Discordance Between Pre and Post Cardiac Transplant Diagnosis

Cardiovascular Pathology Vol. 8, No. 1, January/February 1999:17–23

1998 by Elsevier Science Inc.655 Avenue of the Americas, New York, NY 10010

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Discordance Between Pre and Post Cardiac Transplant Diagnosis: Implications for Pre- and Postoperative Decision Making

Annalisa Angelini, MD,* Giovanni Maria Boffa, MD,

†

Ugolino Livi, MD,

‡

Agata Barchitta, MD,

†

Dino Casarotto, MD,

‡

Gaetano Thiene, MD*

Departments of *Pathology,

†

Cardiology and

‡

Cardiovascular Surgery, University Medical School of Padua, Padua, Italy

11

A correct clinical diagnosis in end-stage patients undergoing cardiac transplantation may haveimportant prognostic and therapeutic implications. A retrospective clinico-pathologic study was car-ried out in 257 patients who had undergone cardiac transplantation at the University of Padua. A dis-crepancy between clinical and pathological diagnosis was found in 20 cases (8%). Among 126patients with the clinical diagnosis of dilated cardiomyopathy, seven were found eventually to haveischemic heart disease (IHD), five myocarditis, one arrhythmogenic right ventricular cardiomyopa-thy (ARVC), and one non-compacted myocardium. Among the 87 patients with clinical diagnosis ofIHD, three turned out to be dilated cardiomyopathy and one granulomatous myocarditis. Among the10 patients with the clinical diagnosis of hypertrophic-restrictive cardiomyopathy, one had ARVCand one had cardiac fibroma. Altogether, only 24.5% underwent endomyocardial biopsy (EMB) and75% coronary angiography before transplantation. Missed diagnosis of myocarditis occurred inpatients in whom EMB was not carried out. EMB and coronary angiography might be indicatedroutinely in patients with apparent dilated cardiomyopathy, before proceeding to cardiectomy.

Cardiovasc Pathol 1999;8:17–23

© 1998 by Elsevier Science Inc.

The role of endomyocardial biopsy (EMB) for the diagnosisof disease that could ultimately lead to cardiac transplant isstill rather ill defined.

A question that awaits a clear answer is who on the waitinglist for transplantation should undergo EMB. The suspicion ofnonischemic cardiomyopathy has been so far considered as anindication for EMB (1–13), although even within this group theprocedure may have a different diagnostic value (14–22).

EMB is considered neither necessary nor to be per-formed in all the cardiomyopathies, because the histopatho-logical features are often not specific and not presentthroughout the myocardium; therefore, the biopsy is consid-ered poorly sensitive because of the risk of “sampling error”

(23). Recently, doubts have been advanced even regardingthe usefulness of performing EMB in cases of suspectedmyocarditis (24,25) or acute heart failure (26).

In the absence of a consensus on the role of EMB, it isreadily understandable why this diagnostic procedure is notincluded among the routine exams to be performed accord-ing to the Guidelines for the Evaluation and Management ofPatients with Heart Failure (26).

The aim of our study was to evaluate retrospectively thediagnostic procedures carried out at the University of Paduain patients entering the waiting list for and subsequently un-dergoing cardiac transplantation, in order to see whether theperformance of EMB may have improved the diagnostic ac-curacy and therefore influenced management and outcome.

Materials and Methods

We reviewed the clinical and pathologic findings of the257 orthotopic heart transplants performed at our institutionfrom November 1985 to February 1994.

Manuscript received April 10, 1998; revised July 8, 1998; acceptedJuly 31, 1998.

