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REVIEW

Managing Diagnosis, Treatment, and Burden of Disease in Hereditary Angioedema Patients with Normal C1-Esterase Inhibitor

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Pages 447-460 | Received 25 Nov 2022, Accepted 23 Feb 2023, Published online: 22 Apr 2023

References

  • Busse PJ, Christiansen SC, Riedl MA, et al. US HAEA medical advisory board 2020 guidelines for the management of hereditary angioedema. J Allergy Clin Immunol Pract. 2021;9(1):132–150.e3. doi:10.1016/j.jaip.2020.08.046
  • Caballero T. Treatment of hereditary angioedema. J Investig Allergol Clin Immunol. 2021;31(1):1–16. doi:10.18176/jiaci.0653
  • Longhurst HJ, Bork K. Hereditary angioedema: an update on causes, manifestations and treatment. Br J Hosp Med. 2019;80(7):391–398. doi:10.12968/hmed.2019.80.7.391
  • Banday AZ, Kaur A, Jindal AK, Rawat A, Singh S. An update on the genetics and pathogenesis of hereditary angioedema. Genes Dis. 2019;7(1):75–83. doi:10.1016/j.gendis.2019.07.002
  • Zuraw BL, Bork K, Binkley KE, et al. Hereditary angioedema with normal C1 inhibitor function: consensus of an international expert panel. Allergy Asthma Proc. 2012;33(Suppl 1):S145–S156. doi:10.2500/aap.2012.33.3627
  • Bork K, Barnstedt SE, Koch P, Traupe H. Hereditary angioedema with normal C1-inhibitor activity in women. Lancet. 2000;356(9225):213–217. doi:10.1016/S0140-6736(00)02483-1
  • Binkley KE, Davis A. Clinical, biochemical, and genetic characterization of a novel estrogen-dependent inherited form of angioedema. J Allergy Clin Immunol. 2000;106(3):546–550. doi:10.1067/mai.2000.108106
  • Busse PJ, Christiansen SC. Hereditary angioedema. N Engl J Med. 2020;382(12):1136–1148. doi:10.1056/NEJMra1808012
  • Jones DH, Bansal P, Bernstein JA, et al. Clinical profile and treatment outcomes in patients with hereditary angioedema with normal C1 esterase inhibitor. World Allergy Organ J. 2022;15(1):100621. doi:10.1016/j.waojou.2021.100621
  • Riedl MA. Hereditary angioedema with normal C1-INH (HAE type III). J Allergy Clin Immunol Pract. 2013;1(5):427–432. doi:10.1016/j.jaip.2013.06.004
  • Magerl M, Germenis AE, Maas C, Maurer M. Hereditary angioedema with normal C1 inhibitor: update on evaluation and treatment. Immunol Allergy Clin North Am. 2017;37(3):571–584. doi:10.1016/j.iac.2017.04.004
  • Henao MP, Kraschnewski JL, Kelbel T, Craig TJ. Diagnosis and screening of patients with hereditary angioedema in primary care. Ther Clin Risk Manag. 2016;12:701–711. doi:10.2147/TCRM.S86293
  • Maurer M, Magerl M, Betschel S, et al. The international WAO/EAACI guideline for the management of hereditary angioedema - the 2021 revision and update. World Allergy Organ J. 2022;15(3):100627. doi:10.1016/j.waojou.2022.100627
  • Gompels MM, Lock RJ, Unsworth DJ, Johnston SL, Archer CB, Davies SV. Misdiagnosis of hereditary angio-oedema type 1 and type 2. Br J Dermatol. 2003;148(4):719–723. doi:10.1046/j.1365-2133.2003.05231.x
  • Dewald G, Bork K. Missense mutations in the coagulation factor XII (Hageman factor) gene in hereditary angioedema with normal C1 inhibitor. Biochem Biophys Res Commun. 2006;343(4):1286–1289. doi:10.1016/j.bbrc.2006.03.092
  • Bafunno V, Firinu D, D’Apolito M, et al. Mutation of the angiopoietin-1 gene (ANGPT1) associates with a new type of hereditary angioedema. J Allergy Clin Immunol. 2018;141(3):1009–1017. doi:10.1016/j.jaci.2017.05.020
