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Significant Beat-to-Beat Hemodynamic Changes in Fetal Circulation: A Consequence of Abrupt Intrathoracic Pressure Variation Induced by Hiccup
Significant Beat-to-Beat Hemodynamic Changes in Fetal Circulation: A Consequence of Abrupt Intrathoracic Pressure Variation Induced by Hiccup Alex Levi, MD, Osnat Benvenisti, and Daniel David, MD, FACC, Kfar Sava, Israel
During routine fetal echocardiographic studies, we incidentally observed abrupt beat-to-beat changes in blood flow velocity and direction during bouts of hiccups in fetuses with a normal heart and regular and synchronized atrioventricular cardiac rhythm. The effect of hiccups on blood flow velocity and direction varied depending on the time of occurrence of hiccups during the cardiac cycle. In systole, a significant transient reduction of peak flow velocity occurred at the aortic and pulmonic valves, and brief tricuspid regurgitation appeared synchronously with each hiccup. In diastole, a transient reversal of flow
direction was recorded simultaneously with the hiccup at the aorta and ductus arteriosus, and acceleration of peak flow velocity was observed across the tricuspid and mitral valves. Throughout the entire cardiac cycle, marked blood flow acceleration was observed in the superior vena cava, inferior vena cava, and ostium secundum simultaneously with the hiccup. A direct transmission of briefly augmented, negative intrathoracic pressure to a compliant aorta and systemic veins appears to be a reasonable explanation for most of our observations. (J Am Soc Echocardiogr 2000;13:295-9.)
INTRODUCTION
pressure reduction on fetal intracardiac and great vessels blood flow velocity and direction.
Fetal intracardiac and intravascular blood flow dynamics have been the focus of some investigations. In the normal fetal heart, laminar antegrade blood flow profiles are recorded across the cardiac valves and the great vessels by color Doppler echocardiography.1-3 During routine fetal echocardiographic studies, we incidentally observed abrupt, and sometimes paradoxical, beat-to-beat changes in blood flow velocity and direction during bouts of fetal hiccups. Hiccups are an involuntary spasmodic and coordinated contraction of the inspiratory muscles. This forceful and involuntary inspiration causes transient intrathoracic pressure reduction.4,5 Ultrasonographic imaging of fetuses has documented the occurrence of hiccups from early gestation through parturition. The purpose of this study was to analyze the effects of hiccup-induced transient intrathoracic
From the Pediatric Cardiology Unit and the Department of Cardiology, Meir Hospital, Sapir Medical Center, Kfar Sava; and the Sackler School of Medicine, University of Tel Aviv; Israel. Reprint requests: Alex Levi, Department of Cardiology, Meir Hospital–Sapir Medical Center, Tschernichovsky St, Kfar Sava, 44281, Israel (E-mail: [email protected]). Copyright © 2000 by the American Society of Echocardiography. 0894-7317/2000 $12.00 + 0 27/1/103867 doi:10.1067/mje.2000.103867
METHODS Seventeen fetuses with normal cardiac anatomy and bouts of hiccups were identified during routine fetal echocardiographic studies of high-risk pregnancies.The gestational age varied between 20 and 30 weeks. All examinations were performed with an HP 2500 (Hewlett-Packard, Andover, Mass) echocardiographic system with a 5-MHz transducer. Blood flow velocity and direction across cardiac valves, ostium secundum, aortic arch, ductus arteriosus, descending aorta, and systemic veins were analyzed with the use of color Doppler and pulsed Doppler spectral analysis in 3 consecutive heart beats: the prehiccup beat, the hiccup beat, and the posthiccup beat.The interbeat flow velocity changes were compared by using analysis of variance and t test and were considered significant at P values <.05.
RESULTS All the fetuses presented regular and synchronized atrioventricular cardiac rhythms without premature contractions during the bouts of hiccups. The heart rates ranged between 110 and 143 bpm.The effects of a hiccup on intracardiac and great vessels blood 295
Journal of the American Society of Echocardiography April 2000
296 Levi, Benvenisti, David
Figure 1 Sagittal view of inferior vena cava (IVC) and superior vena cava (SVC) entering right atrium. A, Laminar flow in IVC (dark blue). B, Accelerated flow across IVC (light blue) and SVC (red) at hiccup. C, Spectral analysis. Accelerated flow across IVC at hiccup beat (asterisks).
Figure 2 Four-chamber view. A, No hiccup. B, Accelerated flow across ostium secundum (blue) at hiccup. C, Tricuspid regurgitation at hiccup. Note the anterior chest wall invagination at hiccup in B and C.
