Familial Hypercholesterolemia: A Narrative Review on Diagnosis and Management Strategies for Children and Adolescents

References

• Kannel WB, Castelli WP, Gordon T, McNamara PM. Serum cholesterol, lipoproteins, and the risk of coronary heart disease. The Framingham study. Ann Intern Med. 1971;74(1):1–12. doi:10.7326/0003-4819-74-1-1
   PubMed Web of Science ®Google Scholar
• Friedman M. Pathogenesis of the spontaneous atherosclerotic plaque. A study on the A/Friedman M: pathogenesis of the spontaneous atherosclerotic plaque. A study on the cholesterol-fed rabbit. Arch Pathol. 1963;76:318–329.
   PubMedGoogle Scholar
• Tada H, Usui S, Sakata K, Takamura M, Kawashiri MA. Low-density lipoprotein cholesterol level cannot be too low: considerations from clinical trials, human genetics, and biology. J Atheroscler Thromb. 2020;27(6):489–498. doi:10.5551/jat.RV17040
   PubMed Web of Science ®Google Scholar
• Baigent C, Blackwell L, Emberson J, Cholesterol Treatment Trialists’ (CTT) Collaboration, et al.. Efficacy and safety of more intensive lowering of LDL cholesterol: a meta-analysis of data from 170,000 participants in 26 randomised trials. Lancet. 2010;376:1670–1681.
   PubMed Web of Science ®Google Scholar
• Cannon CP, Blazing MA, Giugliano RP, IMPROVE-IT Investigators, et al.. Ezetimibe added to statin therapy after acute coronary syndromes. N Engl J Med. 2015;372(25):2387–2397. doi:10.1056/NEJMoa1410489
   PubMed Web of Science ®Google Scholar
• Sabatine MS, Giugliano RP, Keech AC, et al. FOURIER steering committee and investigators. Evolocumab and clinical outcomes in patients with cardiovascular disease. N Engl J Med. 2017;376(18):1713–1722. doi:10.1056/NEJMoa1615664
   PubMed Web of Science ®Google Scholar
• Schwartz GG, Steg PG, Szarek M, ODYSSEY OUTCOMES Committees and Investigators, et al.. Alirocumab and cardiovascular outcomes after acute coronary syndrome. N Engl J Med. 2018;379(22):2097–2107. doi:10.1056/NEJMoa1801174
   PubMed Web of Science ®Google Scholar
• Mabuchi H. Half a century tales of familial hypercholesterolemia (FH) in Japan. J Atheroscler Thromb. 2017;24(3):189–207. doi:10.5551/jat.RV16008
   PubMed Web of Science ®Google Scholar
• Gidding SS, Champagne MA, de Ferranti SD, et al. American heart association atherosclerosis, hypertension, and obesity in young committee of council on cardiovascular disease in young, council on cardiovascular and stroke nursing, council on functional genomics and translational biology, and council on lifestyle and cardiometabolic health. The agenda for familial hypercholesterolemia: a scientific statement from the American heart association. Circulation. 2015;132(22):2167–2192. doi:10.1161/CIR.0000000000000297
   PubMed Web of Science ®Google Scholar
• Wiegman A, Gidding SS, Watts GF, et al. European atherosclerosis society consensus panel. Familial hypercholesterolaemia in children and adolescents: gaining decades of life by optimizing detection and treatment. Eur Heart J. 2015;36(36):2425–2437. doi:10.1093/eurheartj/ehv157
   PubMed Web of Science ®Google Scholar
• Luirink IK, Wiegman A, Kusters DM, et al. 20-Year follow-up of statins in children with familial hypercholesterolemia. N Engl J Med. 2019;381(16):1547–1556. doi:10.1056/NEJMoa1816454
   PubMed Web of Science ®Google Scholar
• Goldstein JL, Hobbs HH, Brown MS. Familial hypercholesterolemia. In: Scriver CR, Beaudet AL, Sly WS, Valle D, editors. The Metabolic and Molecular Bases of Inherited Disease. New York: McGraw-Hill; 2001:2863e913.
   Google Scholar
• Fagge CH. Xanthomatous disease of the skin. I. general xanthelasma of vitiligoides. Trans Pathol Soc. 1873;24:242–250.
