Advertisement
Canadian Journal of Cardiology

Cancer Risk in Congenital Heart Disease—What Is the Evidence?

Published:October 09, 2019DOI:https://doi.org/10.1016/j.cjca.2019.09.023

      Abstract

      As life expectancy in patients with congenital heart disease (CHD) has improved, the risk for developing noncardiac morbidities is increasing in adult patients with CHD (ACHD). Among these noncardiac complications, malignancies significantly contribute to the disease burden of ACHD patients. Epidemiologic studies of cancer risk in CHD patients are challenging because they require large numbers of patients, extended follow-up, detailed and validated clinical data, and appropriate reference populations. However, several observational studies suggest that cancer risks are significantly elevated in patients with CHD compared with the general population. CHD and cancer share genetic and environmental risk factors. An association with exposure to low-dose ionizing radiation secondary to medical therapeutic or diagnostic procedures has been reported. Patients with Down syndrome, as well as, to a lesser extent, deletion of 22q11.2 and renin-angiotensin system pathologies, may manifest both CHD and a predisposition to cancer. Such observations suggest that carcinogenesis and CHD may share a common basis in some cases. Finally, specific conditions, such as Fontan circulation and cyanotic CHD, may lead to multisystem consequences and subsequently to cancer. Nonetheless, there is currently no clear consensus regarding appropriate screening for cancer and surveillance modalities in CHD patients. Physicians caring for patients with CHD should be aware of this potential predisposition and meet screening recommendations for the general population fastidiously. An interdisciplinary and global approach is required to bridge the knowledge gap in this field.

      Résumé

      Comme l’espérance de vie des patients atteints d’une cardiopathie congénitale augmente, le risque d’apparition de maladies non cardiaques est aussi en hausse chez les adultes qui sont atteints de ce type de cardiopathie. Parmi les complications non cardiaques, les affections malignes contribuent fortement au fardeau de la maladie dans cette population. La réalisation d’études épidémiologies sur le risque de cancer chez les patients atteints d’une cardiopathie congénitale présente des défis, car de telles études exigent un grand nombre de sujets qu’il faut suivre sur une longue période, des données cliniques détaillées et validées et des populations de référence appropriées. Malgré tout, plusieurs études observationnelles semblent indiquer que le risque de cancer est considérablement élevé chez les patients atteints d’une cardiopathie congénitale comparativement à la population générale. De fait, les facteurs de risque génétiques et environnementaux sont les mêmes pour la cardiopathie congénitale et pour le cancer. Une association avec l’exposition à de faibles doses de rayonnements ionisants secondaire aux démarches thérapeutiques ou diagnostiques a été rapportée. Les patients atteints du syndrome de Down ainsi que, dans une moindre mesure, ceux qui présentent une délétion 22q11.2 ou dont le système rénine-angiotensine est atteint, sont susceptibles d’avoir à la fois une cardiopathie congénitale et une prédisposition au cancer. De telles observations semblent indiquer que la carcinogenèse et la cardiopathie congénitale pourraient dans certains cas avoir des causes communes. Enfin, certaines conditions, comme la présence d’un circuit de Fontan et une cardiopathie congénitale cyanogène, pourraient avoir des effets sur plusieurs organes et finir par provoquer l’apparition d’un cancer. Il n’en demeure pas moins qu’il n’existe à l’heure actuelle aucun consensus clair quant aux stratégies appropriées de dépistage du cancer et aux modalités de surveillance des patients atteints de cardiopathie congénitale. Les médecins qui traitent des patients atteints de cardiopathie congénitale doivent être au fait de cette prédisposition potentielle et suivre à la lettre les recommandations en matière de dépistage s’appliquant à la population générale. Une approche interdisciplinaire et globale s’impose afin de combler les lacunes des connaissances dans ce domaine.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Canadian Journal of Cardiology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Marelli A.J.
        • Ionescu-Ittu R.
        • Mackie A.S.
        • et al.
        Lifetime prevalence of congenital heart disease in the general population from 2000 to 2010.
        Circulation. 2014; 130: 749-756
        • Marelli A.J.
        • Mackie A.S.
        • Ionescu-Ittu R.
        • Rahme E.
        • Pilote L.
        Congenital heart disease in the general population: changing prevalence and age distribution.
        Circulation. 2007; 115: 163-172
        • Mandalenakis Z.
        • Rosengren A.
        • Skoglund K.
        • et al.
        Survivorship in children and young adults with congenital heart disease in Sweden.
