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Klin Monbl Augenheilkd 2019; 236(03): 236-243
DOI: 10.1055/a-0841-3417
DOI: 10.1055/a-0841-3417
Übersicht
Der natürliche Verlauf der Choroideremie
The Natural History of ChoroideraemiaFurther Information
Publication History
eingereicht 03 September 2018
akzeptiert 18 January 2019
Publication Date:
21 March 2019 (online)
Zusammenfassung
Seit ihrer Erstbeschreibung im Jahr 1872 herrscht um den natürlichen Verlauf der Choroideremie eine rege und in Teilen bis heute andauernde akademische Debatte. Aufgrund der Seltenheit der Erkrankung verlief diese traditionell weitgehend am Rande des klinisch geprägten Interessenhorizonts. Nun jedoch hat die Entwicklung grundlegend neuer, potenziell verlaufsmodifizierender Therapieansätze die Frage nach dem natürlichen Verlauf der Chorioideremie ins Zentrum der Aufmerksamkeit eines größeren Fachpublikums gerückt. Dieser Übersichtsartikel subsumiert den aktuellen Stand der Fachliteratur zum natürlichen Verlauf dieser seltenen Erkrankung und illustriert dessen Eigenheiten anhand eines übersichtlichen 2-Phasen-Modells. Neben einer ausführlichen Besprechung klinisch gängiger Modalitäten liegt der Fokus des Manuskripts auf der Ausarbeitung forschungsrelevanter Fragestellungen wie der intraindividuellen Symmetrie sowie der Etablierung neuer Endpunkte. Darüber hinaus werden die Limitationen bisheriger Studien diskutiert und Empfehlungen für zukünftige Beobachtungsstudien entwickelt.
Abstract
Since its first description in 1872, there has been a lively academic debate about the natural history of choroideremia. Due to the low prevalence of choroideremia, interest in this discussion has been limited to subspecialists. However, the current development of novel, potentially disease-modifying therapies has sparked the attention of a larger professional audience. This review summarises the literature around the natural history of the disease and illustrates its key aspects using a simple two-stage model. Apart from a comprehensive discussion of ubiquitous clinical modalities, the manuscript reviews scientifically relevant questions, such as intra-individual symmetry and the utility of novel endpoints for use in clinical studies. Furthermore, it examines the limitations of past and current studies and develops recommendations for further observational trials.
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Literatur
- 1 Khan KN, Islam F, Moore AT. et al. Clinical and genetic features of choroideremia in childhood. Ophthalmology 2016; 123: 2158-2165 doi:10.1016/j.ophtha.2016.06.051
- 2 Rodrigues MM, Ballintine EJ, Wiggert BN. et al. Choroideremia: a clinical, electron microscopic, and biochemical report. Ophthalmology 1984; 91: 873-883
- 3 MacDonald IM, Russell L, Chan CC. Choroideremia: new findings from ocular pathology and review of recent literature. Surv Ophthalmol 2009; 54: 401-407 doi:10.1016/j.survophthal.2009.02.008
- 4 Genead MA, McAnany JJ, Fishman GA. Retinal nerve fiber thickness measurements in choroideremia patients with spectral-domain optical coherence tomography. Ophthalmic Genet 2011; 32: 101-106 doi:10.3109/13816810.2010.544364
- 5 Xue K, Jolly JK, Barnard AR. et al. Beneficial effects on vision in patients undergoing retinal gene therapy for choroideremia. Nat Med 2018; 24: 1507-1512 doi:10.1038/s41591-018-0185-5
- 6 Edwards TL, Jolly JK, Groppe M. et al. Visual acuity after retinal gene therapy for choroideremia. N Engl J Med 2016; 374: 1996-1998 doi:10.1056/NEJMc1509501