   Google Scholar
• Thannhauser SJ, Magendantz H. The different clinical groups of xanthomatous diseases: a clinical physiological study of 22 cases. Ann Intern Med. 1938;11(9):1162. doi:10.7326/0003-4819-11-9-1662
   Google Scholar
• Brown MS, Goldstein JL. Familial hypercholesterolemia: defective binding of lipoproteins to cultured fibroblasts associated with impaired regulation of 3–hydroxy-3-methylglutaryl coenzyme A reductase activity. Proc Natl Acad Sci U S A. 1974;71(3):788–792. doi:10.1073/pnas.71.3.788
   PubMed Web of Science ®Google Scholar
• Innerarity TL, Weisgraber KH, Arnold KS, et al. Familial defective apolipoprotein B-100: low density lipoproteins with abnormal receptor binding. Proc Natl Acad Sci U S A. 1987;84(19):6919–6923. doi:10.1073/pnas.84.19.6919
   PubMed Web of Science ®Google Scholar
• Abifadel M, Varret M, Rabès JP, et al. Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat Genet. 2003;34(2):154–156. doi:10.1038/ng1161
   PubMed Web of Science ®Google Scholar
• Mabuchi H, Nohara A, Noguchi T, et al. Molecular genetic epidemiology of homozygous familial hypercholesterolemia in the Hokuriku district of Japan. Atherosclerosis. 2011;214(2):404–407. doi:10.1016/j.atherosclerosis.2010.11.005
   PubMed Web of Science ®Google Scholar
• Benn M, Watts GF, Tybjærg-Hansen A, Nordestgaard BG. Mutations causative of familial hypercholesterolaemia: screening of 98 098 individuals from the Copenhagen general population study estimated a prevalence of 1 in 217. Eur Heart J. 2016;37(17):1384–1394. doi:10.1093/eurheartj/ehw028
   PubMed Web of Science ®Google Scholar
• de Ferranti SD, Rodday AM, Mendelson MM, et al. Prevalence of familial hypercholesterolemia in the 1999 to 2012 United States national health and nutrition examination surveys (NHANES). Circulation. 2016;133(11):1067–1072. doi:10.1161/CIRCULATIONAHA.115.018791
   PubMed Web of Science ®Google Scholar
• Beheshti SO, Madsen CM, Varbo A, Nordestgaard BG. Worldwide prevalence of familial hypercholesterolemia: meta-analyses of 11 million subjects. J Am Coll Cardiol. 2020;75(20):2553–2566. doi:10.1016/j.jacc.2020.03.057
   PubMed Web of Science ®Google Scholar
• Tada H, Kawashiri MA, Nohara A, Inazu A, Mabuchi H, Yamagishi M. Impact of clinical signs and genetic diagnosis of familial hypercholesterolaemia on the prevalence of coronary artery disease in patients with severe hypercholesterolaemia. Eur Heart J. 2017;38(20):1573–1579. doi:10.1093/eurheartj/ehx004
   PubMed Web of Science ®Google Scholar
• Virani SS, Alonso A, Benjamin EJ, et al. American heart association council on epidemiology and prevention statistics committee and stroke statistics subcommittee. Heart disease and stroke statistics-2020 update: a report from the American heart association. Circulation. 2020;141:e139–e596.
