Familial dilated cardiomyopathy: clinical features in French families
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1 Ž. European Journal of Heart Failure Familial dilated cardiomyopathy: clinical features in French families Laurence Mangin a, Philippe Charron a,b,c, Frederique Tesson a,c, Alain Mallet c,d, Olivier Dubourg e, Michel Desnos f, Azziz Benaısche a, Christian Gayet g, Pierre Gibelin h, Jean-Marc Davy i, Jacques Bonnet j, Daniel Sidi k, Ketty Schwartz c,l, Michel Komajda a,b,c, a Laboratoire de Genetique et Insuffisance Cardiaque, Association Claude Bernard, Hopital ˆ Pitie-Salpetriere, ˆ ` 47 Bd de l Hopital, ˆ Paris Cedex 13, France b Ser ice de Cardiologie, Pa illon Rambuteau Hopital, ˆ Pitie-Salpetriere, ˆ ` 47 Bd de l Hopital, ˆ Paris Cedex 13, France c Institut Federatif de Recherche Coeur, Muscle, Vaisseaux, Hopital ˆ Pitie Salpetriere, ˆ ` 47 Bd de l Hopital, ˆ Paris Cedex 13, France d Inserm U436, Hopital ˆ Pitie-Salpetriere, ˆ ` Paris, France e Ser ice de Cardiologie, Hopital ˆ Ambroise Pare, Boulogne, France f Ser ice de Cardiologie, Hopital ˆ Boucicaut, Paris, France g Ser ice de Cardiologie, Hopital ˆ de la Croix Rousse, Lyon, France h Ser ice de Cardiologie, Hopital ˆ Pasteur, Nice, France i Ser ice de Cardiologie, Hopital ˆ Arnaud de Villeneu e, Montpellier, France j Ser ice de Cardiologie, Hopital ˆ du Haut-Le eque, Bordeaux, France k Ser ice de Cardiologie Pediatrique, Hopital ˆ Necker-Enfants Malades, Paris, France l Inserm U153, Hopital ˆ Pitie-Salpetriere, ˆ ` Paris, France Received 12 February 1999; received in revised form 9 July 1999; accepted 9 August 1999 Abstract The aims of the study were to analyze the clinical features, the penetrance and the mode of inheritance of 13 French families with dilated cardiomyopathy using diagnostic criteria recently established by a European collaboration. Methods: Screening consisted of physical examination, ECG and Echo of all the probands first degree relatives Ž n Using major Echo criteria ejection fraction Ž EF. 45% or FS 25% and left ventricular diameter Ž LVD. 117% of the predictive value, or combined minor Echo ECG criteria, relatives were classified as affected, unknown or healthy. Results: Ž. 1 Adult affected relatives Ž n 31. were identified with major Echo criteria in 74% of cases, and with combined minor Echo ECG criteria in 26% of cases. Ž. 2 In the unknown relatives Ž n 21., the most common abnormality was an isolated left ventricular dilation Ž 67%.. Ž 3. Mode of inheritance was autosomal dominant Ž AD. in 11 families and possibly autosomal recessive in two. Ž. 4 In AD families, the penetrance was incomplete in adults Ž 72%., age-related Ž O.R.: 1.3 per 10 years; 95% CI and sex-related greater in men Ž 87%. than in women Ž 61%., actuarial survival curve: P Ž. 5 Mortality related to end stage heart failure was 2.2 times as high as mortality related to sudden death Ž 11% vs. 5%.. Conclusions: Ž 1. In the absence of a specific phenotype of FDC, the characterization of relatives appears more accurate when minor criteria were added. Ž. 2 Since high mortality Ž 16%. and incomplete penetrance frequently give rise to small nuclei of clinically affected and alive relatives per family, the accurate model of penetrance that we proposed might be helpful in the future to enhance the statistical power of linkage analysis in this disease European Society of Cardiology. All rights reserved. Keywords: Familial dilated cardiomyopathy; Diagnostic criteria; ECG; Echo; Penetrance Corresponding author. Tel.: ; fax: Ž. address: michel.komajda@psl.ap-hop-paris.fr M. Komajda $ European Society of Cardiology. All rights reserved. Ž. PII: S
2 354 ( ) L. Mangin et al. European Journal of Heart Failure Introduction Idiopathic dilated cardiomyopathy Ž IDCM. is a heart muscle disease of unknown cause characterized by impaired systolic function and dilation of the left or both ventricles 1. Incidence of IDCM was estimated to be person-years and the prevalence was 36.5 per persons in the US population 2. However, the true incidence is probably higher, since many asymptomatic cases remain unrecognized. It is a major healthcare problem as IDCM leads to the development of progressive refractory heart failure and represents the first cause of heart transplantation indications 3. Familial cases have been underestimated until recent prospective studies revealed that at least 25% of patients with IDC had one or more affected first-degree relative 4. Studies about familial dilated cardiomyopathy Ž FDC. suggested different patterns of transmission with autosomal dominant trait prevailing and variable clinical features 4 7. Nevertheless, detailed phenotypic analysis of familial cases of IDCM are still rare. The aims of the present work are to analyze familial cases of IDCM in France according to new diagnostic criteria recently proposed by a European collaboration 8. Mode of inheritance, estimated penetrance of the disease and detailed phenotypic study were analyzed in 13 unrelated French families. 