Address for correspondence: Gaetano Thiene, MD, Cardiovascular Pa-thology, Institute of Pathological Anatomy, Via A. Gabelli, 61, 35121 Padova,Italy. Tel:

1

39 049-8272283; Fax:

1

39 049-8272284; E-mail: [email protected]

18

ANGELINI ET AL. Cardiovasc Pathol Vol. 8, No. 1CLINICAL AND POST-TRANSPLANT PATHOLOGICAL DIAGNOSIS January/February 1999:17–23

Indication for transplant was given because of end-stageheart failure, after the following clinical diagnosis had beenachieved: dilated cardiomyopathy (126 patients), ischemicheart disease (IHD) (87 patients), valvular heart disease (21patients), hypertrophic-restrictive cardiomyopathy (10 pa-tients), congenital heart disease (6 patients), arrhyth-mogenic right ventricular cardiomyopathy (ARVC) (1 pa-tient), neoplasm (1 patient), graft failure (3 patients), activemyocarditis (2 patients) (see Table 1).

The procedures by which clinical diagnosis had been ac-complished are indicated in Figure 1. Diagnosis and indica-tion for cardiac transplantation were achieved either at theDepartment of Cardiology in Padua or elsewhere, our insti-tution being one of the referral centers for cardiac transplan-tation in northern Italy. Two-dimensional echocardiographywas performed in all the patients. Cardiac catheterizationwas carried out in all but two patients (one baby girl with acardiac fibroma and an adult male with sudden congestiveheart failure). Sixteen patients had only a right heart cathe-terization and two of them had EMB. Two hundred thirty-nine patients had right and left heart catheterization; ofthem, 202 (79%) had coronary angiography, whereas 37 didnot. In the former group 52 patients underwent EMB, in thelatter group only 9 patients. Thus, an overall number of 63patients (24.5%) underwent EMB.

The pathological study of all the hearts removed at trans-plantation consisted of gross and histologic examination.The hearts were fixed in formalin. Three transmural, 3-cmlong blocks of ordinary myocardium from left and rightventricles and ventricular septum were obtained from eachheart and embedded in paraffin. Sections were stained withhematoxilin and eosin (HE), Azan Mallory, elastic-VanGieson, congo red. Sections from the coronary arteries werehistologically studied when a lesion was found at gross ex-amination through serial transverse cuts.

Obstructive atherosclerotic coronary artery disease wasdiagnosed when at least one major coronary artery pre-

Table 1.

Cardiac Disease Requiring Transplantation (November 85–February 94)

ClinicalDiagnosis

PathologicalDiagnosis

Cardiac Disease

n

(%)

n

(%)

Dilated cardiomyopathy 126 49.0 115 48.8Ischemic heart disease 87 33.8 90 35.0Valvular disease 21 8.1 21 8.1Hypertrophic-restrictive cardiomyopathy 10 3.9 8 3.1Congenital heart disease 6 2.4 7 2.7Arrhythmogenic right ventricular

cardiomyopathy 1 0.4 3 1.2Neoplasm 1 0.4 2 0.8Graft failure 3 1.2 3 1.2Active myocarditis 2 0.8 8 3.1Total 257 100 257 100

Figure 1. Procedures by which clinical diagnosis was achieved.

Cardiovasc Pathol Vol. 8, No. 1 ANGELINI ET AL.

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January/February 1999:17–23 CLINICAL AND POST-TRANSPLANT PATHOLOGICAL DIAGNOSIS

sented at histology with cross-sectional narrowing

.

70%.The term “obstructive” plaque, should be considered simplya histologically, high-degree stenosis and not necessarily a“critical lesion” (27).

The diagnosis of myocarditis was made by applying theDallas criteria (28).

Immunohistochemical studies were performed in orderto characterize the inflammatory infiltrate and in the pres-ence of tumors. The following monoclonal antibodies wereused: CD45 (DAKO, diluition 1:20), CD43 (CLONAB,1:40), CD45RO (DAKO, 1:100), CD20 (DAKO, 1:100),CD68 (DAKO, 1:50), Mac 387 (DAKO, 1:100), FactorVIII-related antigen (DAKO, 1:300), vimentin (DAKO, 1:50),desmin (DAKO, 1:50), alfa-actin (DAKO, 1:50). The avidin-biotin-peroxidase complex was used as detection system.

Statistics

Differences between concordant and discordant diagno-sis were evaluated by means of Fisher’s exact test. Five per-cent difference was considered statistically significant.

