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Ann Thorac Surg 2000;69:151-155
© 2000 The Society of Thoracic Surgeons

Original Articles

Myocardial tactile stiffness during acute reduction of coronary blood flow

Kagami Miyaji, MDa, Seiryo Sugiura, MDb, Hirotaka Inaba, MDa, Shinichi Takamoto, MDa, Sadao Omata, PhDa

a Department of Cardiothoracic Surgery, University of Tokyo, Tokyo, Japan
b Second Department of Internal Medicine, University of Tokyo, Tokyo, Japan

Address reprint requests to Dr Miyaji, Department of Cardiothoracic Surgery, University of Tokyo Hospital, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113, Japan


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Evaluation of regional myocardial contractile function is of clinical importance. We have developed a new tactile sensor system for accurate measurement of myocardial stiffness in situ. We found that the myocardial stiffness measured by this sensor, which we call tactile stiffness, can be a very useful index for accurate quantification of regional myocardial function. In this study, we used a coronary stenosis model to investigate regional myocardial tactile stiffness under conditions of reduced coronary blood flow.

Methods. The myocardial tactile stiffness, coronary blood flow, and ventricular pressure and volume, of five open chest mongrel dogs weighing 15 to 17 kg, were measured. After measuring the baseline myocardial stiffness, coronary arterial stenosis was induced with a balloon occluder.

Results. Reducing the coronary flow to 50% and 25% of the baseline level reduced the end-systolic tactile stiffness significantly from 2.20 ± 0.16 g/mm2 to 2.05 ± 0.20 g/mm2 (p < 0.05) and from 2.21 ± 0.16 g/mm2 to 1.96 ± 0.18 g/mm2 (p < 0.01), respectively. Reducing the flow, to 50% and 25%, increased the end-diastolic stiffness significantly from 1.29 ± 0.15 g/mm2 to 1.39 ± 0.14 g/mm2 (p < 0.01) and from 1.30 ± 0.16 g/mm2 to 1.46 ± 0.14 g/mm2 (p < 0.05), respectively.

Conclusions. We consider that the regional myocardial tactile stiffness will be a useful index sensitive enough to detect changes in regional contractile function under conditions of reduced coronary blood flow.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Evaluation of regional contractile function is of clinical importance, because various diseased states affect the myocardium heterogeneously. Therefore, many investigators have attempted to quantify regional myocardial contractile function using the wall strain-stress relationship [1–6]. We have developed a new tactile sensor system for accurate measurement of myocardial stiffness in situ. We found that the myocardial stiffness measured by this sensor, which we call tactile stiffness, can be a very useful index for accurate quantification of regional myocardial function [7]. Since Tennant and Wiggers reported in 1935 that regional myocardial contraction was reduced by coronary artery ligation [8], it has been established that regional myocardial contractile function is closely related to coronary perfusion. In our previous study, we used a model of acute myocardial ischemia induced by occlusion of the left anterior descending artery, and showed that the end-systolic stiffness decreased significantly, whereas the global ventricular function did not change appreciably, indicating that this tactile sensor is a sensitive detector of changes in regional myocardial function [7]. In this study, we used a coronary stenosis model to study the regional myocardial tactile stiffness under conditions of reduced coronary blood flow.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Tactile sensor system
The principle of our tactile sensor has been described previously [7, 9]. Our tactile sensor system is composed of a sensor probe, an amplifier, and a filter. The sensor probe (Axiom Co Ltd, Koriyama, Japan) is 5.5-cm long, 7-mm in diameter, weighs 2.08 g, equipped with a small tip, 3-mm in diameter, that is connected accoustically to a piezoelectric transducer made of lead zirconate-barium titanate ceramic with a resonance frequency of 68 kHz. When the sensor probe touches an object and the resonance frequency shifts, the vibration detector picks up the change in frequency and sends a signal to the amplifier, which keeps the piezoelectric transducer vibrating at the new frequency. Measurement was made 150 times per second with a frequency counter device (AX-CNT1001, Axiom Co Ltd, Koriyama, Japan) and the delta f value was processed sequentially by a personal computer (PC9821-Ne, NEC Inc, Tokyo, Japan).

Calibration of stiffness
The relationship between stiffness and delta f for our tactile sensor was derived using the counter-balance method [7] employing bovine gelatins of 7 different concentrations, the stiffness of which was predetermined by a viscoelastance measurement device (AX-SFD001, Axiom Co Ltd). Based on these measurements, we obtained the following calibration formula, which was used in this study: Stiffness (g/mm2) = Exp{[delta f(Hz) + 517.876]/302.069}.