2. Methods 2.1. Clinical in estigations Families included in our study were selected by attending cardiologists aware of the national recruitment of familial cases of IDCM. Patients with IDCM who had at least two first degree relatives with documented disease were identified as familial cases Ž probands.. Thirteen probands were included for this study and all first degree relatives were analyzed. For the 118 relatives screened, informed consent was obtained in accordance with study protocol approved by the Comite d Ethique du Centre Hospitalier Universitaire de la Pitie-Salpetriere ˆ ` Ž Paris.. Clinical evaluation, standard 12 lead electrocardiogram Ž ECG., echocardiography Ž Echo. were performed and 24-h ECG Holter. For deceased relatives, medical records were reviewed and the diagnosis of dilated cardiomyopathy was based on the same criteria used for affected and alive relatives. Coronary angiography was performed in all probands, and in affected relatives only when an ischemic heart disease was suspected. Exclusion criteria were: systemic hypertension Žblood pressure mm Hg confirmed at repeated measurements., coronary heart disease Žob- struction 50% of the luminal diameter in a major branch., history of chronic excess of alcohol consumption Ž 100 g day. with remission of IDCM after 6 months of abstinence, high rate supraventricular arrhythmias, congenital disease and cor pulmonale. Echocardiographic and electrocardiographic criteria used in the study were recently established by a European collaboration 8. In addition, we also considered other minor ECG findings to compare the sensitivity of several criteria Echographic procedure and criteria M-Mode, two-dimensional echocardiography Žin- cluding parasternal short- and long-axis views, apical four- and two-chamber views. and Doppler ultrasonography were performed. Echocardiography images were stored on VHS videotape or on paper for subsequent analysis. Echocardiograms were analyzed independently by two experts without knowledge of the clinical status. Measurements of end diastolic left ventricular diameter were made on two-dimensional guided M-mode Echo at the onset of the QRS complex. Left ventricular Ž LV. ejection fraction was calculated with Teicholz s formula 9. Major diagnostic criteria for IDCM were: the presence of both echocardiographic ejection fraction Ž EF. of the LV 45%, and or fractional shortening Ž FS. 25%, with LV enlargement defined as LV end-diastolic diameter equal or 117% of the predictive value 10 corrected for age and body surface area Ž BSA.. Minor Echo diagnostic criteria were: Ž. 1 LV diameter Ž LVD. 112% of the predictive value; Ž 2. EF less than 50%; Ž. 3 FS less than 28%; Ž. 4 segmental wall motion abnormalities in the absence of intraventricular conduction defect or ischemic heart disease Electrocardiographic procedure and ECG 24-h Holter criteria Standard 12-lead electrocardiograms Ž ECG. were performed with patients in the supine position during quiet respiration. ECG were analyzed blindly. Minor diagnostic criteria were: Ž. 1 unexplained conduction disease: II or III atrio-ventricular conduction defects, complete left-ventricular bundle branch block Ž LBBB., sinus nodal dysfunction; and Ž 2. unexplained supraventricular Žatrial fibrillation or sustained arrhythmias. or ventricular arrhythmias Ž VA. Žfrequent, h or repetitive, 120 b.p.m..; both criteria before the age of Other ECG criteria studied Ž. Isolated left atrial enlargement LAE, PR duration 200 ms, QRS prolongation 120 ms, right bundle
3 ( ) L. Mangin et al. European Journal of Heart Failure branch block Ž RBBB., left ventricular hypertrophy assess by S wave in lead V1 R wave in lead V5 35 mm Ž i.e. Sokolow 35 mm., ST-T waves abnormality Definition of the clinical status Ž. 1 for the proband, presence of the major criteria Ž LV dilation and systolic dysfunction.; Ž 2. relatives were classified as affected in the presence of the major criteria, or marked LV dilation Ž 117% of the predictive value. one minor criterion, or three minor criteria; Ž. 3 relatives were classified as unknown in the presence of one or two minor criteria; and Ž. 4 relatives were classified as healthy in the absence of major or minor criteria Penetrance Since