- 7 MacLaren RE, Groppe M, Barnard AR. et al. Retinal gene therapy in patients with choroideremia: initial findings from a phase 1/2 clinical trial. Lancet 2014; 383: 1129-1137 doi:10.1016/s0140-6736(13)62117-0
- 8 Reichel FF, Dauletbekov DL, Klein R. et al. AAV8 can induce innate and adaptive immune response in the primate eye. Mol Ther 2017; 25: 2648-2660 doi:10.1016/j.ymthe.2017.08.018
- 9 Dimopoulos IS, Hoang SC, Radziwon A. et al. Two-year results after AAV2-mediated gene therapy for choroideremia: the Alberta experience. Am J Ophthalmol 2018; 193: 130-142 doi:10.1016/j.ajo.2018.06.011
- 10 Lam BL, Davis JL, Gregori NZ. et al. Choroideremia gene therapy phase 2 clinical trial: 24-month results. Am J Ophthalmol 2019; 197: 65-73 doi:10.1016/j.ajo.2018.09.012
- 11 Nightstar Therapeutics. Efficacy and Safety of AAV2-REP1 for the Treatment of Choroideremia (STAR). ClinicalTrials.gov. ClinicalTrials.gov Identifier: NCT03496012. Im Internet: https://clinicaltrials.gov/ct2/show/NCT03496012 Stand: 18.02.2019
- 12 Mauthner L. Ein Fall von Chorioideremie. Bericht des Naturwissenschaftlich-Medizinischen Vereins Innsbruck 1872; 1872: 191-197
- 13 Koenig H. Zwei Beobachtungen von mangelhafter Entwickelung der Choroides verbunden mit Hemeralopie. Greifswald: Kunike; 1874
- 14 Sorsby A, Franceschetti A, Joseph R. et al. Choroideremia: clinical and genetic aspects. Br J Ophthalmol 1952; 36: 547-581
- 15 Pameyer JK, Waardenburg PJ, Henkes HE. Choroideremia. Br J Ophthalmol 1960; 44: 724-738
- 16 Cremers FP, Brunsmann F, van de Pol TJ. et al. Deletion of the DXS165 locus in patients with classical choroideremia. Clin Genet 1987; 32: 421-423
- 17 Cremers FP, van de Pol DJ, Diergaarde PJ. et al. Physical fine mapping of the choroideremia locus using Xq21 deletions associated with complex syndromes. Genomics 1989; 4: 41-46
- 18 Cremers FP, Sankila EM, Brunsmann F. et al. Deletions in patients with classical choroideremia vary in size from 45 kb to several megabases. Am J Hum Genet 1990; 47: 622-628
- 19 Seabra MC, Brown MS, Goldstein JL. Retinal degeneration in choroideremia: deficiency of rab geranylgeranyl transferase. Science 1993; 259: 377-381
- 20 Seabra MC, Ho YK, Anant JS. Deficient geranylgeranylation of Ram/Rab27 in choroideremia. J Biol Chem 1995; 270: 24420-24427
- 21 Alexandrov K, Horiuchi H, Steele-Mortimer O. et al. Rab escort protein-1 is a multifunctional protein that accompanies newly prenylated rab proteins to their target membranes. EMBO J 1994; 13: 5262-5273
- 22 Keeling E, Lotery AJ, Tumbarello DA. et al. Impaired cargo clearance in the retinal pigment epithelium (RPE) underlies irreversible blinding diseases. Cells 2018;
- 23 Krock BL, Bilotta J, Perkins BD. Noncell-autonomous photoreceptor degeneration in a zebrafish model of choroideremia. Proc Natl Acad Sci U S A 2007; 104: 4600-4605 doi:10.1073/pnas.0605818104
- 24 Wavre-Shapton ST, Tolmachova T, Lopes da Silva M. et al. Conditional ablation of the choroideremia gene causes age-related changes in mouse retinal pigment epithelium. PLoS One 2013; 8: e57769 doi:10.1371/journal.pone.0057769
- 25 Gibbs D, Kitamoto J, Williams DS. Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VII a, the Usher syndrome 1B protein. Proc Natl Acad Sci U S A 2003; 100: 6481-6486 doi:10.1073/pnas.1130432100
- 26 Jain N, Jia Y, Gao SS. et al. Optical coherence tomography angiography in choroideremia: correlating choriocapillaris loss with overlying degeneration. JAMA Ophthalmol 2016; 134: 697-702 doi:10.1001/jamaophthalmol.2016.0874