For example, stiffness of 1.0 and 2.0 (g/mm2) correspond to the delta f value (frequency change) of -517.9 and -308.5 (Hz), respectively.

Study protocol
All the animals received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23, revised 1985). Five mongrel dogs weighing 15 to 17 kg were anesthetized with ketamine (15 mg/kg im) and sodium pentobarbital (35 mg/kg iv). The animals were then mechanically ventilated through an endotracheal tube. After left thoracotomy, pericardiotomy was performed. A 7F volume conductance catheter (single field, eight electrodes; Leycom, Oegstgeest, The Netherlands) and a 4F micromanometer-tipped catheter (MPC-500; Millar Instruments, Houston, TX) were inserted into the left ventricle from its apex to record the left ventricular volume and pressure, respectively. The left anterior descending artery of each animal was dissected and a balloon occluder (Fuji Systems Co, Ltd, Tokyo, Japan) was placed at this artery, just proximal to the first diagonal branch. A transit ultrasonic flowmeter equipped with a 2.5-mm diameter probe (Transonic Inc, New York, NY) was inserted in the left anterior descending artery between the first and the second diagonal branch to monitor the coronary blood flow. The distal end of the left anterior descending artery and the second diagonal branch were ligated to prevent coronary perfusion because of collateral flow from the circumflex artery. The tactile sensor for measuring myocardial stiffness was placed in the region between the left anterior descending artery and the second diagonal branch. All data were collected simultaneously by an analogue to digital converter (AX-ADC1001, Axiom Co, Ltd) and a personal computer (Fig 1).



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  		Fig 1. Tactile sensor system: the sensor is 5.5-cm long, 7-mm in diameter, weighs 2.08 g, and is equipped with a small tip, 3-mm in diameter, that is connected to a piezoelectric transducer made of lead zirconate-barium titanate ceramics. (A/D converter = analogue to digital converter; LV = left ventricle; LAA = left atrial appendage; PA = pulmonary artery; RV = right ventricle; LAD = left anterior descending branch; D1 = first diagonal branch; D2 = second diagonal branch; * = ligation of coronary artery.)

 
Tactile myocardial stiffness under conditions of reduced coronary blood flow
The baseline myocardial stiffness of each dog was recorded and then coronary arterial stenosis was induced by inflating the balloon occluder at the left anterior descending artery, just proximal to the first diagonal branch. The coronary flow was maintained at about 50% and 25% of the baseline flow by monitoring the data from the transit ultrasonic flow meter and altering the balloon pressure as necessary, and the changes in myocardial stiffness under these conditions were monitored for 30 to 40 seconds. The occlusion to produce flow 25% of the baseline was performed first and the occlusion to produce 50% was performed second. There was a normal flow period at least 5 minutes between the occlusions to produce flow 25% and 50% of the baseline. The values were compared with the baseline tactile myocardial stiffness values at end-systole and end-diastole. Both end-systolic and end-diastolic points were determined using the global pressure-volume loop.

Statistical analysis
All the values are expressed as means ± standard deviation. The two-tailed Student’s t-test was used to compare the values for normal baseline and ischemic myocardium, and differences at p less than 0.05 were regarded as significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Coronary flow
Before reducing the flow to 50% of the baseline level, the mean baseline coronary flow of the left anterior descending artery, just distal to the first diagonal branch, was 19.5 ± 3.7 mL/min. It was reduced to 9.5 ± 1.8 mL/min, 49.0% ± 5.7% of the baseline flow, using the balloon occluder (Table 1). Before reducing the flow to 25% of the baseline level, the mean baseline coronary flow was 20.0 ± 3.2 mL/min, and it was reduced to 5.2 ± 0.9 mL/min, 25.8% ± 2.2% of the baseline flow, using the balloon occluder (Table 2).