Results

A discordance between clinical and pathological diagno-sis emerged in 20 out of 257 cases (8%) (see Tables 2 and 3).

Of the 126 patients in whom the clinical diagnosis of di-lated cardiomyopathy was achieved, 112 (88%) presentedwith a concordant pathological diagnosis, while 14 (12%)did not (Table 2). Of these, seven patients turned out to havean ischemic heart disease with proximal obstructive coro-

Table 3.

Patients with a Discordant Diagnosis

Number Age Clinical DiagnosisPathologicalDiagnosis

CardiacCatheter

EndomiocardialBiopsy

CoronaryAngiography

1 39 Dilated cardiomyopathy Ischemic heart disease Yes No Yes 2 42 Dilated cardiomyopathy Ischemic heart disease Yes No Yes3 39 Dilated cardiomyopathy Ischemic heart disease Yes No No4 58 Dilated cardiomyopathy Ischemic heart disease Yes No Yes5 59 Dilated cardiomyopathy Ischemic heart disease Yes No No6 68 Dilated cardiomyopathy Ischemic heart disease Yes No No7 50 Dilated cardiomyopathy Ischemic heart disease Yes No Yes8 39 Dilated cardiomyopathy Myocarditis Yes No No9 42 Dilated cardiomyopathy Myocarditis Yes No No

10 39 Dilated cardiomyopathy Myocarditis Yes No No11 58 Dilated cardiomyopathy Myocarditis Yes No No12 59 Dilated cardiomyopathy Myocarditis Yes No No13 20 Dilated cardiomyopathy Arrhythmogenic RV cardiomyopathy Yes Yes Yes14 15 Dilated cardiomyopathy Non-compacted myocardium Yes Yes Yes15 49 Ischemic heart disease Dilated cardiomyopathy,

left ventricular aneurysmsYes No Yes

16 39 Ischemic heart disease Sarcoid myocarditis, left ventricular aneurysm

Yes No Yes

17 52 Ischemic heart disease Dilated cardiomyopathy, left ventricular aneurysms

Yes No Yes

18 54 Ischemic heart disease Dilated cardiomyopathy,left ventricular aneurysms

Yes No Yes

19 41 Hypertrophic-restrictivecardiomyopathy

Arrhythmogenic RV cardiomyopathy Yes Yes Yes

20 40 Hypertrophic-restrictivecardiomyopathy

Cardiac fibroma No No No

Table 2

. Discrepancy Between Clinical and Pathological Diagnosis

Cardiac DiseaseClinical

TotalPathologicalConcordant

PathologicalDiscordant

Dilated cardiomyopathy 126 (100%) 112 (88%) 14 (12%)Ischemic heart disease 87 (100%) 83 (95%) 4 (5%)Hypertrophic-restrictive cardiomyopathy 10 (100%) 8 (80%) 2 (20%)

20


nary artery disease, in the setting of mild to moderate myo-cardial damage (Figure 2), five patients had myocarditis(Figure 3), one had ARVC, and another one a congenitalheart disease (non-compacted myocardium). Of the 87 pa-tients with a clinical diagnosis of IHD, 83 (95%) showed aconcordant pathological diagnosis, while four (5%) did not.

Of these, the final pathological diagnosis was dilated cardi-omyopathy in three and sarcoid myocarditis in one (Figure4), all with ventricular aneurysms. Of the 10 patients with aclinical diagnosis of hypertrophic-restrictive cardiomyopathy,eight (80%) had a concordant diagnosis while two (20%)did not: one showed ARVC and one had cardiac fibroma.

Figure 2. Obstructive atherosclerotic lesion of the proximal descending coronary artery in a 68-year-old male patient with clinical diagnosis of dilated cardiomyopathy and no pretransplant coro-nary angiography. (Hematoxylin-eosin, 312.)

Figure 3. Lymphocytic myocarditis in a 39-year-old man with a clinical diagnosis of dilated cardi-omyopathy, which was put forward in the absence of pre-transplant endomyocardial biopsy. Hema-toxylin-eosin, 360.)


