University of Groningen. Inherited Cardiomyopathies Spaendonck-Zwarts, Karin Yvon van
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1 University of Groningen Inherited Cardiomyopathies Spaendonck-Zwarts, Karin Yvon van IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2014 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Spaendonck-Zwarts, K. Y. V. (2014). Inherited Cardiomyopathies: Genetics and Gene-Environment Interactions Groningen: s.n. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date:
2 Part IIB Gene-Environment Interactions in Inherited Cardiomyopathies: Anthracyclinics Spaendonck.indd :00
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4 9 Familial dilated cardiomyopathy: another risk factor for anthracyclineinduced cardiotoxicity? Maarten P. van den Berg Karin Y. van Spaendonck-Zwarts Dirk J. van Veldhuisen Jourik A. Gietema Aleida Postma J. Peter van Tintelen European Journal of Heart Failure 2010; 12: Spaendonck.indd :00
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6 Chapter 9 BACKGROUND Since their introduction in the late 1960s, anthracyclines such as daunorubicin and doxorubicin have been successfully used in the treatment of a wide variety of tumours. However, their use is limited by the occurrence of cardiotoxicity, which may result in left ventricular (LV) dysfunction/dilated cardiomyopathy (DCM) and eventually heart failure. 1,2 Several risk factors have been identified for anthracycline-induced cardiotoxicity: the most important one is the total cumulative dose of anthracycline given, with a cumulative dose of daunorubicin and doxorubicin up to 450 mg/m 2 being considered relatively safe. 1,2 However, in some patients, LV dysfunction/dcm develops after anthracycline treatment which is not fully explicable in terms of the established risk factors, suggesting that other factors, probably including genetic ones, play a role. AIMS Here, we report two patients who were treated for cancer and who later developed DCM; a genetic predisposition for DCM is believed to have played a role. METHODS Among other patients with possible hereditary cardiac disorders, we see at the cardiogenetics outpatient clinic of the University Medical Centre Groningen patients with idiopathic DCM. As part of routine procedures, the patients clinical characteristics are collected, pedigrees are constructed, full family histories are obtained, and family members at risk are invited for pre-symptomatic ( cascade ) screening using family letters. 3,4 Dilated cardiomyopathy is diagnosed if there is both a reduced systolic function (ejection fraction <0.45) and dilation of the LV (end-diastolic dimension >117% of the predicted value corrected for body surface area and age). If only one of these criteria is fulfilled, the case is labelled mild DCM. In addition, identifiable causes like severe hypertension, coronary artery disease, and systemic diseases should have been excluded. 5,6 Familial DCM (fdcm) is diagnosed if two or more affected individuals are present in a family or if the patient with DCM has a first-degree relative who died suddenly before the age of 35 years. 6 All patients are asked to give permission for their clinical data to be used for scientific research. Genomic DNA is isolated from blood samples obtained from the index patients, using DNA samples from 300 ethnically matched control alleles. As part of our routine clinical care, DNA analysis is performed for the following major DCM-related genes: lamin A/C (LMNA), cardiac troponin T (TNNT2), and β-myosin heavy chain (MYH7), using established techniques Spaendonck.indd :00
7 RESULTS Patient A had had acute lymphoid leukaemia at the age of 9 years for which he received several non-cardiotoxic agents. At the age of 12 years, he had a relapse which was treated with daunorubicin (cumulative dose 175 mg/m 2 ) and allogenic stem cell transplantation (including total body radiation (12 Gy)). At the age of 17 years, he presented with reduced exercise tolerance and LV dysfunction, which at that time was attributed to the earlier anti-cancer treatment. He is now 30 years old and he is in New York Heart Association functional class II. Left ventricular ejection fraction and LV end-diastolic dimension are at present 0.40 and 28 mm/m 2, respectively. As part of a research project on the late effects of childhood cancer treatment, his 24-year-old brother recently participated as a healthy sibling control and was found to have an LV ejection fraction of 0.42 and an LV end-diastolic dimension of 27 mm/m 2. After this unexpected finding, the attending oncologist considered the possibility of fdcm and referred the two brothers to our cardiogenetics outpatient clinic for further analysis. The family history revealed that their father had been diagnosed with heart failure due to idiopathic DCM in a regional hospital 3 years earlier at the age of 56 years. Since both Patient A s brother and father were affected with idiopathic (mild) DCM, fdcm was considered in this family (Figure 1A). However, DNA analysis of LMNA, MYH7, and TNNT2 did not reveal an underlying mutation in this family. Patient B had had a neuroblastoma at the age of 2 years for which he had been treated with cyclophosphamide and doxorubicin (cumulative dose 420 mg/m 2 ). At the age of 16 years, he presented with heart failure due to severe LV dysfunction, which at that time was attributed to the chemotherapy. He is now 29 years old and although he has relatively mild symptoms, the LV function is severely depressed (ejection fraction 0.25) and the LV is dilated (LV end-diastolic dimension 31 mm/m 2 ). At a recent routine follow-up, the patient told the attending oncologist that his father had just been diagnosed with heart failure in a regional hospital. The possibility of fdcm was considered and the patient was referred to our cardiogenetics outpatient clinic for further analysis. The review of the available cardiac data from Patient B s father indicated that he had been diagnosed with heart failure due to idiopathic DCM at the age of 57 years. Two family members, Patient B s brother and a paternal uncle, responded to the family letters and were investigated. The uncle was 66 years old and asymptomatic but echocardiography revealed mild DCM. The brother was 24 years old, asymptomatic but echocardiography also revealed mild DCM. Since Patient B s father, uncle, and brother were affected with (mild) idiopathic DCM, fdcm was also considered likely in Family B (Figure 1B). Two mutations in MYH7 were identified in Patient B and his affected family members: c.1633g > A (p.asp545asn) in exon 16 and c.2863g > A (p.asp955asn) in exon 23. Both mutations have been published previously 8 and segregation analysis demonstrated that these two MYH7 mutations were on the same allele (in cis) that also segregated with the disease in this family. 206 Spaendonck.indd :00