Table 1 Peak flow velocity (m/s) at hiccup
Inferior vena cava Superior vena cava Ostium secundum
Prehiccup beat
Hiccup beat
Posthiccup beat
P value
–0.35 ± –0.05 0.30 ± 0.05 0.20 ± 0.05
–1.80 ± –0.20 1.65 ± 0.20 0.50 ± 0.10
–0.35 ± –0.05 0.30 ± 0.05 0.20 ± 0.10
<.0001 <.0001 <.001
flow velocity and direction varied depending on when it occurred during the cardiac cycle. In general, throughout the entire cardiac cycle, marked blood flow acceleration was observed in the superior vena cava, inferior vena cava, and ostium secundum simultaneously with the hiccup beat (Figures 1 and 2,Table 1). Hiccup in Diastole 1. A significant and brief acceleration of peak blood flow velocity was observed across the tricuspid valve and, to a lesser degree, across the mitral valve during beat 2 compared with beats 1 and 3 (Table 2). 2. At the aortic arch, descending aorta, and ductus arteriosus, a transient reversal of flow direction was recorded simultaneously with the hiccup (Figures 3 and 4).
3. Immediately after the reversed diastolic flow, the systolic beat showed a decreased peak flow velocity compared with the previous and the next systolic values (Figure 5,Table 3). Hiccup in Systole 4. At the aortic and pulmonic valves, a decreased peak flow velocity was observed at the hiccup beat (beat 2) compared with beats 1 and 3. The absolute peak flow velocity values were identical to those recorded in the aorta immediately after a reversal flow during a diastolic hiccup (Figure 6,Table 4). 5. Mild to moderate, single-beat, tricuspid regurgitant jet appeared synchronously with each hiccup (Figure 2, C; Table 4). No other valve insufficiency was seen during hiccups.
Journal of the American Society of Echocardiography Volume 13 Number 4
Levi, Benvenisti, David 297
Figure 3 A, Short-axis view at pulmonary artery and ductus. B, Antegrade flow (blue). C, Retrograde flow across ductus (orange-yellow) at hiccup. RV, Right ventricle; RA, right atrium.
Figure 4 Sagittal view of aortic arch and descending aorta. A, Antegrade flow across aortic arch (orangeyellow). B, Retrograde flow across aortic arch (blue) at hiccup.
Table 2 Peak flow velocity (m/s) at diastolic hiccup
Tricuspid valve Mitral valve
Prehiccup beat
Hiccup beat
Posthiccup beat
P value
0.25 ± 0.05 0.20 ± 0.03
0.45 ± 0.10 0.35 ± 0.05
0.25 ± 0.05 0.20 ± 0.03
<.01 <.01
Table 3 Peak flow velocity (m/s) across ductus and descending aorta (DA) at diastolic hiccup
Ductus/DA
Systole–b1
Diastolic hiccup-b2
Systole–b3
P value
0.65 ± 0.10
–0.30 ± –0.10
0.45 ± 0.10
<.0001
Prehiccup beat
Hiccup beat
Posthiccup beat
P value
0.65 ± 0.10 0.00
0.45 ± 0.10 –2.00 ± –0.50
0.65 ± 0.10 0.00
<.01 <.0001
Table 4 Peak flow velocity (m/s) at systolic hiccup
Pulmonic valve/aortic valve Tricuspid valve
DISCUSSION Intrathoracic pressure changes periodically during spontaneous breathing. This phenomenon is accentuated in a number of conditions, such as airway obstructions, snoring, and hiccups.1,2 Inspiratory decrease in systemic arterial blood pressure has been primarily attributed to a decrease in stroke vol-
ume by some investigators,6 whereas others have implicated direct transmission of intrathoracic pressure reduction to the vascular tree as the dominant mechanism.7 Peters et al8 caused a decrease in intrathoracic pressure during diastole in anesthetized dogs by using electrocardiogram-triggered phrenic nerve stimulation. An increase in anteroposterior and lat-
298 Levi, Benvenisti, David
Journal of the American Society of Echocardiography April 2000
Figure 5 Spectral analysis of aortic arch flow at diastolic hiccup. b1, Prehiccup beat; b2, reversal flow at diastolic hiccup beat; b3, decreased peak velocity at next systolic beat.