- 27 Sun LW, Johnson RD, Williams V. et al. Multimodal imaging of photoreceptor structure in choroideremia. PLoS One 2016; 11: e0167526 doi:10.1371/journal.pone.0167526
- 28 Jacobson SG, Cideciyan AV, Sumaroka A. et al. Remodeling of the human retina in choroideremia: rab escort protein 1 (REP-1) mutations. Invest Ophthalmol Vis Sci 2006; 47: 4113-4120 doi:10.1167/iovs.06-0424
- 29 Tolmachova T, Anders R, Abrink M. et al. Independent degeneration of photoreceptors and retinal pigment epithelium in conditional knockout mouse models of choroideremia. J Clin Invest 2006; 116: 386-394 doi:10.1172/jci26617
- 30 Syed R, Sundquist SM, Ratnam K. et al. High-resolution images of retinal structure in patients with choroideremia. Invest Ophthalmol Vis Sci 2013; 54: 950-961 doi:10.1167/iovs.12-10707
- 31 Morgan JI, Han G, Klinman E. et al. High-resolution adaptive optics retinal imaging of cellular structure in choroideremia. Invest Ophthalmol Vis Sci 2014; 55: 6381-6397 doi:10.1167/iovs.13-13454
- 32 Dimopoulos IS, Radziwon A, St Laurent CD. et al. Choroideremia. Curr Opin Ophthalmol 2017; 28: 410-415 doi:10.1097/icu.0000000000000392
- 33 Xue K, Oldani M, Jolly JK. et al. Correlation of optical coherence tomography and autofluorescence in the outer retina and choroid of patients with choroideremia. Invest Ophthalmol Vis Sci 2016; 57: 3674-3684 doi:10.1167/iovs.15-18364
- 34 Battaglia Parodi M, Arrigo A, MacLaren RE. et al. Vascular alterations revealed with optical coherence tomography angiography in patients with choroideremia. Retina 2018;
- 35 Cremers FP, Armstrong SA, Seabra MC. et al. REP-2, a Rab escort protein encoded by the choroideremia-like gene. J Biol Chem 1994; 269: 2111-2117
- 36 Strunnikova NV, Barb J, Sergeev YV. et al. Loss-of-function mutations in Rab escort protein 1 (REP-1) affect intracellular transport in fibroblasts and monocytes of choroideremia patients. PLoS One 2009; 4: e8402 doi:10.1371/journal.pone.0008402
- 37 Zhang AY, Mysore N, Vali H. et al. Choroideremia is a systemic disease with lymphocyte crystals and plasma lipid and rbc membrane abnormalities. Invest Ophthalmol Vis Sci 2015; 56: 8158-8165 doi:10.1167/iovs.14-15751
- 38 Tolmachova T, Tolmachov OE, Barnard AR. et al. Functional expression of Rab escort protein 1 following AAV2-mediated gene delivery in the retina of choroideremia mice and human cells ex vivo. J Mol Med (Berl) 2013; 91: 825-837 doi:10.1007/s00109-013-1006-4
- 39 Xue K, Groppe M, Salvetti AP. et al. Technique of retinal gene therapy: delivery of viral vector into the subretinal space. Eye (Lond) 2017; 31: 1308-1316 doi:10.1038/eye.2017.158
- 40 van Bokhoven H, van den Hurk JA, Bogerd L. et al. Cloning and characterization of the human choroideremia gene. Hum Mol Genet 1994; 3: 1041-1046
- 41 Coussa RG, Traboulsi EI. Choroideremia: a review of general findings and pathogenesis. Ophthalmic Genet 2012; 33: 57-65 doi:10.3109/13816810.2011.620056
- 42 Simunovic MP, Jolly JK, Xue K. et al. The spectrum of CHM gene mutations in choroideremia and their relationship to clinical phenotype. Invest Ophthalmol Vis Sci 2016; 57: 6033-6039 doi:10.1167/iovs.16-20230
- 43 van den Hurk JA, Schwartz M, van Bokhoven H. et al. Molecular basis of choroideremia (CHM): mutations involving the Rab escort protein-1 (REP-1) gene. Hum Mutat 1997; 9: 110-117 doi:10.1002/(SICI)1098-1004(1997)9:2<110::AID-HUMU2>3.0.CO;2-D
- 44 Struck MC. Long-term results of pediatric cataract surgery and primary intraocular lens implantation from 7 to 22 months of life. JAMA Ophthalmol 2015; 133: 1180-1183 doi:10.1001/jamaophthalmol.2015.2062