        JAMA Intern Med. 2017; 177: 224-230
        • Khairy P.
        • Ionescu-Ittu R.
        • Mackie A.S.
        • et al.
        Changing mortality in congenital heart disease.
        J Am Coll Cardiol. 2010; 56: 1149-1157
        • Afilalo J.
        • Therrien J.
        • Pilote L.
        • et al.
        Geriatric congenital heart disease: burden of disease and predictors of mortality.
        J Am Coll Cardiol. 2011; 58: 1509-1515
        • Cohen S.
        • Liu A.
        • Gurvitz M.
        • et al.
        Exposure to low-dose ionizing radiation from cardiac procedures and malignancy risk in adults with congenital heart disease.
        Circulation. 2018; 137: 1334-1345
        • Gurvitz M.
        • Ionescu-Ittu R.
        • Guo L.
        • et al.
        Prevalence of cancer in adults with congenital heart disease compared with the general population.
        Am J Cardiol. 2016; 118: 1742-1750
        • Carozza S.E.
        • Langlois P.H.
        • Miller E.A.
        • Canfield M.
        Are children with birth defects at higher risk of childhood cancers?.
        Am J Epidemiol. 2012; 175: 1217-1224
        • Bjorge T.
        • Cnattingius S.
        • Lie R.T.
        • Tretli S.
        • Engeland A.
        Cancer risk in children with birth defects and in their families: a population based cohort study of 5.2 million children from Norway and Sweden.
        Cancer Epidemiol Biomarkers Prev. 2008; 17: 500-506
        • Sun Y.
        • Overvad K.
        • Olsen J.
        Cancer risks in children with congenital malformations in the nervous and circulatory system-A population based cohort study.
        Cancer Epidemiol. 2014; 38: 393-400
        • Botto L.D.
        • Flood T.
        • Little J.
        • et al.
        Cancer risk in children and adolescents with birth defects: a population-based cohort study.
        PLoS One. 2013; 8e69077
        • Lee Y.S.
        • Chen Y.T.
        • Jeng M.J.
        • et al.
        The risk of cancer in patients with congenital heart disease: a nationwide population-based cohort study in taiwan.
        PLoS One. 2015; 10e0116844
        • Diller G.P.
        • Kempny A.
        • Alonso-Gonzalez R.
        • et al.
        Survival prospects and circumstances of death in contemporary adult congenital heart disease patients under follow-up at a large tertiary centre.
        Circulation. 2015; 132: 2118-2125
        • Raissadati A.
        • Nieminen H.
        • Haukka J.
        • Sairanen H.
        • Jokinen E.
        Late Causes of death after pediatric cardiac surgery: a 60-year population-based study.
        J Am Coll Cardiol. 2016; 68: 487-498
        • Brenner D.J.
        • Doll R.
        • Goodhead D.T.
        • et al.
        Cancer risks attributable to low doses of ionizing radiation: assessing what we really know.
        Proc Natl Acad Sci U S A. 2003; 100: 13761-13766
        • Lawler P.R.
        • Afilalo J.
        • Eisenberg M.J.
        • Pilote L.
        Exposure to low-dose ionizing radiation from cardiac imaging among patients with myocardial infarction.
        Am J Cardiol. 2012; 109: 31-35
        • Beausejour Ladouceur V.
        • Lawler P.R.
        • Gurvitz M.
        • et al.
        Exposure to low-dose ionizing radiation from cardiac procedures in patients with congenital heart disease: 15-year data from a population-based longitudinal cohort.
        Circulation. 2016; 133: 12-20
        • Ait-Ali L.
        • Andreassi M.G.
        • Foffa I.
        • et al.
        Cumulative patient effective dose and acute radiation-induced chromosomal DNA damage in children with congenital heart disease.
        Heart. 2010; 96: 269-274
        • Johnson J.N.
        • Hornik C.P.
        • Li J.S.
        • et al.
        Cumulative radiation exposure and cancer risk estimation in children with heart disease.
        Circulation. 2014; 130: 161-167
        • Glatz A.C.
        • Purrington K.S.
        • Klinger A.
        • et al.
        Cumulative exposure to medical radiation for children requiring surgery for congenital heart disease.
        J Pediatr. 2014; 164: 789-94 e710
        • Hoffmann A.
        • Engelfriet P.
        • Mulder B.
        Radiation exposure during follow-up of adults with congenital heart disease.
        Int J Cardiol. 2007; 118: 151-153
        • Kaul P.