  • Bork K, Wulff K, Steinmüller‐Magin L, et al. Hereditary angioedema with a mutation in the plasminogen gene. Allergy. 2018;73(2):442–450. doi:10.1111/all.13270
  • Bork K, Wulff K, Rossmann H, et al. Hereditary angioedema cosegregating with a novel kininogen 1 gene mutation changing the N‐terminal cleavage site of bradykinin. Allergy. 2019;74(12):2479–2481. doi:10.1111/all.13869
  • Ariano A, D’Apolito M, Bova M, et al. A myoferlin gain-of-function variant associates with a new type of hereditary angioedema. Allergy. 2020;75(11):2989–2992. doi:10.1111/all.14454
  • Bork K, Wulff K, Möhl BS, et al. Novel hereditary angioedema linked with a heparan sulfate 3-O-sulfotransferase 6 gene mutation. J Allergy Clin Immunol. 2021;148(4):1041–1048. doi:10.1016/j.jaci.2021.01.011
  • Bork K, Machnig T, Wulff K, Witzke G, Prusty S, Hardt J. Clinical features of genetically characterized types of hereditary angioedema with normal C1 inhibitor: a systematic review of qualitative evidence. Orphanet J Rare Dis. 2020;15(1):289. doi:10.1186/s13023-020-01570-x
  • Loules G, Parsopoulou F, Zamanakou M, et al. Deciphering the genetics of primary angioedema with normal levels of C1 inhibitor. J Clin Med. 2020;9(11):3402. doi:10.3390/jcm9113402
  • Sharma J, Jindal AK, Banday AZ, et al. Pathophysiology of hereditary angioedema (HAE) beyond the SERPING1 gene. Clin Rev Allergy Immunol. 2021;60(3):305–315. doi:10.1007/s12016-021-08835-8
  • Dickeson SK, Kumar S, Sun MF, et al. A mechanism for hereditary angioedema caused by a lysine 311-to-glutamic acid substitution in plasminogen. Blood. 2022;139(18):2816–2829. doi:10.1182/blood.2021012945
  • Napolitano F, Montuori N. The role of the plasminogen activation system in angioedema: novel insights on the pathogenesis. J Clin Med. 2021;10(3):518. doi:10.3390/jcm10030518
  • d’Apolito M, Santacroce R, Colia AL, Cordisco G, Maffione AB, Margaglione M. Angiopoietin‐1 haploinsufficiency affects the endothelial barrier and causes hereditary angioedema. Clin Exp Allergy. 2019;49(5):626–635. doi:10.1111/cea.13349
  • Farkas H, Martinez‐Saguer I, Bork K, et al. International consensus on the diagnosis and management of pediatric patients with hereditary angioedema with C1 inhibitor deficiency. Allergy. 2017;72(2):300–313. doi:10.1111/all.13001
  • Salguero CAS, Chacon AIS. HAE in children- what is the best treatment strategy? Int J Aller Medications. 2016;2(1):16. doi:10.23937/2572-3308.1510016
  • Bork K, Gül D, Hardt J, Dewald G. Hereditary angioedema with normal C1 inhibitor: clinical symptoms and course. Am J Med. 2007;120(11):987–992. doi:10.1016/j.amjmed.2007.08.021
  • Fragnan NTML, Veronez C, Moreno A, et al. Treatment of patients with hereditary angioedema with normal C1 inhibitor: evaluation of 295 patients. J Allergy Clin Immunol. 2019;143(2):AB40. doi:10.1016/j.jaci.2018.12.120
  • Marcos C, López Lera A, Varela S, Liñares T, Alvarez-Eire MG, López-Trascasa M. Clinical, biochemical, and genetic characterization of type III hereditary angioedema in 13 Northwest Spanish families. Ann Allergy Asthma Immunol. 2012;109(3):195–200.e2. doi:10.1016/j.anai.2012.05.022
  • Bork K, Wulff K, Hardt J, Witzke G, Staubach P. Hereditary angioedema caused by missense mutations in the factor XII gene: clinical features, trigger factors, and therapy. J Allergy Clin Immunol. 2009;124(1):129–134. doi:10.1016/j.jaci.2009.03.038
