Transcoronary Transplantation of Progenitor Cells after Myocardial Infarction
Birgit Assmus, M.D., Jörg Honold, M.D., Volker Schächinger, M.D., Martina B. Britten, M.D., Ulrich Fischer-Rasokat, M.D., Ralf Lehmann, M.D., Claudius Teupe, M.D., Katrin Pistorius, M.D., Hans Martin, M.D., Nasreddin D. Abolmaali, M.D., Torsten Tonn, M.D., Stefanie Dimmeler, Ph.D., and Andreas M. Zeiher, M.D.
Background Pilot studies suggest that intracoronary transplantationof progenitor cells derived from bone marrow (BMC) or circulatingblood (CPC) may improve left ventricular function after acutemyocardial infarction. The effects of cell transplantation inpatients with healed myocardial infarction are unknown.
Methods After an initial pilot trial involving 17 patients,we randomly assigned, in a controlled crossover study, 75 patientswith stable ischemic heart disease who had had a myocardialinfarction at least 3 months previously to receive either nocell infusion (23 patients) or infusion of CPC (24 patients)or BMC (28 patients) into the patent coronary artery supplyingthe most dyskinetic left ventricular area. The patients in thecontrol group were subsequently randomly assigned to receiveCPC or BMC, and the patients who initially received BMC or CPCcrossed over to receive CPC or BMC, respectively, at 3 months'follow-up.
Results The absolute change in left ventricular ejection fractionwas significantly greater among patients receiving BMC (+2.9percentage points) than among those receiving CPC (–0.4percentage point, P=0.003) or no infusion (–1.2 percentagepoints, P<0.001). The increase in global cardiac functionwas related to significantly enhanced regional contractilityin the area targeted by intracoronary infusion of BMC. The crossoverphase of the study revealed that intracoronary infusion of BMCwas associated with a significant increase in global and regionalleft ventricular function, regardless of whether patients crossedover from control to BMC or from CPC to BMC.
Conclusions Intracoronary infusion of progenitor cells is safeand feasible in patients with healed myocardial infarction.Transplantation of BMC is associated with moderate but significantimprovement in the left ventricular ejection fraction after3 months. (ClinicalTrials.gov number, NCT00289822
[ClinicalTrials.gov]
.)
Chronic heart failure is common, and its prevalence continuesto increase.1 Ischemic heart disease is the principal causeof heart failure.2 Although myocardial salvage due to earlyreperfusion therapy has significantly reduced early mortalityrates,3 postinfarction heart failure resulting from ventricularremodeling remains a problem.4 One possible approach to reversingpostinfarction heart failure is enhancement of the regenerationof cardiac myocytes as well as stimulation of neovascularizationwithin the infarcted area. Initial clinical pilot studies havesuggested that intracoronary infusion of progenitor cells isfeasible and may beneficially affect postinfarction remodelingprocesses in patients with acute myocardial infarction.5,6,7,8,9However, it is currently unknown whether such a treatment strategymay also be associated with improvements in cardiac functionin patients with persistent left ventricular dysfunction dueto healed myocardial infarction with established scar formation.
Therefore, in the prospective TOPCARE-CHD (Transplantation ofProgenitor Cells and Recovery of LV [Left Ventricular] Functionin Patients with Chronic Ischemic Heart Disease) trial, we investigatedwhether intracoronary infusion of progenitor cells into theinfarct-related artery at least 3 months after myocardial infarctionimproves global and regional left ventricular function.
Methods
Patients
Between January 2002 and December 2004, a total of 92 patientswho had had a myocardial infarction at least 3 months previouslywere recruited into the study at a single center. Patients between18 and 80 years of age were eligible for inclusion in the studyif they had had a documented myocardial infarction at least3 months before inclusion and had a well-demarcated region ofleft ventricular dysfunction and a patent infarct-related artery.Exclusion criteria were the presence of acutely decompensatedheart failure with a New York Heart Association (NYHA) classof IV, a history of other severe chronic diseases or cancer,or unwillingness to participate. The ethics review board ofthe Johann Wolfgang Goethe University in Frankfurt, Germany,approved the protocol; the trial was registered according tothe German Drug Law (accession numbers, 0703/01 and 0704/01);and the study was conducted in accordance with the Declarationof Helsinki. Written informed consent was obtained from eachpatient.