   PubMed Web of Science ®Google Scholar
• Lozano P, Henrikson NB, Dunn J, et al. Lipid screening in childhood and adolescence for detection of familial hypercholesterolemia: evidence report and systematic review for the US preventive services task force. JAMA. 2016;316(6):645–655. doi:10.1001/jama.2016.6176
   PubMed Web of Science ®Google Scholar
• Groselj U, Kovac J, Sustar U, et al. Universal screening for familial hypercholesterolemia in children: the Slovenian model and literature review. Atherosclerosis. 2018;277:383–391. doi:10.1016/j.atherosclerosis.2018.06.858
   PubMed Web of Science ®Google Scholar
• Bell DA, Hooper AJ, Bender R, et al. Opportunistic screening for familial hypercholesterolaemia via a community laboratory. Ann Clin Biochem. 2012;49(6):534–537. doi:10.1258/acb.2012.012002
   PubMed Web of Science ®Google Scholar
• Scicali R, Di Pino A, Platania R, et al. Detecting familial hypercholesterolemia by serum lipid profile screening in a hospital setting: clinical, genetic and atherosclerotic burden profile. Nutr Metab Cardiovasc Dis. 2018;28(1):35–43. doi:10.1016/j.numecd.2017.07.003
   PubMed Web of Science ®Google Scholar
• Mirzaee S, Choy KW, Doery JCG, Zaman S, Cameron JD, Nasis A. The tertiary hospital laboratory; a novel avenue of opportunistic screening of familial hypercholesterolemia. Int J Cardiol Heart Vasc. 2019;23:100354. doi:10.1016/j.ijcha.2019.100354
   PubMed Web of Science ®Google Scholar
• Besseling J, Sjouke B, Kastelein JJ. Screening and treatment of familial hypercholesterolemia - lessons from the past and opportunities for the future (based on the anitschkow lecture 2014). Atherosclerosis. 2015;241(2):597–606. doi:10.1016/j.atherosclerosis.2015.06.011
   PubMed Web of Science ®Google Scholar
• Tada H, Okada H, Nomura A, et al. Prognostic impact of cascade screening for familial hypercholesterolemia on cardiovascular events. J Clin Lipidol. 2021. doi:10.1016/j.jacl.2020.12.012
   PubMed Web of Science ®Google Scholar
• Rodenburg J, Vissers MN, Wiegman A, et al. Statin treatment in children with familial hypercholesterolemia: the younger, the better. Circulation. 2007;116(6):664–668. doi:10.1161/CIRCULATIONAHA.106.671016
   PubMed Web of Science ®Google Scholar
• Wu X, Pang J, Wang X, et al. Reverse cascade screening for familial hypercholesterolemia in high-risk Chinese families. Clin Cardiol. 2017;40(11):1169–1173. doi:10.1002/clc.22809
   PubMed Web of Science ®Google Scholar
• Vinson A, Guerra L, Hamilton L, Wilson DP. Reverse cascade screening for familial hypercholesterolemia. J Pediatr Nurs. 2019;44:50–55. doi:10.1016/j.pedn.2018.09.011
   PubMed Web of Science ®Google Scholar
• Ibarretxe D, Rodríguez-Borjabad C, Feliu A, Bilbao JÁ, Masana L, Plana N. Detecting familial hypercholesterolemia earlier in life by actively searching for affected children: the DECOPIN project. Atherosclerosis. 2018;278:210–216. doi:10.1016/j.atherosclerosis.2018.09.039
   PubMed Web of Science ®Google Scholar
• Austin MA, Hutter CM, Zimmern RL, Humphries SE. Genetic causes of monogenic heterozygous familial hypercholesterolemia: a HuGE prevalence review. Am J Epidemiol. 2004;160(5):407–420. doi:10.1093/aje/kwh236
   PubMed Web of Science ®Google Scholar
• Williams RR, Hunt SC, Schumacher MC, et al. Diagnosing heterozygous familial hypercholesterolemia using new practical criteria validated by molecular genetics. Am J Cardiol. 1993;72(2):171–176. doi:10.1016/0002-9149(93)90155-6
   PubMed Web of Science ®Google Scholar
• Harada-Shiba M, Ohta T, Ohtake A, et al. Joint Working Group by Japan Pediatric Society and Japan Atherosclerosis Society for Making Guidance of Pediatric Familial Hypercholesterolemia. Guidance for Pediatric Familial Hypercholesterolemia 2017. J Atheroscler Thromb. 2018 ;25(6):539–553.