genes and mutations responsible for the disease in these families were not identified, the penetrance Žor frequency of the clinical expression of the disease among carriers of a mutation. was estimated indirectly, by comparing the observed and theoretical number of clinically affected subjects. All subjects at risk of inheriting the disease gene were analyzed. Only first degree relatives were included. Probands were excluded to ovoid potential bias 11. In autosomal dominant families, the penetrance was determined as the number of clinically affected subjects Ž n. divided by the number of subjects at risk of inheriting the disease gene Ž n., and multiplied by two Ž n n. 2 since the risk of having the disease gene is 1 2 in an autosomal dominant transmission pattern Statistical analysis Values are expressed as mean S.D. Concerning clinical features, an unpaired Student s t-test was used to compare parametrics data between two groups of relatives, P 0.05 was considered statistically significant. Concerning the penetrance, the effects of age was analyzed in a logistic model in which age and sex were taken into account and results were expressed by an odds ratio Ž increase per 10 years.. Effects of sex on age at onset were analyzed by cumulative distributions, according to an actuarial method, similar to that used in survival studies 11. Differences between curves were tested with the log rank test. 3. Results 3.1. Clinical features The pedigrees of the 13 families are shown in Figs. 1 and 2. Two affected relatives were excluded from the study because of the presence of a significant coronary artery disease on coronary angiography and two others had undergone orthotopic heart transplantation for end stage dilated cardiomyopathy at the time of the study. Four of the affected relatives were undiagnosed prior to the study and identified only through prospective screening. Medical reports were reviewed for 19 deceased and affected relatives. Mean age at death were years Ž range 8 75 years.. There was a high mortality in this population Ž 16%. and death related to end stage heart failure was 2.2 times as high as mortality related to sudden death Ž 11% vs. 5%.. Clinical data of probands and relatives are shown in Table 1. Thirty-six Ž 31%. relatives were clinically affected, 25 Ž 21%. unknown and 57 Ž 48%. healthy. In the affected relatives, 58% were in class I II of the NYHA. Our data revealed a delayed onset of the disease Ž years.. Echocardiographic and electrocardiographic analysis were performed for all the families but data are given only in the adult population Ž Table 2. to avoid bias due to the specific pediatric population. There was a significant difference between groups of affected, unknown and healthy relatives for diastolic dimension, systolic dimension, left ventricular ejection fraction and fractional shortening except between unknown and healthy relatives for the last criterion. Among relatives, 31 were classified as affected, since they fulfilled either the major Echo diagnostic criteria Ž or 74%., or the combined minor Echo ECG criteria Ž 8 31 or 26%. ŽFig. 3.. In the latter group, all had a LV dilation Ž 8 8. and only four had also a minor LV dysfunction. Among relatives classified as unknown, the most common abnormality was a marked and isolated LV dilation Ž or 67%.. None had a marked and isolated LV dysfunction and only one had a mild LV dysfunction without dilation. In the unknown group, no subject had minor ECG criteria Ž Table 2. according to European criteria. Concerning 24-h ECG Holter, ventricular arrhythmias were present in 19% of the affected relatives and supra-ventricular arrhythmias in 3%. ECG abnormalities Ž LBBB: 3. were found only in subjects classified as clinically affected Ž 3 31 or 10%.. Other ECG findings are given in Table 2: in the unknown group we found 8 21 or 38% of the minor ECG findings previously defined and 20% Ž of such abnormalities in the healthy group Mode of inheritance and penetrance There were 2.7 affected subjects Žprobands excluded. per family on average Ž range Two generations were studied in three families, three genera-
4 356 L. Mangin et al. European Journal of Heart Failure 1 ( 1999 ) Ž. Ž. Fig. 1. Pedigree of 13 families showing mode of inheritance of cardiomyopathy. The arrow shows the proband. Blackened squares male and circles female indicate confirmed cases of DCM. Half blackened symbols indicate unknown cases and crossed symbol subjects not examined. Three quarter blackened symbol indicate exclusion cases i.e. with DCM and significant coronary artery disease. Open symbols indicate normal subjects.