Study Design
The study consisted of three phases: a pilot trial comprising17 patients (7 receiving progenitor cells derived from bonemarrow [BMC] and 10 receiving progenitor cells derived fromcirculating blood [CPC]); a second phase, in which 75 patientswere randomly assigned to receive intracoronary infusion ofBMC (28 patients) or CPC (24) or no cell infusion (23); anda third phase, in which the 75 randomly assigned patients crossedover to one of the active treatments if they had originallybeen in the control group or to the alternate cell type if theyhad initially received intracoronary cell infusion (Figure 1).
Eligible patients with chronic ischemic cardiomyopathy had a severely hypokinetic area on the baseline left ventricular angiogram (LVA) and had had a myocardial infarction at least 3 months previously.
The primary end point of the study was the absolute change inglobal left ventricular ejection fraction (LVEF) as measuredby quantitative left ventricular angiography 3 months aftercell infusion. Secondary end points included quantitative variablesrelating to the regional left ventricular function of the targetarea, as well as left ventricular volumes derived from serialleft ventricular angiograms. In addition, functional statuswas assessed by NYHA classification. Finally, event-free survivalwas defined as freedom from death, myocardial infarction, stroke,or rehospitalization for worsening heart failure. Causes ofrehospitalization during follow-up were verified by review ofthe discharge letters or charts of hospital stays.
Preparation and Transplantation of Progenitor Cells
For patients assigned to receive CPC, mononuclear cells wereisolated by Ficoll density-gradient centrifugation of 270 mlof venous blood and cultured for 3 days ex vivo, as previouslyreported.6,7,9,10,11,12 A mean of 22x106±11x106 CPC wereinfused. For patients assigned to receive BMC, 50 ml of bonemarrow aspirate was obtained while the patients were under localanesthesia on the morning of cell-transplantation day. BMC wereisolated by Ficoll density-gradient centrifugation, as previouslyreported.6,7,9 We infused a mean of 205x106±110x106 BMC,of which on average less than 1% were positive for the hematopoieticprogenitor-cell marker CD34.
For cell transplantation, arterial puncture was followed bythe administration of 7500 to 10,000 U of heparin and (in 89%of the cell-treated patients) a bolus of abciximab (0.25 mgper kilogram of body weight). Cells were infused into the vesselsupplying the most dyskinetic left ventricular area by meansof a balloon catheter with a stop-flow technique, as previouslydescribed.6
Evaluation of Safety and Feasibility
Clinical, laboratory, and safety-related data were prospectivelycollected. Follow-up visits after 3 months were performed byphysicians. Procedural complications were defined as any ventriculararrhythmia, visible thrombus formation, distal embolization,or injury of the coronary artery associated with the cell-infusioncatheterization procedure. For patients undergoing bone marrowaspiration, potential bleeding complications were assessed.During hospitalization, telemetry was routinely performed for24 hours after the procedure in all patients.
Left Ventricular Angiography
Left ventricular angiograms were obtained at the time of thebaseline procedure and at 3 months' follow-up. Quantitativeanalysis of paired left ventricular angiograms recorded in identicalprojections was performed by an investigator who was blindedto the individual patients' treatments; the analysis was performedwith QCA-CMS software (version 5.2, Medis), as described elsewhere.6,7,9
Magnetic Resonance Imaging
In a subgroup of 35 patients who did not have implanted defibrillatorsor pacemakers and who consented to and tolerated the imagingprocedure, cardiac magnetic resonance imaging (MRI) (a 1.5-Tsystem; Magnetom Sonata, Siemens Medical Solutions) was performedat baseline and at 3 months' follow-up. The results were analyzedas previously described7 by an experienced investigator whowas blinded to the type of cells infused.
Detection of Viable Myocardium
All patients underwent low-dose dobutamine stress echocardiography,combined thallium single-photon-emission computed tomographyand [18F]fluorodeoxyglucose positron-emission tomography, orboth, as previously described.6 It was possible to analyze regionalleft ventricular viability in 80 patients (87%).
Statistical Analysis
Continuous variables are presented as means (±SD), unlessotherwise noted. Categorical variables were compared with useof the chi-square test or Fisher's exact test. Statistical comparisonsbetween initial and follow-up data were performed in a nonparametric,paired fashion with use of the Wilcoxon signed-rank test. NonparametricMann–Whitney U tests and Kruskal–Wallis tests wereused to compare continuous variables with categorical variablesas well as to compare the results between treatment groups.Bonferroni-adjusted analysis-of-variance testing was used forbetween-group analysis of quantitative left ventricular angiographicresults in phases 1 and 2 (the pilot phase and first randomizedphase). For multivariate analysis, the treatment groups werecategorized as follows: control, 0; CPC, 1; and BMC, 2. Themultivariate analysis was performed with use of a stepwise linearregression model with a forward-entry stepping algorithm; variableswith a P value of 0.05 on univariate analysis were entered inthe model. Statistical significance was assumed for P valuesof less than 0.05. All statistical analyses were performed withSPSS software (version 12.0).