21


The review of the diagnostic work-up, performed in allthe transplanted patients in order to identify possible sourceof error, led to the following results (Table 4).

Dilated Cardiomyopathy (126 Cases)

Among the 112 patients with a concordant pathologicaldiagnosis, right and left cardiac catheterization was performed

in 100 patients (89%) associated with coronary angiographyin 80 patients (71%) and with EMB in 45 patients (37%).Eleven patients (10%) underwent right catheterization andEMB was performed only in one of them. One patient wastransplanted solely on the basis of echocardiographic evalu-ation. Of the group of 14 patients with a discordant diagno-sis, all had a cardiac catheterization but coronary angiogra-

Figure 4. Sarcoid myocarditis in a 39-year-old female patient who was clinically diagnosed as af-fected by ischemic heart disease, despite the normal coronary angiography, because of the presenceof left ventricular aneurysm. Pre-transplant endomyocardial biopsy was not performed. (Hematoxy-lin-eosin, 360.)

Table 4.

Procedures Performed in the Setting of Concordant and Discordant Diagnosis in Relation to the Different Pathology

Concordant Diagnosis Discordant Diagnosis

EMB COR EMB COR

Dilated CardiomyopathyLRCath 100 45 80 14 2 6Rcath 11 1 – – – –ECHO 1 – – – – –Total 112 46 (37.5%)

a

80 (71%) 14 2 (14%)

a

6 (43%)Ischemic Heart Disease

LRCath 82 4 77 4 1 4Rcath 1 – – – – –ECHO – – – – – –Total 83 4 (5%) 77 (93%) 4 1 4

Hypertrophic-Restrictive Cardiomyopathy

LRCath 7 5 4 1 1 –Rcath 1 1 – – – –ECHO – – – 1 – –Total 8 6 (75%) 4 (50%) 2 1 (50%) –

Abbreviations: COR

5

coronary angiography; ECHO

5

echocardiogram; EMB

5

endomyocardial biopsy;LRCath

5

left and right catheterization; Rcath

5

right cardiac catheterization.

a

p

5

0.004.

22


phy was performed in 6 (43%) and EMB in two (14%) (

p

5

0.004 vs concordant diagnostic group). Of the seven caseswith the final pathological diagnosis of IHD, four had a cor-onary angiography; among the five patients in whom thepathological diagnosis merged into myocarditis, none hadundergone EMB (Table 3).

IHD (87 Cases)

Among the 83 (95%) patients with a concordant diagno-sis, right and left cardiac catheterization was performed in82 patients (99%) associated with coronary angiography in77 (93%) and EMB in four (5%). One patient underwentonly a right catheterization. Of the four patients with a dis-cordant diagnosis, none had EMB and all underwent coro-nary angiography (Table 3).

Hypertrophic-Restrictive Cardiomyopathy (10 Cases)

Of the eight patients (80%) with a concordant diagnosis,right and left cardiac catheterization was performed inseven (87.5%) associated with coronary angiography in four(50%) and EMB in five (62.5%); only one had right cathe-terization with EMB. Of the two patients with a discordantdiagnosis, both had left and right catheterization with EMBin one disclosing remarkable fibrosis; in this patient the ulti-mate diagnosis was ARVC, while in the other one, a 42 yearold female with final pathological diagnosis of cardiac fi-broma of the interventricular septum, disproportional thick-ening of the ventricular septum had been misinterpreted asasymmetric hypertrophic cardiomyopathy.

Discussion

Our results show that in 8% of cardiac transplanted pa-tients at our institution from 1985 to 1994 there was a dis-cordance between the pre-transplant clinical diagnosis andthe pathological diagnosis achieved after transplant. Aneven higher discrepancy was recently reported by Bortmanet al. (29). These findings are of utmost importance, takinginto consideration the way that an incorrect diagnosis of ahereditary disorder discovered on pathological examinationmay have implications for the family of the recipient.