   Google Scholar
• Eissa MA, Mihalopoulos NL, Holubkov R, Dai S, Labarthe DR. Changes in fasting lipids during puberty. J Pediatr. 2016;170:199–205. doi:10.1016/j.jpeds.2015.11.018
   PubMed Web of Science ®Google Scholar
• Tada H, Nohara A, Kawashiri MA. Monogenic, polygenic, and oligogenic familial hypercholesterolemia. Curr Opin Lipidol. 2019;30(4):300–306. doi:10.1097/MOL.0000000000000609
   PubMed Web of Science ®Google Scholar
• Masana L, Ibarretxe D, Rodríguez-Borjabad C, et al. Expert group from the Spanish arteriosclerosis society. Toward a new clinical classification of patients with familial hypercholesterolemia: one perspective from Spain. Atherosclerosis. 2019;287:89–92. doi:10.1016/j.atherosclerosis.2019.06.905
   PubMed Web of Science ®Google Scholar
• France M. Homozygous familial hypercholesterolaemia: update on management. Paediatr Int Child Health. 2016;36(4):243–247. doi:10.1080/20469047.2016.1246640
   PubMed Web of Science ®Google Scholar
• Raal FJ, Hovingh GK, Catapano AL. Familial hypercholesterolemia treatments: guidelines and new therapies. Atherosclerosis. 2018;277:483–492. doi:10.1016/j.atherosclerosis.2018.06.859
   PubMed Web of Science ®Google Scholar
• Pottle A, Thompson G, Barbir M, et al. Lipoprotein apheresis efficacy, challenges and outcomes: a descriptive analysis from the UK lipoprotein apheresis registry, 1989–2017. Atherosclerosis. 2019;290:44–51. doi:10.1016/j.atherosclerosis.2019.09.006
   PubMed Web of Science ®Google Scholar
• Kawagishi N, Satoh K, Akamatsu Y, et al. Long-term outcome after living donor liver transplantation for two cases of homozygous familial hypercholesterolemia from a heterozygous donor. J Atheroscler Thromb. 2007;14(2):94–98. doi:10.5551/jat.14.94
   PubMed Web of Science ®Google Scholar
• Mlinaric M, Bratanic N, Dragos V, et al. Case report: liver transplantation in homozygous familial hypercholesterolemia (HoFH)-long-term follow-up of a patient and literature review. Front Pediatr. 2020;8:567895. doi:10.3389/fped.2020.567895
   PubMed Web of Science ®Google Scholar
• Santos RD, Stein EA, Hovingh GK, et al. Long-term evolocumab in patients with familial hypercholesterolemia. J Am Coll Cardiol. 2020;75(6):565–574. doi:10.1016/j.jacc.2019.12.020
   PubMed Web of Science ®Google Scholar
• Malhotra A, Shafiq N, Arora A, Singh M, Kumar R, Malhotra S. Dietary interventions (plant sterols, stanols, omega-3 fatty acids, soy protein and dietary fibers) for familial hypercholesterolaemia. Cochrane Database Syst Rev. 1975;2014;2014(3):CD001918. doi:10.1152/ajplegacy.1975.229.3.570
   Google Scholar
• Tada H, Nohara A, Inazu A, Sakuma N, Mabuchi H, Kawashiri M-A. Sitosterolemia, hypercholesterolemia, and coronary artery disease. J Atheroscler Thromb. 2018;25(9):783–789. doi:10.5551/jat.RV17024
   PubMed Web of Science ®Google Scholar
• Tada H, Okada H, Nomura A, et al. Rare and deleterious mutations in ABCG5/ABCG8 genes contribute to mimicking and worsening of familial hypercholesterolemia phenotype. Circ J. 2019;83(9):1917–1924. doi:10.1253/circj.CJ-19-0317
   PubMed Web of Science ®Google Scholar
• Tada H, Kawashiri MA, Takata M, et al. Infantile cases of sitosterolaemia with novel mutations in the ABCG5 gene: extreme hypercholesterolaemia is exacerbated by breastfeeding. JIMD Rep. 2015;21:115–122.