        • Medvedev S.
        • Hohmann S.F.
        • et al.
        Ionizing radiation exposure to patients admitted with acute myocardial infarction in the United States.
        Circulation. 2010; 122: 2160-2169
        • Hausleiter J.
        • Meyer T.
        • Hermann F.
        • et al.
        Estimated radiation dose associated with cardiac CT angiography.
        JAMA. 2009; 301: 500-507
        • Bacher K.
        • Bogaert E.
        • Lapere R.
        • de Wolf D.
        • Thierens H.
        Patient-specific dose and radiation risk estimation in pediatric cardiac catheterization.
        Circulation. 2005; 111: 83-89
        • Beausejour Ladouceur V.
        • Lawler P.R.
        Estimating cancer risk from invasive cardiac procedures in children.
        Heart. 2017; 103: 329-330
        • Beels L.
        • Bacher K.
        • de Wolf D.
        • Werbrouck J.
        • Thierens H.
        Gamma-H2AX foci as a biomarker for patient X-ray exposure in pediatric cardiac catheterization: are we underestimating radiation risks?.
        Circulation. 2009; 120: 1903-1909
        • Vecoli C.
        • Borghini A.
        • Foffa I.
        • Ait-Ali L.
        • Picano E.
        • Andreassi M.G.
        Leukocyte telomere shortening in grown-up patients with congenital heart disease.
        Int J Cardiol. 2016; 204: 17-22
        • Pierce D.A.
        • Preston D.L.
        Radiation-related cancer risks at low doses among atomic bomb survivors.
        Radiat Res. 2000; 154: 178-186
        • Preston D.L.
        • Ron E.
        • Tokuoka S.
        • et al.
        Solid cancer incidence in atomic bomb survivors: 1958-1998.
        Radiat Res. 2007; 168: 1-64
        • Preston D.L.
        • Shimizu Y.
        • Pierce D.A.
        • Suyama A.
        • Mabuchi K.
        Studies of mortality of atomic bomb survivors. Report 13: Solid cancer and noncancer disease mortality: 1950-1997.
        Radiat Res. 2003; 160: 381-407
        • Eisenberg M.J.
        • Afilalo J.
        • Lawler P.R.
        • Abrahamowicz M.
        • Richard H.
        • Pilote L.
        Cancer risk related to low-dose ionizing radiation from cardiac imaging in patients after acute myocardial infarction.
        CMAJ. 2011; 183: 430-436
        • Mathews J.D.
        • Forsythe A.V.
        • Brady Z.
        • et al.
        Cancer risk in 680,000 people exposed to computed tomography scans in childhood or adolescence: data linkage study of 11 million Australians.
        BMJ. 2013; 346: f2360
        • Pearce M.S.
        • Salotti J.A.
        • Little M.P.
        • et al.
        Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study.
        Lancet. 2012; 380: 499-505
        • Journy N.
        • Dreuil S.
        • Rage E.
        • et al.
        Projected future cancer risks in children treated with fluoroscopy-guided cardiac catheterization procedures.
        Circ Cardiovasc Interv. 2018; 11e006765
        • Harbron R.W.
        • Chapple C.L.
        • O’Sullivan J.J.
        • et al.
        Survival adjusted cancer risks attributable to radiation exposure from cardiac catheterisations in children.
        Heart. 2017; 103: 341-346
        • McLaughlin J.R.
        • Kreiger N.
        • Sloan M.P.
        • et al.
        An historical cohort study of cardiac catheterization during childhood and the risk of cancer.
        International journal of epidemiology. 1993; 22: 584-591
        • Modan B.
        • Keinan L.
        • Blumstein T.
        • Sadetzki S.
        Cancer following cardiac catheterization in childhood.
        Int J Epidemiol. 2000; 29: 424-428
        • Committee to Assess Health Risks from Exposure to Low Levels of Ionizing Radiation, Board on Radiation Effects Research, Division on Earth and Life Studies, National Research Council of the National Academies
        Health Risks from Exposure to Low Levels of Ionizing Radiation: BEIR VII Phase 2.
        National Academies Press, Washington, DC2006
        • Einstein A.J.
        • Henzlova M.J.
        • Rajagopalan S.
        Estimating risk of cancer associated with radiation exposure from 64-slice computed tomography coronary angiography.
        JAMA. 2007; 298: 317-323
        • Lawler P.R.
        • Afilalo J.
        • Eisenberg M.J.
