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Thickness After Heart Transplantation Acute Cellular Rejection and Left Downloaded from heart.bmj.com on 19 November 2006 Intragraft interleukin 2 mRNA expression during acute cellular rejection and left ventricular total wall thickness after heart transplantation H A de Groot-Kruseman, C C Baan, E M Hagman, W M Mol, H G Niesters, A P Maat, P E Zondervan, W Weimar and A H Balk Heart 2002;87;363-367 doi:10.1136/heart.87.4.363 Updated information and services can be found at: http://heart.bmj.com/cgi/content/full/87/4/363 These include: References This article cites 27 articles, 5 of which can be accessed free at: http://heart.bmj.com/cgi/content/full/87/4/363#BIBL 1 online articles that cite this article can be accessed at: http://heart.bmj.com/cgi/content/full/87/4/363#otherarticles Rapid responses You can respond to this article at: http://heart.bmj.com/cgi/eletter-submit/87/4/363 Email alerting Receive free email alerts when new articles cite this article - sign up in the box at the service top right corner of the article Topic collections Articles on similar topics can be found in the following collections Other Cardiovascular Medicine (2051 articles) Transplantation (283 articles) Molecular Medicine (1113 articles) Other immunology (943 articles) Notes To order reprints of this article go to: http://www.bmjjournals.com/cgi/reprintform To subscribe to Heart go to: http://www.bmjjournals.com/subscriptions/ Downloaded from heart.bmj.com on 19 November 2006 363 BASIC RESEARCH Intragraft interleukin 2 mRNA expression during acute cellular rejection and left ventricular total wall thickness after heart transplantation H A de Groot-Kruseman, C C Baan, E M Hagman, W M Mol, H G Niesters, A P Maat, P E Zondervan, W Weimar, A H Balk ............................................................................................................................. Heart 2002;87:363–367 Objective: To assess whether diastolic graft function is influenced by intragraft interleukin 2 (IL-2) mes- senger RNA (mRNA) expression in rejecting cardiac allografts. Design: 16 recipients of cardiac allografts were monitored during the first three months after transplantation. The presence of IL-2 mRNA in endomyocardial biopsies (n = 123) was measured by reverse transcriptase polymerase chain reaction. To determine heart function, concurrent M mode and See end of article for authors’ affiliations two dimensional Doppler echocardiograms were analysed. ....................... Results: Histological signs of acute rejection (International Society for Heart and Lung Transplantation (ISHLT) rejection grade > 2) were strongly associated with IL-2 mRNA expression (IL-2 mRNA was Correspondence to: DrHAde present in 12 of 20 endomyocardial biopsies (60%) with acute rejection and in 24 of 103 endomyo- Groot-Kruseman, University cardial biopsies (23%) without acute rejection, p = 0.002). No significant relation was found between Hospital Rotterdam, either histology or IL-2 mRNA expression alone and the studied echocardiographic parameters. How- Department of Internal ever, stratification of the echocardiographic data into those of patients with and those without acute Medicine, Room Bd 299, rejection showed that during acute rejection IL-2 mRNA expression was significantly associated with Dr Molewaterplein 40, 3015 GD Rotterdam, increased left ventricular total wall thickness (mean change in total wall thickness was +0.22 cm in Netherlands; patients with IL-2 mRNA expression versus −0.18 cm in patients without IL-2 mRNA expression, [email protected] p = 0.048). Accepted Conclusions: An increase in left ventricular total wall thickness precedes IL-2 positive acute rejection 21 November 2001 after heart transplantation. Thus, cardiac allograft rejection accompanied by intragraft IL-2 mRNA ....................... expression may be indicative of more severe rejection episodes. eversible diastolic dysfunction of cardiac allografts in the function.89One of the crucial cytokines in the modulation of first postoperative months has been reported to correlate the alloimmune response is interleukin (IL) 2, which with reduced long term survival.1 This diastolic dysfunc- enhances the proliferation and differentiation of specific T R 10 11 tion can be the result of acute rejection, a major complication lymphocytes directed against the allograft. In non- shortly after transplantation.2 However, not all histologically transplant settings, IL-2 has been shown to cause dysfunction proven acute rejection episodes result in changes of diastolic of the heart both in experimental and in clinical studies.12 13 A function parameters. The underlying mechanism of the dose dependent negative inotropic effect of IL-2 was observed difference between acute rejection episodes with and those in isolated hamster papillary muscle