5 Ž. Ž. Fig. 2. Pedigree of 13 families showing mode of inheritance of cardiomyopathy. The arrow shows the proband. Blackened squares male and circles female indicate confirmed cases of DCM. Half blackened symbols indicate unknown cases and crossed symbol subjects not examined. Three-quarter blackened symbol indicate exclusion cases, i.e. with DCM and significant coronary artery disease. Open symbols indicate normal subjects. L. Mangin et al. European Journal of Heart Failure 1 ( 1999 )
6 358 L. Mangin et al. European Journal of Heart Failure 1 ( 1999 ) Fig. 3. Left: characteristics of affected relatives showing distribution according to left ventricular end diastolic diameter Ž LVEDD., ejection fraction Ž EF. and ECG abnormalities. Right: characteristics of unknown relatives showing distribution according to left ventricular end diastolic diameter Ž LVEDD. and ejection fraction Ž EF..
7 ( ) L. Mangin et al. European Journal of Heart Failure Table 1 Clinical data of probands and relatives a Probands A U H relatives relatives relatives Cases M F Age at study Ž year Age at diagnosis Ž year Dyspnea Ž NYHA. I II 5 21 III IV 8 15 a Notes: Values are mean S.D.; A, affected; U, unknown; H, healthy; M, male; F, female; NYHA, New York American Heart Ž functional status.. tions in nine, and four generations in one. In 11 families Ž 1 11., the mode of inheritance was autosomal dominant Ž AD., and it was indeterminate in two Ž Žpossibly autosomal recessive but not X-linked.. Estimated penetrance of the disease in AD families Ž 98 subjects, probands excluded. was 66% Ž in the total population and 72% Ž in the adult population Ž 18 years old.. The penetrance increased with age: 35% before the age of 18, 37% between 18 and 39, 96% between 40 and 59 years old and 100% after 60 years old and it was also higher in men Ž 87%. than in women Ž 61%.. Refined analysis in a logistic model indicated that the effect of age on the penetrance was statistically significant, and the increase could be quantified by the odds ratio: 1.3 per 10 years Ž 95% CI, The O.R. was similar in men and in women. Fig. 4 indicates age at onset of the disease, according to sex. Age at onset was significantly delayed in women as compared to men Žlog rank test: P Discussion This study is the first detailed phenotypic analysis using the European guidelines recently proposed for the study of familial dilated cardiomyopathy Ž FDC Diagnostic criteria Due to the fact that no gene has yet been identified in these French families, it was not possible to evaluate the sensitivity and the specificity of the two major diagnostic tools, i.e ECG and echocardiography as already performed in familial hypertrophic cardiomyopathy 12. If there is a general agreement for obviously affected individuals with marked cardiac dilation and profoundly reduced ejection fraction, differences exist for less typical clinical situations. Current diagnostic criteria 3 for dilated cardiomyopathy identify patients with end stage heart disease but not Table 2 Echo and ECG data of the relatives Ž adult population. a A P U P H P relatives relatives relatives Cases Echo criteria LVEDD 63 8 P P P LVESD P P P LVEF P P P FS 19 6 P NS 36 6 P ECG and VA Holter ECG criteria Ž European criteria. SVA LBBB Other minor ECG LAE findings PR 200 ms QRS 120 ms RBBB Sokolow 35 mm ST-T wave Abnormality a Abbre iations: A, affected; U, unknown; H, healthy; LVEDD, left ventricular end diastolic diameter; LVESD, left ventricular end systolic diameter; LVEF, left ventricular ejection fraction; FS, fractional shortening; VA, ventricular arrhythmias; SVA, supraventricular arrhythmias; LBBB, left bundle branch block; LAE, left atrial enlargement; RBBB, right bundle branch block. Values are mean S.D. P; U vs. A values are mean S.D. P; H vs. U values are mean S.D. P; H vs. A values are mean S.D.