        • Pilote L.
        Comparison of cancer risk associated with low-dose ionizing radiation from cardiac imaging and therapeutic procedures after acute myocardial infarction in women versus men.
        Am J Cardiol. 2013; 112: 1545-1550
        • Yang Q.
        • Rasmussen S.A.
        • Friedman J.M.
        Mortality associated with Down’s syndrome in the USA from 1983 to 1997: a population-based study.
        Lancet. 2002; 359: 1019-1025
        • Patja K.
        • Pukkala E.
        • Sund R.
        • Iivanainen M.
        • Kaski M.
        Cancer incidence of persons with Down syndrome in Finland: a population-based study.
        Int J Cancer. 2006; 118: 1769-1772
        • Hill D.A.
        • Gridley G.
        • Cnattingius S.
        • et al.
        Mortality and cancer incidence among individuals with Down syndrome.
        Arch Intern Med. 2003; 163: 705-711
        • Hasle H.
        • Friedman J.M.
        • Olsen J.H.
        • Rasmussen S.A.
        Low risk of solid tumors in persons with Down syndrome.
        Genet Med. 2016; 18: 1151-1157
        • Hasle H.
        • Clemmensen I.H.
        • Mikkelsen M.
        Risks of leukaemia and solid tumours in individuals with Down’s syndrome.
        Lancet. 2000; 355: 165-169
        • Bosse K.R.
        • Shukla A.R.
        • Pawel B.
        • et al.
        Malignant rhabdoid tumor of the bladder and ganglioglioma in a 14 year-old male with a germline 22q11.2 deletion.
        Cancer Genet. 2014; 207: 415-419
        • Chakrapani A.L.
        • White C.R.
        • Korcheva V.
        • et al.
        Congenital extrarenal malignant rhabdoid tumor in an infant with distal 22q11.2 deletion syndrome: the importance of SMARCB1.
        Am J Dermatopathol. 2012; 34: e77-e80
        • Finch P.T.
        • Pivnick E.K.
        • Furman W.
        • Odom C.C.
        Wilms tumor in a patient with 22q11.2 microdeletion.
        Am J Med Genet A. 2011; 155A: 1162-1164
        • Forest F.
        • David A.
        • Arrufat S.
        • et al.
        Conventional chondrosarcoma in a survivor of rhabdoid tumor: enlarging the spectrum of tumors associated with SMARCB1 germline mutations.
        Am J Surg Pathol. 2012; 36: 1892-1896
        • Itoh S.
        • Ohno T.
        • Kakizaki S.
        • Ichinohasama R.
        Epstein-Barr virus–positive T-cell lymphoma cells having chromosome 22q11.2 deletion: an autopsy report of DiGeorge syndrome.
        Hum Pathol. 2011; 42: 2037-2041
        • McDonald-McGinn D.M.
        • Reilly A.
        • Wallgren-Pettersson C.
        • et al.
        Malignancy in chromosome 22q11.2 deletion syndrome (DiGeorge syndrome/velocardiofacial syndrome).
        Am J Med Genet A. 2006; 140: 906-909
        • Murray J.C.
        • Donahue D.J.
        • Malik S.I.
        • et al.
        Temporal lobe pleomorphic xanthoastrocytoma and acquired BRAF mutation in an adolescent with the constitutional 22q11.2 deletion syndrome.
        J Neurooncol. 2011; 102: 509-514
        • Mussai F.J.
        • Cunningham L.C.
        • Rezvani G.
        • et al.
        Hypocalcemia in a patient with osteosarcoma and 22q11.2 deletion syndrome.
        J Pediatr Hematol Oncol. 2008; 30: 612-617
        • Pongpruttipan T.
        • Cook J.R.
        • Reyes-Mugica M.
        • Spahr J.E.
        • Swerdlow S.H.
        Pulmonary extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue associated with granulomatous inflammation in a child with chromosome 22q11.2 deletion syndrome (DiGeorge syndrome).
        J Pediatr. 2012; 161: 954-958
        • Rauen K.A.
        The RASopathies.
        Annu Rev Genomics Hum Genet. 2013; 14: 355-369
        • Jongmans M.C.
        • van der Burgt I.
        • Hoogerbrugge P.M.
        • et al.
        Cancer risk in patients with Noonan syndrome carrying a PTPN11 mutation.
        Eur J Hum Genet. 2011; 19: 870-874
        • Smpokou P.
        • Zand D.J.
        • Rosenbaum K.N.
