et al., 2014 330.


Figure 21. Summary illustration of the continuum of physiological events initiated by hemorrhage. Hypovolemic stimuli are translated through direct effects (blue broken arrows) or afferent nerve activation (blue solid lines). Compensatory responses are activated through cell metabolism, efferent nerve transmission (pink solid lines), or motor nerves innervating respiratory muscles and the diaphragm (orange solid line).
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Article Title: Physiology of Human Hemorrhage and Compensation
 

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Victor A. Convertino, Natalie J. Koons, Mithun R. Suresh. Physiology of Human Hemorrhage and Compensation. Compr Physiol 2021, 11: 1531-1574. doi: 10.1002/cphy.c200016