8 360 ( ) L. Mangin et al. European Journal of Heart Failure Fig. 4. Cumulative distributions of age-at-onset according to sex. Age at onset was significantly delayed in women as compared to men Žlog rank test: P those with early disease in which there may be less marked ventricular dilation or dysfunction 13. The new minor criteria 8 used in our study represent a proposal for the classification of unknown relatives that might be helpful for phenotype characterization. However, diagnostic criteria for preclinical forms are still matter of investigation and those criteria will have to be reassessed and refined in the future. In our families, subjects Ž 15%. were identified either as affected Ž 8%., or unknown Ž 7%. with the combined minor Echo ECG criteria. Identification of a group of subjects with an unknown clinical status is interesting: the minor abnormalities found in this subgroup may be early markers of the disease 5,13 or phenocopies, i.e a phenotype of dilated cardiomyopathy due to a non-genetic cause. Furthermore, the most common abnormality in the unknown group was isolated dilation, whereas no difference in EF or FS was found between this group and the group of healthy relatives. It is not known whether these individuals are potential carriers of the disease since the genetic status was not available. However, it has been suggested that isolated left ventricular enlargement may be an early marker of the disease in first degree relatives of probands with definite DCM 13. Until the disease genes have been identified, the answer to this question can come only from follow-up studies. When minor ECG criteria alone were taken into account, 32% of affected relatives had ECG abnormalities. This low apparent sensitivity underlines the need of optimization of ECG criteria for future analysis. When other minor ECG findings were taken into account, the sensitivity increased Ž Table 2.. All those criteria will have to be reassessed with the genetic status as the reference criterion Mode of inheritance and penetrance We found that inheritance of the disease was autosomal dominant in most of our families, a finding in agreement with previous reports 4,6,7,14. Only one previous study to our knowledge studied the penetrance in FDC 14, but the methodology used was not detailed. Estimated penetrance in the French families was incomplete in adults and was significantly influenced by age and sex. However, we point out that our study has been carried out on a highly selected group of family because at least three members were known to be affected. Consequently estimated penetrance may be even lower than that found in our study. These findings may have important implications in the future for clinical practice and genetic counseling. Even when a subject has a normal cardiovascular examination, the risk of being genetically affected can not be excluded, especially before 40 years of age and in women. Furthermore, our results could help the molecular biologists to define a more accurate model of penetrance in linkage analysis for this disease. This might improve the statistical power of linkage analyses since high mortality and incomplete penetrance
9 ( ) L. Mangin et al. European Journal of Heart Failure give frequently rise to small nuclei of clinically affected and alive relatives per family. Acknowledgements We are indebted to the family members and their physicians, without whose participation this work could not have been done. This work was made possible by generous grants from Parke Davis, Association Française des Myopathies, European Human and Capital Mobility Project on Familial Dilated Cardiomyopathy Ž ERBCHRXCT , Delegation `a la recherche clinique Assistance publique-hopitaux ˆ de Paris Ž EMUL et PHRC and Institut Electricité Sante. References 1 Task Force on the Definition and Classification of Cardiomyopathies. Circulation 1996;93: Codd MB, Sugrue DD, Gersh BJ et al. Epidemiology of idiopathic dilated and hypertrophic cardiomyopathy. Circulation 1989;80: Manolio TA, Baughman KL, Rodeheffer R et al. Prevalence and etiology of idiopathic dilated cardiomyopathy. Am J Cardiol 1992;69: Keeling PJ, Gang Y, Smith G et al. Familial dilated cardiomyopathy in the United Kingdom. Br Heart J 1995; 73: Michels VV, Moll PP, Miller FA et al. The frequency of familial dilated cardiomyopathy in a series of patients with idiopathic dilated cardiomyopathy. N Engl J Med 1992; 326: Mestroni L, Miani D, Di Lenarda A et al. Clinical and pathologic study of familial dilated cardiomyopathy. Am J Cardiol 1990;65: Zachara E, Caforio A, Carboni GP et al. Familial aggregation of idiopathic dilated cardiomyopathy: clinical features and pedigree analysis in 14 families. Br Heart J 1993;69: Mestroni L, Maisch B, Mc Kenna WJ et al. Guidelines for the study of familial dilated cardiomyopathies. Eur Heart J 1999;20: Teichholz LE, Kreulent T, Herman MV et al. Problems in echocardiographic volume determinations: echocardiographic-angiographic correlation in the presence or absence of asynergy. Am J Cardiol 1976;37: Henry WL, Gardin JM, Ware JH. Echocardiographic measurements in normal subjects from infancy to old age. Circulation 1980;62Ž. 5 : Cupples LA, Terrin NC, Myers RH et al. Genet Epidemiol 1989;6: Charron P, Dubourg O, Desnos M et al. Diagnostic value of electrocardiography and echocardiography for familial hypertrophic cardiomyopathy in a genotyped adult population. Circulation 1997;96: Kamran BM, Goldman JH, Caforio A et al. Familial dilated cardiomyopathy: cardiac abnormalities are common in asymptomatic relatives and may represent early disease. J Am Coll Cardiol 1998;31: Mestroni L, Krajinovic M, Severini GM et al. Familial dilated cardiomyopathy. Br Heart J 1994;72:S35 S41.
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