Results
Baseline Characteristics of the Patients
A total of 92 patients were enrolled in the study. Of these,35 patients received BMC as their initial treatment (in phases1 and 2 of the trial), 34 patients received CPC (in phases 1and 2), and 23 patients received no intracoronary cell infusion(in phase 2, as the control group). Table 1 illustrates thatthe three groups of patients were well matched.
Table 1. Baseline Characteristics of the Patients.
Effects of Progenitor-Cell Infusion
Quantitative Characteristics of Left Ventricular Function
Patients with an adverse clinical event (six), subtotal stenosisof the target vessel at follow-up (three), an intraventricularthrombus precluding performance of left ventricular angiography(one), or atrial flutter or fibrillation at follow-up (one)were excluded from the exploratory analysis. In addition, ofthe 81 eligible patients, left ventricular angiograms couldnot be quantitatively analyzed in 4 because of inadequate contrastopacification, in 1 because of ventricular extrasystoles, andin 4 because of the patients' refusal to undergo invasive follow-up.Thus, a total of 72 of 81 serial paired left ventricular angiogramswere available for quantitative analysis (28 in the BMC group,26 in the CPC group, and 18 in the control group).
Table 2 summarizes the angiographic characteristics of the 75patients included in the randomized phase of the study. At baseline,the three groups did not differ with respect to global LVEF,the extent or magnitude of regional left ventricular dysfunction,left ventricular volumes, or stroke volumes.
Table 2. Quantitative Variables Pertaining to Left Ventricular Function, as Assessed by Left Ventricular Angiography.
The absolute change in global LVEF from baseline to 3 monthsdid significantly differ among the three groups of patients.Patients receiving BMC had a significantly larger change inLVEF than patients receiving CPC (P=0.003) and those in thecontrol group (P<0.001). Similar results were obtained whenpatients from the first two phases of the study (the pilot phaseand the randomized phase) were pooled. The results did not differwhen patients without evidence of viable myocardium before inclusionwere analyzed separately. The change in LVEF was –0.3±3.4percentage points in the control group (9 patients), +0.4±3.0percentage points in the CPC group (18 patients), and +3.7±4.0percentage points in the BMC group (18 patients) (P=0.02 forthe comparison with the control group and P=0.02 for the comparisonwith the CPC group).
In the subgroup of 35 patients who underwent serial assessmentof left ventricular function by MRI, MRI-derived global LVEFincreased significantly, by 4.8±6.0% (P=0.03) among thosereceiving BMC (11 patients) and by 2.8±5.2% (P=0.02)among those receiving CPC (20 patients), whereas no change wasobserved in 4 control patients (P=0.14). Thus, MRI-derived assessmentof left ventricular function further corroborated the resultsobtained from the total patient population.
Analysis of regional left ventricular function revealed thatBMC treatment significantly increased contractility in the centerof the left ventricular target area (Table 2). Likewise, MRI-derivedregional analysis of left ventricular function revealed thatthe number of hypocontractile segments was significantly reduced,from 10.1±3.6 to 8.7±3.6 segments (P=0.02), andthe number of normocontractile segments significantly increased,from 3.8±4.5 to 5.4±4.6 segments (P=0.01), inthe BMC group, whereas no significant changes were observedin the CPC group. MRI-derived infarct size, as measured by lateenhancement volume normalized to left ventricular mass, remainedconstant both in the CPC group (25±18% at baseline and23±14% at 3 months, 13 patients) and in the BMC group(20±10% at both time points, 9 patients). Thus, takentogether, the data suggest that intracoronary infusion of BMCis associated with significant improvements in global and regionalleft ventricular contractile function among patients with persistentleft ventricular dysfunction due to prior myocardial infarction.
To identify independent predictors of improved global LVEF,a stepwise multivariate regression analysis was performed; itincluded classic determinants of LVEF as well as various baselinecharacteristics of the three groups (Table 3). The multivariateanalysis identified the type of progenitor cell infused andthe baseline stroke volume as the only statistically significantindependent predictors of LVEF recovery.
Table 3. Stepwise Linear Regression Analysis for Predictors of Improvement in Global Left Ventricular Ejection Fraction.