Figure 6 Spectral analysis of aortic valve flow at systolic hiccup. Note the decreased peak velocity of the hiccup beat (the third beat) in relation to the prehiccup and posthiccup beats.
eral dimensions of the intrathoracic aorta and a reduction of blood pressure were demonstrated simultaneously with the diaphragmatic contraction. Mathew9 showed a transient blood pressure reduction in 10 intubated preterm infants at bouts of “systolic” hiccups. During bouts of fetal hiccups in our study, the effect on blood flow velocity and direction varied with the time of occurrence. When the hiccup appeared in early systole, a significant transient reduction of peak flow velocity occurred at the aortic and pulmonic valve level, compared with the beat before and the beat after the hiccup. For hiccups occurring during diastole, the most relevant finding was a transient reversal of blood flow through the aortic arch, ductus arteriosus, and descending aorta in fetuses with a normal heart and normal, regular rhythm. A similar observation was described by Mueller and Sipes.10 They incidentally found a transient reversed umbilical artery blood flow in normal fetuses during bouts of hiccups. Clinically, it is known that permanent reversed aortic or ductal blood flow is a poor prognostic sign that may appear in certain cases of complex congenital heart diseases. This study demonstrates that transient reversal of fetal aortic and ductal blood flow simultaneously with hiccup may occur in fetuses with absolutely normal cardiac anatomy. A significant acceleration of diastolic blood flow across the tricuspid and mitral valves and during the entire cardiac cycle across the superior vena cava,
inferior vena cava, and ostium secundum was demonstrated during bouts of hiccups. Such findings agree with the well-know augmentation of venous return to right cardiac chambers during deep inspiration. This is a consequence of direct transmission of the negative intrathoracic pressure to the great systemic veins.11 The intermittent and simultaneous tricuspid regurgitation induced by hiccups occurring during systole cannot be explained by the mechanism of augmented right ventricular preload. It is known that the exacerbation of an existent tricuspid regurgitation during inspiration takes a few beats to occur (Rivero Carvallo’s sign).12 A significant collapse of the right ventricular anterior wall, clearly distinguishable from the regular systolic contraction, was recorded together with a rhythmic anterior chest wall invagination induced by hiccup.We wonder if a transient distortion of the tricuspid valve apparatus occurs at that moment and a valvular insufficiency is caused. No regurgitation from other valves was found during bouts of hiccups. Conclusion Significant transient changes in intracardiac and great vessels blood flow velocity and direction were observed in fetuses with normal cardiac anatomy and regular cardiac rhythm during bouts of hiccups. A direct transmission of briefly augmented, negative intrathoracic pressure to a compliant aorta and systemic veins appears to be a reasonable explanation for most of our observations. REFERENCES 1. Allan LD, Chita SK, Al-Ghazali W, Crawford DC, Tynan M. Doppler echocardiographic evaluation of the normal human fetal heart. Br Heart J 1987;57:528-33. 2. Kleinman CS, Huhta JC, Silverman NH. Doppler echocardiography in the human fetus. J Am Soc Echocardiogr 1988; 1:287-90. 3. Sharland GK, Chita SK, Allan LD. The use of color Doppler in fetal echocardiography. Int J Cardiol 1990;28:229-36. 4. Buda A, Pinsky M, Ingels N, Daughters G, Stinson E,
Journal of the American Society of Echocardiography Volume 13 Number 4
5.
6.
7.
8.
Alderman E. Effect of intrathoracic pressure on left ventricular performance. N Engl J Med 1979;301:453-9. Scharf S, Brown M, Saunders N, Green L. Effects of normal and loaded spontaneous inspiration on cardiac function. J Appl Physiol 1979;47:582-90. Karam M, Wise R, Natarajan T, Permutt S, Wagner H. Mechanism of decreased left ventricular stroke volume during inspiration in man. Circulation 1984;69:866-73. Olsen C, Tyson G, Maier G, Davis J, Rankin J. Diminished stroke volume during inspiration: a reverse thoracic pump. Circulation 1985;72:668-79. Peters J, Kindred M, Robothan J. Transient analysis of car-
Levi, Benvenisti, David 299
9.
10.
11. 12.
diopulmonary interactions: I. Diastolic events. J Appl Physiol 1988;64:1506-17. Mathew O. Effects of transient intrathoracic pressure changes (hiccups) on systemic arterial pressure. J Appl Physiol 1997; 83:371-5. Mueller G, Sipes S. Isolated reverse umbilical arterial blood flow on Doppler ultrasonography in fetal hiccups. J Ultrasound Med 1993;12:641-3. Guyton A, Adkins J. Quantitative aspects of the collapse factor in relation to venous return. Am J Physiol 1954;177:523-7. Podio R. Aparato Cardiovascular Textbook. Vol 2. Buenos Aires: Intermedica; 1969. [Spanish] p. 182-6.