   PubMedGoogle Scholar
• Tada H, Kawashiri MA, Okada H, et al. Assessments of carotid artery plaque burden in patients with familial hypercholesterolemia. Am J Cardiol. 2017;120(11):1955–1960. doi:10.1016/j.amjcard.2017.08.012
   PubMed Web of Science ®Google Scholar
• Tada H, Nakagawa T, Okada H, et al. Clinical impact of carotid plaque score rather than carotid intima-media thickness on recurrence of atherosclerotic cardiovascular disease events. J Atheroscler Thromb. 2020;27(1):38–46. doi:10.5551/jat.49551
   PubMed Web of Science ®Google Scholar
• Okada H, Tada H, Hayashi K, et al. Aortic root calcification score as an independent factor for predicting major adverse cardiac events in familial hypercholesterolemia. J Atheroscler Thromb. 2018;25(7):634–642. doi:10.5551/jat.42705
   PubMed Web of Science ®Google Scholar
• Tada H, Kawashiri MA, Okada H, et al. Assessment of coronary atherosclerosis in patients with familial hypercholesterolemia by coronary computed tomography angiography. Am J Cardiol. 2015;115(6):724–729. doi:10.1016/j.amjcard.2014.12.034
   PubMed Web of Science ®Google Scholar
• Tada H, Kawashiri MA, Nohara A, Inazu A, Mabuchi H, Yamagishi M. Assessment of arterial stiffness in patients with familial hypercholesterolemia. J Clin Lipidol. 2018;12(2):397–402. doi:10.1016/j.jacl.2017.12.002
   PubMed Web of Science ®Google Scholar
• Dombalis S, Nash A. The effect of statins in children and adolescents with familial hypercholesterolemia: a systematic review. J Pediatr Health Care. 2020;S0891-5245(20)30308–4. doi:10.1016/j.pedhc.2020.11.007
   PubMed Web of Science ®Google Scholar
• Anagnostis P, Vaitsi K, Kleitsioti P, et al. Efficacy and safety of statin use in children and adolescents with familial hypercholesterolaemia: a systematic review and meta-analysis of randomized-controlled trials. Endocrine. 2020;69(2):249–261. doi:10.1007/s12020-020-02302-8
   PubMed Web of Science ®Google Scholar
• Goldberg AC, Hopkins PN, Toth PP, et al. Familial hypercholesterolemia: screening, diagnosis and management of pediatric and adult patients: clinical guidance from the national lipid association expert panel on familial hypercholesterolemia. J Clin Lipidol. 2011;5(3):133–140. doi:10.1016/j.jacl.2011.03.001
   PubMedGoogle Scholar
• Glueck CJ, Mellies MJ, Dine M, Perry T, Laskarzewski P. Safety and efficacy of long-term diet and diet plus bile acid-binding resin cholesterol-lowering therapy in 73 children heterozygous for familial hypercholesterolemia. Pediatrics. 1986;78(2):338–348.
   PubMed Web of Science ®Google Scholar
• van der Graaf A, Cuffie-Jackson C, Vissers MN, et al. Efficacy and safety of coadministration of ezetimibe and simvastatin in adolescents with heterozygous familial hypercholesterolemia. J Am Coll Cardiol. 2008;52(17):1421–1429. doi:10.1016/j.jacc.2008.09.002
   PubMed Web of Science ®Google Scholar
• Santos RD, Ruzza A, Hovingh GK, HAUSER-RCT Investigators, et al.. Evolocumab in pediatric heterozygous familial hypercholesterolemia. N Engl J Med. 2020;383(14):1317–1327. doi:10.1056/NEJMoa2019910
   PubMed Web of Science ®Google Scholar
• Ramaswami U, Futema M, Bogsrud MP, Holven KB. Comparison of the characteristics at diagnosis and treatment of children with heterozygous familial hypercholesterolaemia (FH) from eight European countries. Atherosclerosis. 2020;292:178–187. doi:10.1016/j.atherosclerosis.2019.11.012
   PubMed Web of Science ®Google Scholar
• Raal FJ, Rosenson RS, Reeskamp LF, ELIPSE HoFH Investigators, et al.. Evinacumab for homozygous familial hypercholesterolemia. N Engl J Med. 2020;383(8):711–720. doi:10.1056/NEJMoa2004215
   PubMed Web of Science ®Google Scholar
• Tada H, Kawashiri MA, Nomura A, et al. Oligogenic familial hypercholesterolemia, LDL cholesterol, and coronary artery disease. J Clin Lipidol. 2018;12(6):1436–1444. doi:10.1016/j.jacl.2018.08.006
   PubMed Web of Science ®Google Scholar