Functional Status
The functional status of the patients, as assessed by NYHA classification,improved significantly in the BMC group (from 2.23±0.6to 1.97±0.7, P=0.005). It did not improve significantlyeither in the CPC group (class, 2.16±0.8 at baselineand 1.93±0.8 at 3 months; P=0.13) or in the control group(class, 1.91±0.7 and 2.09±0.9, respectively; P=0.27).
Randomized Crossover Phase
Of the 24 patients who initially were randomly assigned to CPCinfusion, 21 received BMC at the time of their first follow-upexamination. Likewise, of the 28 patients who initially wererandomly assigned to BMC infusion, 24 received CPC after 3 months.Of the 23 patients of the control group, 10 patients receivedCPC and 11 received BMC at their reexamination at 3 months (Figure 1).As illustrated in Figure 2, regardless of whether patients receivedBMC as initial treatment, as crossover treatment after CPC infusion,or as crossover treatment after no cell infusion, global LVEFincreased significantly after infusion of BMC. In contrast,CPC treatment did not significantly alter LVEF when given eitherbefore or after BMC.
Figure 2. Absolute Change in Quantitative Global Left Ventricular Ejection Fraction (LVEF) during the Crossover Phase of the Trial.
Data at 3 and 6 months are shown for all patients crossing over from BMC to CPC infusion (18 patients), from CPC to BMC infusion (18 patients), and from no cell infusion to either CPC infusion (10 patients) or BMC infusion (11 patients). I bars represent standard errors.
Thus, the intrapatient comparison of the different treatmentstrategies not only documents the superiority of intracoronaryinfusion of BMC over the infusion of CPC for improving globalleft ventricular function, but also corroborates our findingsin the analysis of data according to initial treatment assignment.The preserved improvement in cardiac function observed amongpatients who initially received BMC treatment and then crossedover to CPC treatment demonstrates that the initially achieveddifferences in cardiac function persisted for at least 6 monthsafter intracoronary infusion of BMC.
Procedural Safety and Clinical Outcomes
In 3 of the 135 intracoronary progenitor-cell–infusionprocedures (pooled data from all study phases), local dissectionof the coronary arterial wall was angiographically visible afterinflation of the balloon during cell infusion; in these casesthe dissection was successfully treated with immediate stentimplantation. However, two of these three patients had subsequentelevations in creatine kinase (Table 4). The further clinicalcourse of these three patients was uneventful. One additionalpatient required defibrillation from his implanted defibrillatorfor ventricular fibrillation during induction of myocardialischemia by transient balloon occlusion for cell infusion. Theclinical events before and after discharge from the hospitalare listed in Table 4.
Table 4. Clinical Events during the 3-Month Follow-up Period.
Discussion
Using a randomized, controlled trial design, we examined theeffects of intracoronary infusion of adult progenitor cellson global and regional left ventricular function in patientswith chronic ischemic heart disease who had had a myocardialinfarction at least 3 months previously. Our results demonstratethat infusion of BMC into the infarct-related artery is associatedwith moderate but significant improvements in both global andregional left ventricular contractile function. These improvementswere observed in the presence of full conventional pharmacologictreatment and lasted at least 6 months.
The application procedures, infusion media, and infused volumesof cell suspension were identical in the two intracoronary-infusiongroups. Therefore, potential confounding effects relating toischemic preconditioning or microvascular activation can beruled out in accounting for the improved cardiac function observedin the group treated with BMC. Moreover, intrapatient comparisonin the crossover phase of the trial rules out the possibilitythat differences in the patient populations studied may haveaffected outcomes. However, the mechanisms involved in mediatingimproved contractile function after intracoronary progenitor-cellinfusion are not well understood.
Experimentally, although there is no definitive proof that cardiacmyocytes may be regenerated, BMC were shown to contribute tofunctional recovery of left ventricular contraction when injectedinto freshly infarcted hearts,13,14,15 whereas CPC profoundlystimulated ischemia-induced neovascularization.16,17 Both celltypes were shown to prevent cardiomyocyte apoptosis and reducethe development of myocardial fibrosis and thereby improve cardiacfunction after acute myocardial infarction.18,19 Indeed, inour TOPCARE-AMI (Transplantation of Progenitor Cells and RegenerationEnhancement in Acute Myocardial Infarction) studies,6,7,9 intracoronaryinfusion of CPC was associated with functional improvementssimilar to those found with the use of BMC immediately aftermyocardial infarction. In the current study, however, whichinvolved patients who had had a myocardial infarction at least3 months before therapy, transcoronary administration of CPCwas significantly inferior to administration of BMC in alteringglobal left ventricular function.