During routine fetal echocardiographic studies, we incidentally observed abrupt beat-to-beat changes in blood flow velocity and direction during bouts of hiccups in fetuses with a normal heart and regular and synchronized atrioventricular cardiac rhythm. The effect of hiccups on blood flow velocity and direction varied depending on the time of occurrence of hiccups during the cardiac cycle. In systole, a significant transient reduction of peak flow velocity occurred at the aortic and pulmonic valves, and brief tricuspid regurgitation appeared synchronously with each hiccup. In diastole, a transient reversal of flow
direction was recorded simultaneously with the hiccup at the aorta and ductus arteriosus, and acceleration of peak flow velocity was observed across the tricuspid and mitral valves. Throughout the entire cardiac cycle, marked blood flow acceleration was observed in the superior vena cava, inferior vena cava, and ostium secundum simultaneously with the hiccup. A direct transmission of briefly augmented, negative intrathoracic pressure to a compliant aorta and systemic veins appears to be a reasonable explanation for most of our observations. (J Am Soc Echocardiogr 2000;13:295-9.)
INTRODUCTION
pressure reduction on fetal intracardiac and great vessels blood flow velocity and direction.
Fetal intracardiac and intravascular blood flow dynamics have been the focus of some investigations. In the normal fetal heart, laminar antegrade blood flow profiles are recorded across the cardiac valves and the great vessels by color Doppler echocardiography.1-3 During routine fetal echocardiographic studies, we incidentally observed abrupt, and sometimes paradoxical, beat-to-beat changes in blood flow velocity and direction during bouts of fetal hiccups. Hiccups are an involuntary spasmodic and coordinated contraction of the inspiratory muscles. This forceful and involuntary inspiration causes transient intrathoracic pressure reduction.4,5 Ultrasonographic imaging of fetuses has documented the occurrence of hiccups from early gestation through parturition. The purpose of this study was to analyze the effects of hiccup-induced transient intrathoracic
From the Pediatric Cardiology Unit and the Department of Cardiology, Meir Hospital, Sapir Medical Center, Kfar Sava; and the Sackler School of Medicine, University of Tel Aviv; Israel. Reprint requests: Alex Levi, Department of Cardiology, Meir Hospital–Sapir Medical Center, Tschernichovsky St, Kfar Sava, 44281, Israel (E-mail: [email protected]). Copyright © 2000 by the American Society of Echocardiography. 0894-7317/2000 $12.00 + 0 27/1/103867 doi:10.1067/mje.2000.103867
METHODS Seventeen fetuses with normal cardiac anatomy and bouts of hiccups were identified during routine fetal echocardiographic studies of high-risk pregnancies.The gestational age varied between 20 and 30 weeks. All examinations were performed with an HP 2500 (Hewlett-Packard, Andover, Mass) echocardiographic system with a 5-MHz transducer. Blood flow velocity and direction across cardiac valves, ostium secundum, aortic arch, ductus arteriosus, descending aorta, and systemic veins were analyzed with the use of color Doppler and pulsed Doppler spectral analysis in 3 consecutive heart beats: the prehiccup beat, the hiccup beat, and the posthiccup beat.The interbeat flow velocity changes were compared by using analysis of variance and t test and were considered significant at P values <.05.
RESULTS All the fetuses presented regular and synchronized atrioventricular cardiac rhythms without premature contractions during the bouts of hiccups. The heart rates ranged between 110 and 143 bpm.The effects of a hiccup on intracardiac and great vessels blood 295
Journal of the American Society of Echocardiography April 2000
296 Levi, Benvenisti, David
Figure 1 Sagittal view of inferior vena cava (IVC) and superior vena cava (SVC) entering right atrium. A, Laminar flow in IVC (dark blue). B, Accelerated flow across IVC (light blue) and SVC (red) at hiccup. C, Spectral analysis. Accelerated flow across IVC at hiccup beat (asterisks).
Figure 2 Four-chamber view. A, No hiccup. B, Accelerated flow across ostium secundum (blue) at hiccup. C, Tricuspid regurgitation at hiccup. Note the anterior chest wall invagination at hiccup in B and C.