        • Summar M.L.
        Malignancy in Noonan syndrome and related disorders.
        Clin Genet. 2015; 88: 516-522
        • Kratz C.P.
        • Franke L.
        • Peters H.
        • et al.
        Cancer spectrum and frequency among children with Noonan, Costello, and cardio-facio-cutaneous syndromes.
        Br J Cancer. 2015; 112: 1392-1397
        • Schneider M.
        • Chandler K.
        • Tischkowitz M.
        • Meyer S.
        Fanconi anaemia: genetics, molecular biology, and cancer—implications for clinical management in children and adults.
        Clin Genet. 2015; 88: 13-24
        • Alter B.P.
        • Rosenberg P.S.
        VACTERL-H association and Fanconi anemia.
        Mol Syndromol. 2013; 4: 87-93
        • Asrani S.K.
        • Asrani N.S.
        • Freese D.K.
        • et al.
        Congenital heart disease and the liver.
        Hepatology. 2012; 56: 1160-1169
        • Wang A.
        • Book W.M.
        • McConnell M.
        • et al.
        Prevalence of hepatitis C infection in adult patients who underwent congenital heart surgery prior to screening in 1992.
        Am J Cardiol. 2007; 100: 1307-1309
        • Schwartz M.C.
        • Sullivan L.
        • Cohen M.S.
        • et al.
        Hepatic pathology may develop before the Fontan operation in children with functional single ventricle: an autopsy study.
        J Thorac Cardiovasc Surg. 2012; 143: 904-909
        • Kiesewetter C.H.
        • Sheron N.
        • Vettukattill J.J.
        • et al.
        Hepatic changes in the failing Fontan circulation.
        Heart. 2007; 93: 579-584
        • Baek J.S.
        • Bae E.J.
        • Ko J.S.
        • et al.
        Late hepatic complications after Fontan operation; noninvasive markers of hepatic fibrosis and risk factors.
        Heart. 2010; 96: 1750-1755
        • Asrani S.K.
        • Warnes C.A.
        • Kamath P.S.
        Hepatocellular carcinoma after the Fontan procedure.
        N Engl J Med. 2013; 368: 1756-1757
        • Josephus Jitta D.
        • Wagenaar L.J.
        • Mulder B.J.
        • Guichelaar M.
        • Bouman D.
        • van Melle J.P.
        Three cases of hepatocellular carcinoma in Fontan patients: review of the literature and suggestions for hepatic screening.
        Int J Cardiol. 2016; 206: 21-26
        • Egbe A.C.
        • Poterucha J.T.
        • Warnes C.A.
        • et al.
        Hepatocellular carcinoma after Fontan operation.
        Circulation. 2018; 138: 746-748
        • Lenders J.W.
        • Duh Q.Y.
        • Eisenhofer G.
        • et al.
        Pheochromocytoma and paraganglioma: an endocrine society clinical practice guideline.
        J Clin Endocrinol Metab. 2014; 99: 1915-1942
        • Folger Jr., G.M.
        • Roberts W.C.
        • Mehrizi A.
        • et al.
        Cyanotic malformations of the heart with pheochromocytoma. A report of five cases.
        Circulation. 1964; 29: 750-757
        • Adunuri N.
        • Mrkobrada M.
        Not so incidental: pheochromocytoma in an adult with unrepaired cyanotic heart disease.
        Eur J Case Rep Intern Med. 2018; 5000959
        • Aresta C.
        • Butera G.
        • Tufano A.
        • et al.
        Pheochromocytoma in congenital cyanotic heart disease.
        Case Rep Endocrinol. 2018; 2018: 2091257
        • Song M.K.
        • Kim G.B.
        • Bae E.J.
        • et al.
        Pheochromocytoma and paraganglioma in Fontan patients: more common than expected.
        Congenit Heart Dis. 2018; 13: 608-616
        • Kita T.
        • Imamura T.
        • Date H.
        • et al.
        Two cases of pheochromocytoma associated with tetralogy of Fallot.
        Hypertens Res. 2003; 26: 433-437
        • Opotowsky A.R.
        • Moko L.E.
        • Ginns J.
        • et al.
        Pheochromocytoma and paraganglioma in cyanotic congenital heart disease.
        J Clin Endocrinol Metab. 2015; 100: 1325-1334
        • Bhatt A.B.
        • Foster E.
        • Kuehl K.
        • et al.
        Congenital heart disease in the older adult: a scientific statement from the American Heart Association.