This study does not explain the cellular mechanisms associatedwith the significantly improved left ventricular function inthe patients treated with BMC, nor does it explain the responsesto CPC infusion, which were of only borderline significance.It is likely that the smaller number of progenitor cells derivedfrom 270 ml of venous blood, which was 1/10 the number of monocyticcells obtained from 50 ml of bone marrow aspirate, may havecontributed to the smaller effects of CPC in improving leftventricular contractile function. Moreover, CPC obtained frompatients with chronic ischemic heart disease show profound functionalimpairments,20,21 which might limit their recruitment, afterintracoronary infusion, into chronically reperfused scar tissuemany months or years after myocardial infarction. Thus, additionalstudies in which larger numbers of functionally enhanced CPCare used will be required to increase the response to intracoronaryinfusion of CPC.
The magnitude of the improvement after intracoronary infusionof BMC, with absolute increases in global LVEF of approximately2.9 percentage points according to left ventricular angiographyand 4.8 percentage points according to MRI, was modest. However,it should be noted that the improvement in LVEF occurred inthe setting of full conventional pharmacologic treatment: morethan 90% of the patients were receiving beta-blocker and angiotensin-converting–enzymeinhibitor treatment. Moreover, results from trials of contemporaryreperfusion for the treatment of acute myocardial infarction,which is regarded as the most effective treatment strategy forimproving left ventricular contractile performance after ischemicinjury, have reported increases in global LVEF of 2.8% (in theCADILLAC [Controlled Abciximab and Device Investigation to LowerLate Angioplasty Complications] trial) and 4.1% (in the ADMIRAL[Abciximab before Direct Angioplasty and Stenting in MyocardialInfarction Regarding Acute and Long-Term Follow-up] trial).22,23
The number of patients, as well as the duration of follow-up,is not sufficient to address the question of whether the moderateimprovement in LVEF associated with one-time intracoronary BMCinfusion is associated with reduced mortality and morbidityamong patients with heart failure secondary to previous myocardialinfarction. We conclude that intracoronary infusion of BMC isassociated with persistent improvements in regional and globalleft ventricular function and improved functional status amongpatients who have had a myocardial infarction at least 3 monthspreviously. Given the reasonable short-term safety profile ofthis therapeutic approach, studies on a larger scale are warrantedto examine its potential effects on morbidity and mortalityamong patients with postinfarction heart failure.
Supported by the Deutsche Forschungsgemeinschaft (FOR 501-1:WA 146/2-1), the Foundation Leducq Transatlantic Network ofExcellence for Cardiac Regeneration, the European Union EuropeanVascular Genomics Network (contract no. LSHM-CT-2003-503254),and the Alfried Krupp Stiftung (to Dr. Dimmeler).
Dr. Schächinger reports having received consulting feesfrom Guidant and AstraZeneca and lecture fees from AstraZeneca,Merck Sharp & Dohme, Pfizer, Novartis, Guidant, Boston Scientific,Boehringer Ingelheim, Sanofi-Aventis, and Lilly. Dr. Dimmelerreports being a member of the scientific advisory board of Guidant.Dr. Zeiher reports having received consulting fees from Guidant.Drs. Dimmeler and Zeiher report that they are cofounders oft2cure, a for-profit company focused on regenerative therapiesfor cardiovascular disease. They serve as scientific advisorsand are shareholders. No other potential conflict of interestrelevant to this article was reported.
We are indebted to the staff of our catheterization laboratories;to Beate Mantz, Isabel Geweyer, and Heike Braun (study nurses);to Tina Rasper (biologic technician); and to Arne Koch (MRIstaff member).
Source Information
From the Division of Cardiology and Molecular Cardiology, Department of Medicine III (B.A., J.H., V.S., M.B.B., U.F.-R., R.L., C.T., K.P., S.D., A.M.Z.), Division of Hematology, Department of Medicine II (H.M.), and the Department of Diagnostic and Interventional Radiology (N.D.A.), Johann Wolfgang Goethe University; and the Institute for Transfusion Medicine and Immunohematology, Red Cross Blood Donor Service, Baden–Württemberg–Hessen (T.T.) — both in Frankfurt, Germany. Drs. Assmus and Honold contributed equally to the article.
Address reprint requests to Dr. Zeiher at the Department of Medicine III, J.W. Goethe University, Theodor-Stern-Kai 7, 60590 Frankfurt, Germany, or at zeiher{at}em.uni-frankfurt.de.
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0.05 on univariate analysis were entered in the model. Statistical significance was assumed for P values of less than 0.05. All statistical analyses were performed with SPSS software (version 12.0). 
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