Table 1 Peak flow velocity (m/s) at hiccup
Inferior vena cava Superior vena cava Ostium secundum
Prehiccup beat
Hiccup beat
Posthiccup beat
P value
–0.35 ± –0.05 0.30 ± 0.05 0.20 ± 0.05
–1.80 ± –0.20 1.65 ± 0.20 0.50 ± 0.10
–0.35 ± –0.05 0.30 ± 0.05 0.20 ± 0.10
<.0001 <.0001 <.001
flow velocity and direction varied depending on when it occurred during the cardiac cycle. In general, throughout the entire cardiac cycle, marked blood flow acceleration was observed in the superior vena cava, inferior vena cava, and ostium secundum simultaneously with the hiccup beat (Figures 1 and 2,Table 1). Hiccup in Diastole 1. A significant and brief acceleration of peak blood flow velocity was observed across the tricuspid valve and, to a lesser degree, across the mitral valve during beat 2 compared with beats 1 and 3 (Table 2). 2. At the aortic arch, descending aorta, and ductus arteriosus, a transient reversal of flow direction was recorded simultaneously with the hiccup (Figures 3 and 4).
3. Immediately after the reversed diastolic flow, the systolic beat showed a decreased peak flow velocity compared with the previous and the next systolic values (Figure 5,Table 3). Hiccup in Systole 4. At the aortic and pulmonic valves, a decreased peak flow velocity was observed at the hiccup beat (beat 2) compared with beats 1 and 3. The absolute peak flow velocity values were identical to those recorded in the aorta immediately after a reversal flow during a diastolic hiccup (Figure 6,Table 4). 5. Mild to moderate, single-beat, tricuspid regurgitant jet appeared synchronously with each hiccup (Figure 2, C; Table 4). No other valve insufficiency was seen during hiccups.
Journal of the American Society of Echocardiography Volume 13 Number 4
Levi, Benvenisti, David 297
Figure 3 A, Short-axis view at pulmonary artery and ductus. B, Antegrade flow (blue). C, Retrograde flow across ductus (orange-yellow) at hiccup. RV, Right ventricle; RA, right atrium.
Figure 4 Sagittal view of aortic arch and descending aorta. A, Antegrade flow across aortic arch (orangeyellow). B, Retrograde flow across aortic arch (blue) at hiccup.
Table 2 Peak flow velocity (m/s) at diastolic hiccup
Tricuspid valve Mitral valve
Prehiccup beat
Hiccup beat
Posthiccup beat
P value
0.25 ± 0.05 0.20 ± 0.03
0.45 ± 0.10 0.35 ± 0.05
0.25 ± 0.05 0.20 ± 0.03
<.01 <.01
Table 3 Peak flow velocity (m/s) across ductus and descending aorta (DA) at diastolic hiccup
Ductus/DA
Systole–b1
Diastolic hiccup-b2
Systole–b3
P value
0.65 ± 0.10
–0.30 ± –0.10
0.45 ± 0.10
<.0001
Prehiccup beat
Hiccup beat
Posthiccup beat
P value
0.65 ± 0.10 0.00
0.45 ± 0.10 –2.00 ± –0.50
0.65 ± 0.10 0.00
<.01 <.0001
Table 4 Peak flow velocity (m/s) at systolic hiccup
Pulmonic valve/aortic valve Tricuspid valve
DISCUSSION Intrathoracic pressure changes periodically during spontaneous breathing. This phenomenon is accentuated in a number of conditions, such as airway obstructions, snoring, and hiccups.1,2 Inspiratory decrease in systemic arterial blood pressure has been primarily attributed to a decrease in stroke vol-
ume by some investigators,6 whereas others have implicated direct transmission of intrathoracic pressure reduction to the vascular tree as the dominant mechanism.7 Peters et al8 caused a decrease in intrathoracic pressure during diastole in anesthetized dogs by using electrocardiogram-triggered phrenic nerve stimulation. An increase in anteroposterior and lat-
298 Levi, Benvenisti, David
Journal of the American Society of Echocardiography April 2000
Figure 5 Spectral analysis of aortic arch flow at diastolic hiccup. b1, Prehiccup beat; b2, reversal flow at diastolic hiccup beat; b3, decreased peak velocity at next systolic beat.