        Circulation. 2015; 131: 1884-1931
        • Christman M.P.
        • Castro-Zarraga M.
        • Defaria Yeh D.
        • Liberthson R.R.
        • Bhatt A.B.
        Adequacy of cancer screening in adult women with congenital heart disease.
        ISRN Cardiol. 2013; 2013: 827696
        • Hill K.D.
        • Frush D.P.
        • Han B.K.
        • et al.
        Radiation safety in children with congenital and acquired heart disease: a scientific position statement on multimodality dose optimization from the Image Gently Alliance.
        JACC Cardiovasc Imaging. 2017; 10: 797-818
        • Martin G.R.
        • Beekman R.H.
        • Ing F.F.
        • et al.
        The IMPACT registry: Improving Pediatric and Adult Congenital Treatments.
        Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu. 2010; 13: 20-25
        • Martin G.R.
        • Anderson J.B.
        • Vincent R.N.
        IMPACT Registry and National Pediatric Cardiology Quality Improvement Collaborative: contributions to quality in congenital heart disease.
        World J Pediatr Congenit Heart Surg. 2019; 10: 72-80
        • Lang N.N.
        • Walker N.L.
        Adult congenital heart disease and radiation exposure: the malignant price of cardiac care.
        Circulation. 2018; 137: 1346-1348
        • Baumgartner H.
        • Bonhoeffer P.
        • de Groot N.M.
        • et al.
        ESC guidelines for the management of grown-up congenital heart disease (new version 2010).
        Eur Heart J. 2010; 31: 2915-2957
        • Stout K.K.
        • Daniels C.J.
        • Aboulhosn J.A.
        • et al.
        2018 AHA/ACC guideline for the management of adults with congenital heart disease: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines.
        J Am Coll Cardiol. 2019; 73: e81-e192
        • Silversides C.K.
        • Salehian O.
        • Oechslin E.
        • et al.
        Canadian Cardiovascular Society 2009 consensus conference on the management of adults with congenital heart disease: complex congenital cardiac lesions.
        Can J Cardiol. 2010; 26: e98-e117
        • Burak K.W.
        • Sherman M.
        Hepatocellular carcinoma: consensus, controversies and future directions. A report from the Canadian Association for the Study of the Liver hepatocellular carcinoma meeting.
        Can J Gastroenterol Hepatol. 2015; 29: 178-184
        • Hilscher M.B.
        • Johnson J.N.
        • Cetta F.
        • et al.
        Surveillance for liver complications after the Fontan procedure.
        Congenit Heart Dis. 2017; 12: 124-132
        • Mazzarelli C.
        • Cannon M.D.
        • Hudson M.
        • et al.
        Hepatocellular carcinoma as a complication of vascular disease of the liver after Fontan procedure.
        Hepatology. 2019; 69: 911-913
        • Villani A.
        • Greer M.C.
        • Kalish J.M.
        • et al.
        Recommendations for cancer surveillance in individuals with RASopathies and other rare genetic conditions with increased cancer risk.
        Clin Cancer Res. 2017; 23: e83-e90
        • Cohen S.
        • Marelli A.
        Increasing survival in patients with congenital heart disease—a glass half full or half empty?.
        JAMA Intern Med. 2017; 177: 1690-1691
        • Klarenbach S.
        • Sims-Jones N.
        • Lewin G.
        • et al.
        Recommendations on screening for breast cancer in women aged 40-74 years who are not at increased risk for breast cancer.
        CMAJ. 2018; 190: E1441-E1451
        • Dickinson J.
        • Tsakonas E.
        • Conner Gorber S.
        • et al.
        Recommendations on screening for cervical cancer.
        CMAJ. 2013; 185: 35-45
        • Canadian Task Force on Preventive Health Care
        Recommendations on screening for colorectal cancer in primary care.
        CMAJ. 2016; 188: 340-348
        • Bell N.
        • Connor Gorber S.
        • Shane A.
        • et al.
        Recommendations on screening for prostate cancer with the prostate-specific antigen test.
        CMAJ. 2014; 186: 1225-1234
        • Canadian Task Force on Preventive Health Care
        Recommendations on screening for lung cancer.
        CMAJ. 2016; 188: 425-432
        • Lui G.K.
        • Saidi A.
        • Bhatt A.B.
        • et al.
        Diagnosis and management of noncardiac complications in adults with congenital heart disease: a scientific statement from the American Heart Association.
        Circulation. 2017; 136: e348-e392