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Effects of Cellular Cardiomyoplasty on Ventricular Remodeling Assessed by Doppler Echocardiography and Topographic Immunohistochemistry

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Effects of Cellular Cardiomyoplasty on Ventricular Remodeling Assessed by Doppler Echocardiography and Topographic Immunohistochemistry EXPERIMENTAL INVESTIGATION Circ J 2004; 68: 580–586 Effects of Cellular Cardiomyoplasty on Ventricular Remodeling Assessed by Doppler Echocardiography and Topographic Immunohistochemistry Minoru Yoshiyama, MD; Tetsuya Hayashi, MD**; Yasuhiro Nakamura, MD; Takashi Omura, MD; Yasukatsu Izumi, MD*; Ryo Matsumoto, MD; Kazuhide Takeuchi, MD; Yasushi Kitaura, MD**; Junichi Yoshikawa, MD Background Myocardial infarction (MI) promotes deleterious remodeling of the myocardium, resulting in ventricular dilation and pump dysfunction. Supplementing infarcted myocardium with neonatal myocyte would attenuate deleterious remodeling and so the present study used Doppler echocardiography and histology to analyze the cardiac function and histological regeneration of the damaged myocardium after cellular cardiomyo- plasty. Methods and Results Experimental MI was induced by 24-h coronary ligation followed by reperfusion in adult male Lewis rats and neonatal myocytes were injected directly into the infarct and peri-infarct regions. Three groups of animals were studied at 4 weeks after cellular cardiomyoplasty: noninfarcted control (control), MI plus sham injection (MI), and MI plus cell injection (MI+cell). Ventricular remodeling and cardiac perfor- mance were assessed by Doppler echocardiography or contrast echocardiography. At 4 weeks after cellular car- diomyoplasty, MI+cell hearts exhibited attenuation of global ventricular dilation and cardiac function compared with MI hearts not receiving cellular cardiomyoplasty. Immunohistochemically, connexin-43-positive small cells were observed in the vicinity of the infarction in MI+cell heart. By electron microscopy, these cells con- tained myofilaments with Z-bands and poorly developed intercalated disks, suggesting neonatal myocardial cells. Furthermore, the myocardial cells were often making close contact with interstitial cells. Conclusions Implanted neonatal myocytes form viable grafts after MI, resulting in attenuated ventricular dila- tion and enhanced contractile function. Echocardiography, electron microscopy, and immunohistochemistry are useful methods for assessing the functional and histological regeneration of the damaged myocardium. (Circ J 2004; 68: 580–586) Key Words: Cell therapy; Echocardiography; Myocardial infarction; Remodeling espite advances in the treatment of myocardial The recent development of cellular cardiomyoplasty infarction (MI), congestive heart failure secondary offers a new approach to restore impaired heart function8 D to infarction continues to be a major complication. and evaluation of the survival of the transplanted cells and MI promotes acute and chronic transformation of both the estimation of their ultimate effect on left ventricular func- necrotic infarct zone and the nonnecrotic, peri-infarct tion are very important issues. Doppler echocardiography tissue, leading to global alterations that have collectively is a useful tool for measuring cardiac systolic and diastolic been termed ‘ventricular remodeling’.1,2 The cardiomyo- function. In this study, we used invasive hemodynamic cytes lost during an MI cannot be regenerated, and the studies and non-invasive Doppler echocardiography to extent of the loss is inversely related to cardiac output, evaluate the cardiac function of rats with myocardial pressure-generating capacity, and, ultimately, survival.3,4 infarcts after the injection of neonatal cardiomyocytes or Cellular cardiomyoplasty, or the supplementation of tissue culture media alone. In addition, cell survival and cell –cell with exogenous cells, has previously been used in the treat- attachment were analyzed by electron microscopy, and ment of disease in which terminally differentiated cells are immunohistochemistry. irreparably damaged5 and supplementing infarcted myocar- dium with fetal or neonatal myocytes would result in the formation of viable muscle grafts capable of attenuating Methods deleterious post-MI remodeling.6,7 Myocardial Infarction Model Lewis strain male rats (300g, 8 weeks old; Seac (Received December 8, 2003; revised manuscript received March 3, Yoshitomi Ltd, Fukuoka, Japan) were cared for humanely, 2004; accepted March 12, 2004) in compliance with the ‘Principles of Laboratory Animal Departments of Internal Medicine and Cardiology, and *Pharmacol- Care’ formulated by the National Society for Medical Re- ogy, Graduate School of Medicine, Osaka City University, Osaka and search and the ‘Guide for the Care and Use of Laboratory **Third Department of Medicine, Osaka Medical College, Takatsuki, Japan Animals’ prepared by the Institute of Laboratory Animal Mailing