  • Deroux A, Boccon-Gibod I, Fain O, et al. Hereditary angioedema with normal C1 inhibitor and factor XII mutation: a series of 57 patients from the French National Center of Reference for Angioedema. Clin Exp Immunol. 2016;185(3):332–337. doi:10.1111/cei.12820
  • Bova M, Suffritti C, Bafunno V, et al. Impaired control of the contact system in hereditary angioedema with normal C1‐inhibitor. Allergy. 2020;75(6):1394–1403. doi:10.1111/all.14160
  • Gabriel N, Marcelino F, Ferriani MPL, et al. Pregnancy in patients with hereditary angioedema and normal C1 inhibitor. Front Allergy. 2022;3:846968. doi:10.3389/falgy.2022.846968
  • Bork K. Diagnosis and treatment of hereditary angioedema with normal C1 inhibitor. Allergy Asthma Clin Immunol. 2010;6(1):15. doi:10.1186/1710-1492-6-15
  • Jones D, Park N, Thompson A. M101 joint pain: a rare symptom in patients with hereditary angioedema with normal C1-INH. Ann Allergy Asthma Immunol. 2021;127(5 Suppl):S82. doi:10.1016/j.anai.2021.08.255
  • Caballero T, Maurer M, Longhurst HJ, et al. Triggers and prodromal symptoms of angioedema attacks in patients with hereditary angioedema. J Investig Allergol Clin Immunol. 2016;26(6):383–386. doi:10.18176/jiaci.0102
  • Magerl M, Doumoulakis G, Kalkounou I, et al. Characterization of prodromal symptoms in a large population of patients with hereditary angio‐oedema. Clin Exp Dermatol. 2014;39(3):298–303. doi:10.1111/ced.12285
  • Taya J, Veronez CL, Pesquero JB, Bork K, Grumach AS. Uncommon signs associated with hereditary angioedema with normal C1 inhibitor. J Investig Allergol Clin Immunol. 2021;31(3):257–258. doi:10.18176/jiaci.0509
  • Lara-Marquez ML, Christiansen SC, Riedl MA, Herschbach J, Zuraw BL. Threshold-stimulated kallikrein activity distinguishes bradykinin- from histamine-mediated angioedema. Clin Exp Allergy. 2018;48(11):1429–1438. doi:10.1111/cea.13219
  • McKibbin L, Barber C, Kalicinsky C, Warrington R. Review of the Manitoba cohort of patients with hereditary angioedema with normal C1 inhibitor. Allergy Asthma Clin Immunol. 2019;15:66. doi:10.1186/s13223-019-0381-y
  • Bernstein JA. Severity of hereditary angioedema, prevalence, and diagnostic considerations. Am J Manag Care. 2018;24(14 Suppl):S292–S298.
  • Zafra H. Hereditary angioedema: a review. WMJ. 2022;121(1):48–53.
  • Dias MM, Moreno AS, Maia LSM, et al. A cost-effective algorithm for diagnosis of hereditary angioedema with normal C1 inhibitor: applying molecular approach to clinical practice. J Allergy Clin Immunol Pract. 2020;8(1):419–421.e4. doi:10.1016/j.jaip.2019.06.041
  • Cicardi M, Zuraw BL. Angioedema due to bradykinin dysregulation. J Allergy Clin Immunol Pract. 2018;6(4):1132–1141. doi:10.1016/j.jaip.2018.04.022
  • Lunn ML, Santos CB, Craig TJ. Is there a need for clinical guidelines in the United States for the diagnosis of hereditary angioedema and the screening of family members of affected patients? Ann Allergy Asthma Immunol. 2010;104(3):211–214. doi:10.1016/j.anai.2009.12.004
  • Lumry WR, Settipane RA. Hereditary angioedema: epidemiology and burden of disease. Allergy Asthma Proc. 2020;41(Suppl 1):S08–S13. doi:10.2500/aap.2020.41.200050
  • Pappalardo E, Cicardi M, Duponchel C, et al. Frequent de novo mutations and exon deletions in the C1inhibitor gene of patients with angioedema. J Allergy Clin Immunol. 2000;106(6):1147–1154. doi:10.1067/mai.2000.110471
  • Kelbel T. A case of normal C1 esterase inhibitor hereditary angioedema successfully treated with berotralstat. Ann Allergy Asthma Immunol. 2022;128(4):462–463. doi:10.1016/j.anai.2022.01.014