preparations.12 Moreover, without impaired heart function is unknown but may involve intravenous administration of IL-2 in patients with cancer 2 the local or systemic release of cytokines. causes cardiovascular side effects including decreased ejection Acute cellular rejection is morphologically characterised by fraction, decreased blood pressure, increased heart rate, and the presence of a mononuclear cell infiltrate and signs of fluid retention.13 Therefore, we speculate that after transplan- myocyte damage on endomyocardial biopsy (EMB).3 The tation the local presence of IL-2 may be related to allograft combination of infiltrated immune competent cells with dysfunction by reflecting the severity of the immune response interstitial and perivascular oedema, vascular leakage of against the allograft and by its direct negative inotropic effect fibrin, and in the more severe cases diffuse myocyte necrosis can result in stiffness of the myocardium.4 Consequently, the on the myocardium. To determine whether local IL-2 acute rejection process may change left ventricular wall expression during histological rejection indeed affects diasto- dimensions and left ventricular filling parameters, reflecting lic graft function, we monitored serially sampled EMB for the the loss of diastolic heart function. Previously reported presence of IL-2 messenger RNA (mRNA) expression and for echocardiographic changes related to acute cellular rejection histological signs of acute rejection during the first three include increased left ventricular total wall thickness, months after heart transplantation. These findings were ana- increased peak early mitral flow velocity (E), decreased decel- lysed in relation to echocardiographic changes in wall dimen- eration time, and shortened isovolumetric relaxation sions and diastolic flow parameters. period.56 Alternatively, during vascular (humoral) rejection, cells of the microvasculature instead of myocytes may be the target of tissue injury, which has been associated with ............................................................. increased left ventricular mass and depressed myocyte − 47 Abbreviations: AR+, in the presence of acute rejection; AR , in the function. absence of acute rejection; cDNA, complementary DNA; E, peak early In addition to cell infiltration and tissue damage, local pro- mitral flow velocity; EMB, endomyocardial biopsy; IL, interleukin; ISHLT, duction of cytokines (low molecular weight regulatory International Society for Heart and Lung Transplantation; mRNA, proteins) during rejection may also influence myocardial messenger RNA; PCR, polymerase chain reaction www.heartjnl.com Downloaded from heart.bmj.com on 19 November 2006 364 de Groot-Kruseman, Baan, Hagman, et al Table 1 Demographics of the studied patients and the numbers of endomyocardial biopsies (EMB) positive for acute rejection (AR+) and interleukin 2 (IL-2) messenger RNA (mRNA) expression (IL-2+) Primary Patient Age (years) Sex disease EMB AR+ EMB IL-2+ EMB AR+/IL-2+ AR−/IL-2+ 120FCMP82110 252MIHD90505 3 60 M IHD Excluded from the study due to poor echocardiographic quality 448MIHD92422 558MCMP81110 651MCMP81211 756FCMP71312 858MIHD92321 953FCMP84202 10 50 M IHD 7 1 1 0 1 11 16 F CMP 6 2 2 2 0 12 54 M IHD 8 2 4 1 3 13 43 M CMP 8 2 3 1 2 14 55 M IHD 9 0 2 0 2 15 58 M IHD 9 0 2 0 2 16 52 M IHD 10 0 1 0 1 Total 123 20 36 12 24 CMP, cardiomyopathy; F, female; IHD, ischaemic heart disease; M, male. METHODS thickness and end diastolic interventricular septum thickness. Patients Left ventricular total wall thickness was calculated by adding We studied 16 consecutive heart transplant recipients who end diastolic posterior wall thickness and end diastolic inter- were operated upon between November 1997 and October ventricular septum thickness. Two dimensional Doppler 1998. Table 1 summarises the demographic data of these echocardiograms were analysed for the following diastolic patients. Maintenance immunosuppressive therapy consisted function parameters: E, peak atrial mitral flow velocity (A), of ciclosporin A and low dose steroids. Serial EMB and E/A ratio, deceleration time of E, and isovolumetric relaxation echocardiograms during the first three months after trans- period. For Doppler echocardiogram analysis, means of 10 plantation were studied. Surveillance biopsies during this consecutive end expiratory beats were calculated. Beats that period were taken weekly during the first six weeks and were distorted by the recipient atrial contraction were not biweekly during the following eight weeks. During routine analysed with respect to deceleration time. The transmitral biopsies two additional samples were harvested for cytokine filling pattern was classified as “summation filling” when only studies after informed consent of the patients. One patient
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