8 Chapter 9 Figure 1: Pedigree of the family of Patient A (left panel) and Patient B (right panel). Square and round symbols depict male and female, respectively. Filled symbols depict family members with (mild) dilated cardiomyopathy. Arrows indicate the cancer patients. CONCLUSION Our two cases suggest the presence of a previously unrecognized risk factor for the development of anthracycline-induced cardiotoxicity, namely a genetic/familial predisposition for DCM. Patient A developed DCM at a young age, despite having received only a low dose of daunorubicin. 1,2,9 Even though other factors may have contributed to the anthracycline cardiotoxicity, in particular radiation therapy and young age, it remains difficult to accept that the anticancer treatment was solely responsible. Rather, it is conceivable that Patient A is a carrier of a yet unidentified mutation causing DCM in his family and that this contributed to the development of his DCM. In the case of Patient B, a proven carrier of DCM-causing mutations, it is also likely that his genetic predisposition for DCM contributed to its actual development. Our study not only provides new insight for the oncologist but also for the cardiogeneticist dealing with DCM patients and their families. fdcm is characterized by variable penetrance, 10 implying that even within a single family, proven disease-causing mutation carriers may live into senescence without showing any clinical signs of DCM, whereas other mutation carriers may experience the early onset of disease and progression to heart failure. Variable penetrance was also evident in our two families, the two fathers presenting with DCM at a later age than their sons. The phenomenon of variable penetrance suggests that in addition to the specific genetic 207 Spaendonck.indd :00
9 predisposition, other factors, including environmental ones, must also play a role in the pathogenesis of fdcm. Our two cases represent probable examples of an environmental factor, namely anti-cancer treatment with known cardiotoxic agents. Our study thus provides evidence for a gene environment interaction with regard to the development of DCM after anti-cancer treatment, with an environmental factor (cardiotoxic treatment) eliciting early-onset and/or severe DCM in the setting of a genetic predisposition for DCM. In terms of practicality, we recommend careful evaluation of the family history for fdcm before treating a cancer patient with cardiotoxic agents. And conversely, clinicians should be aware of the possibility that disproportionate LV dilatation and systolic dysfunction after chemotherapy may be a manifestation of fdcm. In conclusion, our study suggests that a family history of DCM is another risk factor for the development of anthracycline-induced cardiotoxicity. A way to further explore this concept would be to perform genetic research (investigation of family members and DNA analysis) in patients with disproportionate LV dilatation and systolic dysfunction after chemotherapy. Acknowledgements We thank Dr Jan Jongbloed for performing the DNA analyses and Jackie Senior for editing this paper. 208 Spaendonck.indd :00
10 Chapter 9 REFERENCES 1. Meinardi MT, van der Graaf WTA, van Veldhuisen DJ, Gietema JA, de Vries EGE, Sleijfer DTh. Detection of anthracycline-induced cardiotoxicity. Cancer Treat Rev 1999;25: Yeh ETH, Bickford CL. Cardiovascular complications of cancer therapy. Incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol 2009;53: van Tintelen JP, Hofstra R, Katerberg H, Rossenbacker T, Wiesfeld ACP, Marchie du Servaas G, Wilde AAM, van Langen IM, Nannenberg E, van der Kooi AJ, Kraak M, Buys CHCM, van Veldhuisen DJ, Vos Y, van den Berg MP. High yield of LMNA mutations in patients with dilated cardiomyopathy and/or conduction disease referred to cardiogenetics outpatients clinics. Am Heart J 2007;154: van der Roest WP, Pennings JM, Bakker M, van den Berg MP, van Tintelen JP. Family letters an effective way to inform relative about inherited cardiac disease. Am J Med Genet 2009;149A: Henry WL, Gardin JM, Ware JH. Echocardiographic measurements in normal subjects from infancy to old age. Circulation 1980;62: Mestroni L, Maisch B, McKenna WJ, Schwartz K, Charron P, Rocco C, Tesson F, Richter A, Wilke A, Komajda M. on behalf of the Collaborative Research Group of the European Human and Capital Mobility Project on Familial Dilated Cardiomyopathy. Eur Heart J 1999;20: van Tintelen JP, Tio RA, Kerstjens-Frederikse WS, Boven LG, van Berlo JH, Suurmeijer AJH, White S, den Dunnen JT, te Meerman GJ, van den Berg MP, van Veldhuisen DJ, Buys CHCM, Hofstra RWM, Pinto YM. Severe myocardial fibrosis caused by deletion of the 5 of the lamin A/C gene. J Am Coll Cardiol 2007;49: Hoedemaekers YM, Caliskan K, Majoor-Krakauer D, et al. Cardiac β-myosin heavy chain defects in two families with non-compaction cardiomyopathy: linking non-compaction to hypertrophic, restrictive, and dilated cardiomyopathies. Eur Heart J 2007;28: Brouwer CAJ, Gietema JA, van den Berg MP, et al. Low-dose anthracyclines childhood acute lymphoblastic leukemia (ALL): no cardiac deterioration more than 20 years post-treatment. J Cancer Surviv 2007;1: Burkett EL, Hershberger RE. Clinical and genetic issues in familial dilated cardiomyopathy. J Am Coll Cardiol 2005;45: Spaendonck.indd :00
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