  • Lumry WR. Hereditary angioedema: the economics of treatment of an orphan disease. Front Med. 2018;5:22. doi:10.3389/fmed.2018.00022
  • Riedl MA, Banerji A, Gower R. Current medical management of hereditary angioedema: follow-up survey of US physicians. Ann Allergy Asthma Immunol. 2021;126(3):264–272. doi:10.1016/j.anai.2020.10.009
  • Bork K, Wulff K, Witzke G, Hardt J. Treatment for hereditary angioedema with normal C1‐INH and specific mutations in the F12 gene (HAE‐FXII). Allergy. 2017;72(2):320–324. doi:10.1111/all.13076
  • Bork K, Wulff K, Witzke G, Machnig T, Hardt J. Treatment of patients with hereditary angioedema with the c.988A>G (p.Lys330Glu) variant in the plasminogen gene. Orphanet J Rare Dis. 2020;15(1):52. doi:10.1186/s13023-020-1334-8
  • Perego F, Wu MA, Valerieva A, et al. Current and emerging biologics for the treatment of hereditary angioedema. Expert Opin Biol Ther. 2019;19(6):517–526. doi:10.1080/14712598.2019.1595581
  • Saule C, Boccon‐Gibod I, Fain O, et al. Benefits of progestin contraception in non‐allergic angioedema. Clin Exp Allergy. 2013;43(4):475–482. doi:10.1111/cea.12055
  • Crosignani P, Olive D, Bergqvist A, Luciano A. Advances in the management of endometriosis: an update for clinicians. Hum Reprod Update. 2006;12(2):179–189. doi:10.1093/humupd/dmi049
  • Luciano AA, Turksoy RN, Carleo J. Evaluation of oral medroxyprogesterone acetate in the treatment of endometriosis. Obstet Gynecol. 1988;72(3 Pt 1):323–327.
  • Bouillet L, Boccon‐Gibod I, Launay D, et al. Hereditary angioedema with normal C1 inhibitor in a French cohort: clinical characteristics and response to treatment with icatibant. Immun Inflamm Dis. 2017;5(1):29–36. doi:10.1002/iid3.137
  • ORLADEYO™ (berotralstat) capsules, for oral use [prescribing information]. Durham, NC, USA: BioCryst Pharmaceuticals, Inc; 2020.
  • European Medicines Agency. Summary of opinion (initial authorisation): Orladeyo: berotralstat; 2021. Available from: https://www.ema.europa.eu/en/documents/smop-initial/chmp-summary-positive-opinion-orladeyo_en.pdf. Accessed October 7, 2022.
  • Garcia JFB, Takejima P, Veronez CL, et al. Use of pdC1-INH concentrate for long-term prophylaxis during pregnancy in hereditary angioedema with normal C1-INH. J Allergy Clin Immunol Pract. 2018;6(4):1406–1408. doi:10.1016/j.jaip.2017.12.022
  • Caballero T, Canabal J, Rivero-Paparoni D, Cabañas R. Management of hereditary angioedema in pregnant women: a review. Int J Womens Health. 2014;6:839–848. doi:10.2147/IJWH.S46460
  • Sundler Björkman L, Persson B, Aronsson D, Skattum L, Nordenfelt P, Egesten A. Comorbidities in hereditary angioedema-A population‐based cohort study. Clin Transl Allergy. 2022;12(3):e12135. doi:10.1002/clt2.12135
  • Fouche AS, Saunders EFH, Craig T. Depression and anxiety in patients with Hereditary angioedema. Ann Allergy Asthma Immunol. 2014;112(4):371–375. doi:10.1016/j.anai.2013.05.028
  • Zarnowski J, Rabe M, Kage P, Simon JC, Treudler R. Prophylactic treatment in hereditary angioedema is associated with reduced anxiety in patients in Leipzig, Germany. Int Arch Allergy Immunol. 2021;182(9):819–826. doi:10.1159/000514973
  • Bork K, Bygum A, Hardt J. Benefits and risks of danazol in hereditary angioedema: a long-term survey of 118 patients. Ann Allergy Asthma Immunol. 2008;100(2):153–161. doi:10.1016/S1081-1206(10)60424-3