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  		Table 1. End-Systolic Myocardial Tactile Stiffness Under Reduced Coronary Blood Flow

 

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  		Table 2. End-Systolic Myocardial Tactile Stiffness Under Reduced Coronary Blood Flow

 
Left ventricular pressure and volume
The baseline end-systolic left ventricular pressure was 151.9 ± 16.7 mm Hg and it was 151.4 ± 17.9 mm Hg when the coronary blood flow was reduced to 50% of the baseline level. These values were not significantly different (p = 0.65). The baseline end-systolic left ventricular pressure was 154.1 ± 11.9 mm Hg and it was 154.6 ± 11.5 mm Hg when the coronary blood flow was reduced to 25% of the baseline level. These values did not differ significantly (p = 0.39). The baseline end-diastolic left ventricular pressure of the 50% baseline flow model was 10.2 ± 1.7 mm Hg and it was 10.8 ± 1.4 mm Hg when the coronary blood flow was reduced to 50% of the baseline level. The values before and after coronary flow reduction were not significant (p = 0.38). The baseline end-diastolic left ventricular pressure of the 25% baseline flow model was 9.7 ± 1.4 mm Hg and it was 10.2 ± 1.4 mm Hg when the coronary blood flow was reduced to 25% of the baseline level. These values did not differ significantly (p = 0.39).

Under condition of reduced coronary flow, the pressure-volume (P-V) loop shifted slightly to the right, but neither the left ventricular pressure, nor the pressure-volume area (PVA), which represents the total mechanical energy generated by a left ventricular contraction, changed (Fig 2). These data indicate that the global ventricular function status remained fairly constant.



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  		Fig 2. The pressure-volume loop (P-V loop) shifted to the right after coronary flow reduction, but neither the left ventricular pressure nor the pressure-volume area (PVA) changed.

 
Tactile myocardial stiffness under conditions of reduced coronary flow
The phasic changes in the mean coronary blood flow and myocardial stiffness of the ischemic region are shown in Figure 3. The upper and lower panels represent myocardial tactile stiffness, and the mean coronary blood flow of the left anterior descending artery just distal to the first diagonal branch respectively. It is clear that the end-systolic stiffness of the myocardium decreased as the coronary flow decreased.



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  		Fig 3. Phasic changes in myocardial stiffness in response to reducing the coronary blood flow by 50%. (Left) Baseline myocardial tactile stiffness and coronary blood flow of the left anterior descending artery just distal to the first diagonal branch. (Right) Myocardial tactile stiffness under the reduced coronary blood flow. End-systolic tactile stiffness decreased as the coronary flow decreased. (Solid line = myocardial tactile stiffness; dotted line = coronary blood flow of the left anterior descending artery just distal to the first diagonal branch.)

 
Reducing the flow to 50% of the baseline level reduced the end-systolic tactile stiffness significantly from 2.20 ± 0.16 g/mm2 to 2.05 ± 0.20 g/mm2 (n = 5, p = 0.045 < 0.05, Table 1) and reducing it to 25% reduced the end-systolic tactile stiffness significantly from 2.21 ± 0.16 g/mm2 to 1.96 ± 0.18 g/mm2 (n = 5, p = 0.003 < 0.01, Table 2).

Reducing the flow to 50% of the baseline level increased the end-diastolic tactile stiffness significantly from 1.29 ± 0.15 g/mm2 to 1.39 ± 0.14 g/mm2 (n = 5, p = 0.007 < 0.01, Table 3) and reducing it to 25% increased the end-diastolic tactile stiffness significantly from 1.30 ± 0.16 g/mm2 to 1.46 ± 0.14 g/mm2 (n = 5, p = 0.012 < 0.05, Table 4).


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  		Table 3. End-Diastolic Myocardial Tactile Stiffness Under Reduced Coronary Blood Flow

 

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  		Table 4. End-Diastolic Myocardial Tactile Stiffness Under Reduced Coronary Blood Flow

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Since the classic study of Tennant and Wiggers [8] the relationship between coronary blood flow and myocardial contraction has been elucidated. During partial coronary occlusion, regional myocardial contraction deteriorates as the blood flow is reduced. As it is of clinical and basic importance, many attempts have been made to estimate accurately regional myocardial contraction under conditions of reduced coronary blood flow. The indices derived so far include regional myocardial shortening [10–13], regional myocardial work [10, 14, 15], and the length-thickness at end-systole [13, 16]. In 1987, Halperin and associates [17] defined transverse stiffness as the ratio of indentation stress to strain when the ventricular wall was indented in a direction perpendicular to the wall. They used arterially perfused canine ventricular septa mounted in an apparatus that could exert biaxial load in the plane of the wall and showed that the transverse stiffness was proportional to the stresses in the plane of the wall. When similar wall stresses were applied, the transverse stiffness of the contracting ventricular septum was greater than that of the relaxed one. On the basis of these findings, they concluded that measurement of transverse stiffness might allow accurate quantification of the regional contractile state. However, this experimental setting was far from in situ application.