The highest percentage of discordance was found in thegroup of dilated cardiomyopathy, and was mainly attribut-able to misdiagnosed IHD and myocarditis. Interestingly,the pathologic diagnosis of IHD was missed, although a cor-onary angiography had been performed in four of the sevenmisdiagnosed patients, because of underestimated coronaryartery disease. These patients, because of proximal site ofobstructive coronary lesion and presence of enough viablemyocardium, might have been potentially amenable to sur-gical revascularization as an alternative to transplant. Amongthe five patients with post-transplant diagnosis of myocardi-tis, none had undergone EMB, which would have increased

the chance of achieving a correct diagnosis. We do notagree with Davies and Ward (23) who deny the usefulnessof performing EMB in myocarditis. If this may be true forfocal myocarditis, which is mainly clinically characterizedby arrhythmias or could mimic IHD, this is not the case ofdiffuse involvement of the myocardium, which may lead tocardiac dilatation and end-stage heart failure, as is the caseof patients requiring transplantation. The achievement of acorrect diagnosis of myocarditis is mandatory, first becauseof the possibility of an alternative therapeutic option throughimmunosuppressive therapy, even though the data from theMulticenter Myocarditis Trial did not show demonstrabletherapeutic benefit for immunosuppression in cases of activemyocarditis (24,25). Moreover, patients with myocarditishave also a high chance of more severe and frequent rejec-tions as well as of recurrence of native disease (30).

Other data in favor of pre-transplant cardiac biopsyemerge also from the analysis of our four patients with aclinical diagnosis of IHD. This diagnosis was put forwardbecause of the presence of aneurysms of the left ventricle,despite angiographic evidence of apparently normal coro-nary arteries or no critical stenosis. These patients weretransplanted for medically refractory heart failure, so itwould not really matter if they had IHD or not, since trans-plant would have been the treatment of choice. Nonetheless,the definitive histopathologic diagnosis was dilated cardi-omyopathy with left ventricular aneurysms in three cases,and sarcoid myocarditis in the other. In the latter case, astudy of other organs would have been also indicated, assarcoidosis is a systemic disease with secondary localiza-tion in the cardiac muscle, and immunosuppression mighthave constituted an alternative medical therapy to transplan-tation, even though immunosuppression in sarcoid heart dis-ease entails the risk of promoting aneurysm formation (31).

From our experience, it emerges that in patients withheart muscle disease there was an excessive diagnostic dis-cordance that might have been avoided in part by perform-ing EMB. McKenna and Davies (25) think that there aregood reasons not to perform cardiac biopsies with conven-tional histologic staining to diagnose acute myocarditis inpatients with heart failure of recent onset. On the otherhand, Mason and O’Connel (12) recognized the clinicalmerit of EMB and, accordingly, we agree with the recom-mendations of the AHA Scientific Council Special Reporton Heart Transplantation (2) which in the setting of non-ischemic dilated cardiomyopathy consider EMB an indica-tion to prove or exclude the presence of active lymphocyticmyocarditis or to confirm or exclude other potentially re-versible causes of heart failure, such as hemochromatosis orconditions that may represent a contraindication to hearttransplantation, such as amyloidosis.

Thus, our suggestion is that, whenever heart muscle dis-ease is suspected, EMB may be indicated to increase the di-agnostic accuracy, to avoid unnecessary orthotopic cardiactransplant, and to obtain a better management of trans-


23


planted patients. This aspect is important in the light of thedonor shortage and the possible alternative therapeutic op-tions to heart transplantation. If fact, in the cases whichturned out to be IHD, a coronary revascularization mighthave been performed while in the cases diagnosed as myo-carditis, immunosuppressive therapy, as well as conserva-tive approaches, such as temporary mechanical ventricularassistance or heterotopic transplantation, might have beenattempted to allow the recovery of contractile function.

This paper was supported by Veneto Region–Venice, and by MURST–

Rome, Italy.

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Discordance Between Pre and Post Cardiac Transplant Diagnosis