  • Birjmohun RS, Kees Hovingh G, Stroes ESG, et al. Effects of short-term and long-term danazol treatment on lipoproteins, coagulation, and progression of atherosclerosis: two clinical trials in healthy volunteers and patients with Hereditary angioedema. Clin Ther. 2008;30(12):2314–2323. doi:10.1016/j.clinthera.2008.12.021
  • Füst G, Farkas H, Csuka D, Varga L, Bork K. Long‐term efficacy of danazol treatment in hereditary angioedema. Eur J Clin Invest. 2011;41(3):256–262. doi:10.1111/j.1365-2362.2010.02402.x
  • Kalaria S, Craig T. Assessment of hereditary angioedema treatment risks. Allergy Asthma Proc. 2013;34(6):519–522. doi:10.2500/aap.2013.34.3702
  • Kuwahara S, Fukunaga A, Ohata M, et al. High prevalence of epilepsy in HAE with normal C1-INH. Allergol Int. 2020;69(4):630–632. doi:10.1016/j.alit.2020.04.008
  • Veronez CL, Campos RA, Constantino-Silva RN, Nicolicht P, Pesquero JB, Grumach AS. Hereditary angioedema-associated acute pancreatitis in C1-inhibitor deficient and normal C1-inhibitor patients: case reports and literature review. Front Med. 2019;6:80. doi:10.3389/fmed.2019.00080
  • Bygum A. Hereditary angio-oedema for dermatologists. Dermatology. 2019;235(4):263–275. doi:10.1159/000500196
  • Gutierrez M, Veronez CL, Rodrigues Valle SO, et al. Unnecessary abdominal surgeries in attacks of hereditary angioedema with normal C1 inhibitor. Clin Rev Allergy Immunol. 2021;61(1):60–65. doi:10.1007/s12016-021-08852-7
  • Malesker M. Addressing the individualized needs in hereditary angioedema: managed care strategies to optimize access to care. Am J Manag Care. 2022;28(1 Suppl):S3–S9. doi:10.37765/ajmc.2022.88822
  • Veronez CL, Moreno AS, Constantino-Silva RN, et al. Hereditary angioedema with normal C1 inhibitor and F12 mutations in 42 Brazilian families. J Allergy Clin Immunol Pract. 2018;6(4):1209–1216.e8. doi:10.1016/j.jaip.2017.09.025
  • Banerji A, Busse P, Christiansen SC, et al. Current state of hereditary angioedema management: a patient survey. Allergy Asthma Proc. 2015;36(3):213–217. doi:10.2500/aap.2015.36.3824
  • Maurer M, Aygören-Pürsün E, Banerji A, et al. Consensus on treatment goals in hereditary angioedema: a global Delphi initiative. J Allergy Clin Immunol. 2021;148(6):1526–1532. doi:10.1016/j.jaci.2021.05.016
  • Geba D, Mohd Sani J, Gascon M, Hahn R, Aggarwal K, Rosselli J. Hereditary angioedema patients would prefer newer-generation oral prophylaxis. J Drug Assess. 2021;10(1):51–56. doi:10.1080/21556660.2020.1863699
  • Martinez-Saguer I, Rusicke E, Aygören-Pürsün E, Heller C, Klingebiel T, Kreuz W. Characterization of acute hereditary angioedema attacks during pregnancy and breast-feeding and their treatment with C1 inhibitor concentrate. Am J Obstet Gynecol. 2010;203(2):131.e1–131.e7. doi:10.1016/j.ajog.2010.03.003
  • Czaller I, Visy B, Csuka D, Füst G, Tóth F, Farkas H. The natural history of hereditary angioedema and the impact of treatment with human C1-inhibitor concentrate during pregnancy: a long-term survey. Eur J Obstet Gynecol Reprod Biol. 2010;152(1):44–49. doi:10.1016/j.ejogrb.2010.05.008
  • Machado AM, Pires RM, Martins RO, Grumach AS. Pregnancy and postpartum in hereditary angioedema with C1 inhibitor deficit in women who have no access to therapy. J Investig Allergol Clin Immunol. 2017;27(5):322–323. doi:10.18176/jiaci.0175
  • Giavina-Bianchi P, Arruda LK, Aun MV, et al. Brazilian guidelines for hereditary angioedema management - 2017 update part 1: definition, classification and diagnosis. Clinics. 2018;73:e310. doi:10.6061/clinics/2018/e310