Since Omata and associates developed their original tactile sensor in 1989, its applications in various fields, including medical science, have been studied [18–22]. In our previous study, we reported that the myocardial stiffness measured by a tactile sensor, which we called the tactile stiffness, followed a similar time course to the left ventricular pressure and was a good index of regional wall stress. We also calculated the fiber stress based on the model of Arts and colleagues [23] and compared it with the tactile stiffness. The tactile stiffness followed a similar time course to that of the fiber stress. The relationship between end-systolic tactile stiffness and end-systolic fiber stress revealed a strong correlation over a wide range of contractility. These results support the idea that tactile stiffness reflects left ventricular muscle fiber stress or regional wall stress [7]. In a study using an acute myocardial ischemia model induced by occlusion of coronary artery, the end-systolic myocardial stiffness was found to decrease significantly and the end-diastolic myocardial stiffness was found to increase significantly, whereas the global ventricular function did not change appreciably, indicating that such a tactile sensor is a sensitive detector of the changes in regional myocardial function [7]. However, these previous studies did not clearly show whether the regional myocardial tactile stiffness could be a sensitive index under conditions of reduced coronary blood flow. Therefore, we used a coronary stenosis model to study the changes in regional myocardial tactile stiffness under such conditions. Reducing the coronary flow to 25% of the baseline level reduced the end-systolic regional tactile stiffness significantly, as did reducing the flow to 50%, without any appreciable changes in the global ventricular function. Reducing the coronary flow to 25% of the baseline level increased the end-diastolic tactile stiffness significantly, as did reducing the flow to 50%, without any appreciable changes in the end-diastolic ventricular pressure and the global ventricular function. These results indicate that the regional tactile stiffness is an index sensitive enough to detect changes in regional contractile and diastolic function under conditions of reduced coronary blood flow.

In conclusion, we have shown that myocardial tactile stiffness may be a very useful index for accurate quantification of regional myocardial function under conditions of reduced coronary blood flow. Further improvements of the tactile sensor probe and additional experimental studies should enable us to expand its clinical applications from cardiac operation to cardiac catheterization to evaluate the regional changes in myocardial contractility that we often encounter in patients with ischemic heart disease.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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  8. Tennant R., Wiggers C.J. The effect of coronary occlusion on myocardial contraction. Am J Physiol 1935;112:351-361.[Free Full Text]
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  10. Theroux P., Franklin D., Ross J., Jr, Kemper W.S. Regional myocardial function during acute coronary artery occlusion and its modification by pharmacologic agents in the dog. Cir Res 1974;35:896-908.[Abstract/Free Full Text]
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  18. Ohtsuka T., Furuse A., Kohno T., Nakajima J., Yagyu K., Omata S. Application of a new tactile sensor to thoracic surgery. Ann Thorac Surg 1995;60:610-614.[Abstract/Free Full Text]
  19. Omata S., Constantinou C.E. Modeling of micturition characteristics based on prostatic stiffness modulation induced using hormones and adrenergic antagonists. IEEE Trans Biomed Eng 1995;42:843-848.[Medline]
  20. Constantinou C.E., Omata S. Analysis of the relative biomechanical effects of {alpha}1 and {alpha}2 antagonists in modifying the compliance of the prostate and micturition parameters of the hormonally manipulated male rat. Neurourol Urodyn 1996;15:85-101.[Medline]
  21. Kaga N., Katsuki Y., Kakinuma C., Ohata M., Shibutani Y., Omata S. Usefulness of a new tactile sensor for measurement of uterine cervical ripening in mice in a quantitative and noninvasive manner. Am J Obstet Genecol 1996;175:713-718.[Medline]
  22. Miyaji K., Furuse A., Nakajima J., et al. The stiffness of lymph nodes containing metastatic lung cancer. Cancer 1997;80:1920-1925.[Medline]
  23. Arts T., Bovendeers P.H., Prinzen F.W., Renenman R.S. Relation between left ventricular cavity pressure and volume and systolic fiber stress and strain in the wall. Biophys J 1991;59:93-102.[Medline]
Accepted for publication June 28, 1999.





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