Figure 6 Spectral analysis of aortic valve flow at systolic hiccup. Note the decreased peak velocity of the hiccup beat (the third beat) in relation to the prehiccup and posthiccup beats.
eral dimensions of the intrathoracic aorta and a reduction of blood pressure were demonstrated simultaneously with the diaphragmatic contraction. Mathew9 showed a transient blood pressure reduction in 10 intubated preterm infants at bouts of “systolic” hiccups. During bouts of fetal hiccups in our study, the effect on blood flow velocity and direction varied with the time of occurrence. When the hiccup appeared in early systole, a significant transient reduction of peak flow velocity occurred at the aortic and pulmonic valve level, compared with the beat before and the beat after the hiccup. For hiccups occurring during diastole, the most relevant finding was a transient reversal of blood flow through the aortic arch, ductus arteriosus, and descending aorta in fetuses with a normal heart and normal, regular rhythm. A similar observation was described by Mueller and Sipes.10 They incidentally found a transient reversed umbilical artery blood flow in normal fetuses during bouts of hiccups. Clinically, it is known that permanent reversed aortic or ductal blood flow is a poor prognostic sign that may appear in certain cases of complex congenital heart diseases. This study demonstrates that transient reversal of fetal aortic and ductal blood flow simultaneously with hiccup may occur in fetuses with absolutely normal cardiac anatomy. A significant acceleration of diastolic blood flow across the tricuspid and mitral valves and during the entire cardiac cycle across the superior vena cava,
inferior vena cava, and ostium secundum was demonstrated during bouts of hiccups. Such findings agree with the well-know augmentation of venous return to right cardiac chambers during deep inspiration. This is a consequence of direct transmission of the negative intrathoracic pressure to the great systemic veins.11 The intermittent and simultaneous tricuspid regurgitation induced by hiccups occurring during systole cannot be explained by the mechanism of augmented right ventricular preload. It is known that the exacerbation of an existent tricuspid regurgitation during inspiration takes a few beats to occur (Rivero Carvallo’s sign).12 A significant collapse of the right ventricular anterior wall, clearly distinguishable from the regular systolic contraction, was recorded together with a rhythmic anterior chest wall invagination induced by hiccup.We wonder if a transient distortion of the tricuspid valve apparatus occurs at that moment and a valvular insufficiency is caused. No regurgitation from other valves was found during bouts of hiccups. Conclusion Significant transient changes in intracardiac and great vessels blood flow velocity and direction were observed in fetuses with normal cardiac anatomy and regular cardiac rhythm during bouts of hiccups. A direct transmission of briefly augmented, negative intrathoracic pressure to a compliant aorta and systemic veins appears to be a reasonable explanation for most of our observations. REFERENCES 1. Allan LD, Chita SK, Al-Ghazali W, Crawford DC, Tynan M. Doppler echocardiographic evaluation of the normal human fetal heart. Br Heart J 1987;57:528-33. 2. Kleinman CS, Huhta JC, Silverman NH. Doppler echocardiography in the human fetus. J Am Soc Echocardiogr 1988; 1:287-90. 3. Sharland GK, Chita SK, Allan LD. The use of color Doppler in fetal echocardiography. Int J Cardiol 1990;28:229-36. 4. Buda A, Pinsky M, Ingels N, Daughters G, Stinson E,
Journal of the American Society of Echocardiography Volume 13 Number 4
5.
6.
7.
8.
Alderman E. Effect of intrathoracic pressure on left ventricular performance. N Engl J Med 1979;301:453-9. Scharf S, Brown M, Saunders N, Green L. Effects of normal and loaded spontaneous inspiration on cardiac function. J Appl Physiol 1979;47:582-90. Karam M, Wise R, Natarajan T, Permutt S, Wagner H. Mechanism of decreased left ventricular stroke volume during inspiration in man. Circulation 1984;69:866-73. Olsen C, Tyson G, Maier G, Davis J, Rankin J. Diminished stroke volume during inspiration: a reverse thoracic pump. Circulation 1985;72:668-79. Peters J, Kindred M, Robothan J. Transient analysis of car-
Levi, Benvenisti, David 299
9.
10.
11. 12.
diopulmonary interactions: I. Diastolic events. J Appl Physiol 1988;64:1506-17. Mathew O. Effects of transient intrathoracic pressure changes (hiccups) on systemic arterial pressure. J Appl Physiol 1997; 83:371-5. Mueller G, Sipes S. Isolated reverse umbilical arterial blood flow on Doppler ultrasonography in fetal hiccups. J Ultrasound Med 1993;12:641-3. Guyton A, Adkins J. Quantitative aspects of the collapse factor in relation to venous return. Am J Physiol 1954;177:523-7. Podio R. Aparato Cardiovascular Textbook. Vol 2. Buenos Aires: Intermedica; 1969. [Spanish] p. 182-6.