address: Minoru Yoshiyama, MD, Department of Internal Resource and published by the National Institutes of Health Medicine and Cardiology, Graduate School of Medicine, Osaka City (NIH Publication No. 86-23, revised 1985). Acute MI was University, 1-4-3 Asahi-machi, Abeno-ku, Osaka 545-8585, Japan induced as described elsewhere.9 Circulation Journal Vol.68, June 2004 Effects of Cellular Cardiomyoplasty on Ventricular Remodeling 581 Fig1. A, M-mode echocardiograms from control rats, and untreated, cellular cardiomyoplasty therapy treated rats with MI at 4 weeks. Note left ventricular cavity dilatation, thin- ning and akinesis of the anterior wall in the rats with MI. Cellular cardiomyoplasty prevented left ventricular dilata- tion and improved anterior wall motion. AW indicates ante- rior wall; and PW, posterior wall. B, Pulsed-wave Doppler spectra of mitral inflow from control rats, and untreated, cellular cardiomyoplasty treated rats with MI at 4 weeks. The mitral inflow pattern of rats with MI shows increased peak E-wave velocity, rapid deceleration of the E wave, and decreased peak A-wave velocity compared with controls. Cellular cardiomyoplasty visually changed a relatively normal transmitral flow pattern in rats with MI. Fig2. Two-dimensional echocardiograms (apical view) from rats 4 weeks after MI. Four-chamber view is shown at diastole and systole. Cell Isolation and Purification py (MI + cell). Cells or medium were injected into the Rat neonatal ventricular myocytes were isolated as infarct area with a 26-gauge needle bent at an angle of 45°, previously reported. In brief, apical halves of the cardiac 3 mm from the tip. This configuration was designed to ventricles from 1- to 2-day-old Lewis rats were separated, facilitate injection into the infarct. Rats that survived to minced, and dispersed with 80 U/ml collagenase IV and 24h after coronary artery occlusion were randomized to 0.6mg/ml pancreatin. A discontinuous gradient of Percoll receive either injection of cells (3–5×106/50μl) or medium was used to segregate myocytes from nonmyocytes. After (50μl). Cardiac echocardiography was performed at 24h centrifugation for 30min at room temperature, the upper after MI and 4 weeks after cellular cardiomyoplasty. layer consisted of a mixed population of nonmyocyte cell types, and the lower layer consisted almost exclusively of Hemodynamic and Doppler Echocardiographic Studies cardiac myocytes. After the myocytes were incubated on Rats were lightly anesthetized with ketamine HCl uncoated 10cm culture dishes for 30min to remove any (25mg/kg, ip) and xylazine (10mg/kg, ip). Echocardiogra- remaining nonmyocytes, the nonattached viable cells were phy was performed using a commercially available echocar- used for cell transplantation. diographic system equipped with a 12-MHz phased-array transducer (SONOS 5500, Phillips, Andover, MA, USA). Animal Groups and Cardiomyocyte Transplantation A 2-dimensional short-axis view of the LV was obtained at (Cellular Cardiomyoplasty) the level of the papillary muscles. Ejection fraction was Three groups of animals were studied: control animals measured by modifying Simpson’s method, which uses 4- receiving neither infarction nor implantation and only chamber views (Fig1).10 If the left ventricular chamber injected with culture medium (control), infarcted animals could not be gained clearly, we used contrast echocardio- not receiving neonatal cardiomyocyte therapy (MI), and graphy. The contrast agent, optison, was injected into the infarcted animals receiving neonatal cardiomyocyte thera- left ventricular cavity via the femoral vein (Fig2). Pulsed- Circulation Journal Vol.68, June 2004 582 YOSHIYAMA M et al. Fig3. Contrast echocardiograms (apical view) from rats 4 weeks after MI. Untreated and cellular cardiomyoplasty treated rats with MI at 4 weeks were shown. Cellular cardiomyoplasty prevented left ventricular dilatation. Table 1 Doppler Echocardiographic Measurements lead citrate, and were examined with a Hitachi H-7000 electron microscope.13 Control MI MI + cell n 101112 Immunohistochemistry LVDd (mm) 6.5±0.2 8.8±0.3** 8.2±0.3** Additional sections were obtained from the paraffin LVDs (mm) 4.2±0.1 6.6±0.2** 5.7±0.2**‡ block for the immunohistochemical microscopic study. The FS (%) 35±2 24±2.9** 30±1.7 EDV (μl) 427±15 636±24** 532±22**‡ sections were placed on silanized glass slides (No.S3003, EF (%) 72±5 49±3** 62±3*† DAKO Japan, Kyoto, Japan), which were then dried, E wave (cm/s) 70±5 93±3** 84±5* dewaxed in xylene, and rehydrated in graded concentra- A wave (cm/s) 46±3 13±1** 32±4**† tions of ethanol. After incubation with normal blocking E/A 1.6±0.2 7.3±0.4** 3.1±0.4**‡ serum, the sections were incubated overnight at 4°C with EDV, end-diastolic volume; EF, ejection fraction; FS, fractional shorten- monoclonal antibody against connexin-43 (ZYM#71-0700, ing; LVDd, LV end-diastolic dimension; LVDs, LV end-systolic dimension. Zymed Laboratories,
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