- 45 Lundvall A, Zetterstrom C. Complications after early surgery for congenital cataracts. Acta Ophthalmol Scand 1999; 77: 677-680
- 46 Freund PR, Sergeev YV, MacDonald IM. Analysis of a large choroideremia dataset does not suggest a preference for inclusion of certain genotypes in future trials of gene therapy. Mol Genet Genomic Med 2016; 4: 344-358 doi:10.1002/mgg3.208
- 47 Kurstjens JH. Choroideremia and gyrate atrophy of the choroid and retina. Doc Ophthalmol 1965; 19: 2-122 doi:10.1007/bf00180759
- 48 Hammerstein W, Bischof G, Leide E. Chorioideremie im Kindesalter. Klin Monatsbl Augenheilkd 1979; 174: 599-604
- 49 Mura M, Sereda C, Jablonski MM. et al. Clinical and functional findings in choroideremia due to complete deletion of the CHM gene. Arch Ophthalmol 2007; 125: 1107-1113 doi:10.1001/archopht.125.8.1107
- 50 Sieving PA, Niffenegger JH, Berson EL. Electroretinographic findings in selected pedigrees with choroideremia. Am J Ophthalmol 1986; 101: 361-367
- 51 Curcio CA, Allen KA, Sloan KR. et al. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J Comp Neurol 1991; 312: 610-624 doi:10.1002/cne.903120411
- 52 McCulloch C. Choroideremia: a clinical and pathologic review. Trans Am Ophthalmol Soc 1969; 67: 142-195
- 53 Dimopoulos IS, Freund PR, Knowles JA. et al. The natural history of full-field stimulus threshold decline in choroideremia. Retina 2018; 38: 1731-1742 doi:10.1097/iae.0000000000001764
- 54 Kärnä J. Choroideremia. A clinical and genetic study of 84 Finnish patients and 126 female carriers. Acta Ophthalmol Suppl 1986; 176: 1-68
- 55 Seitz IP, Zhour A, Kohl S. et al. Multimodal assessment of choroideremia patients defines pre-treatment characteristics. Graefes Arch Clin Exp Ophthalmol 2015; 253: 2143-2150 doi:10.1007/s00417-015-2976-4
- 56 Jolly JK, Xue K, Edwards TL. et al. Characterizing the natural history of visual function in choroideremia using microperimetry and multimodal retinal imaging. Invest Ophthalmol Vis Sci 2017; 58: 5575-5583 doi:10.1167/iovs.17-22486
- 57 Roberts MF, Fishman GA, Roberts DK. et al. Retrospective, longitudinal, and cross sectional study of visual acuity impairment in choroideraemia. Br J Ophthalmol 2002; 86: 658-662
- 58 Heon E, Alabduljalil T, McGuigan III DB. et al. Visual function and central retinal structure in choroideremia. Invest Ophthalmol Vis Sci 2016; 57: OCT377-OCT387 doi:10.1167/iovs.15-18421
- 59 Aylward JW, Xue K, Patricio MI. et al. Retinal degeneration in choroideremia follows an exponential decay function. Ophthalmology 2018; 125: 1122-1124 doi:10.1016/j.ophtha.2018.02.004
- 60 Birch DG, Anderson JL, Fish GE. Yearly rates of rod and cone functional loss in retinitis pigmentosa and cone-rod dystrophy. Ophthalmology 1999; 106: 258-268 doi:10.1016/s0161-6420(99)90064-7
- 61 Iannaccone A, Kritchevsky SB, Ciccarelli ML. et al. Kinetics of visual field loss in Usher syndrome Type II. Invest Ophthalmol Vis Sci 2004; 45: 784-792
- 62 Cideciyan AV, Swider M, Aleman TS. et al. ABCA4 disease progression and a proposed strategy for gene therapy. Hum Mol Genet 2009; 18: 931-941 doi:10.1093/hmg/ddn421
- 63 Massof RW, Dagnelie G, Benzschawel T. et al. First order dynamics of visual field loss in retinitis pigmentosa. Clin Vis Sci 1990; 5: 1-26
- 64 Grover S, Fishman GA, Anderson RJ. et al. Rate of visual field loss in retinitis pigmentosa. Ophthalmology 1997; 104: 460-465
- 65 Jolly JK, Groppe M, Birks J. et al. Functional defects in color vision in patients with choroideremia. Am J Ophthalmol 2015; 160: 822-831.e3 doi:10.1016/j.ajo.2015.06.018
- 66 Seitz IP, Jolly JK, Dominik Fischer M. et al. Colour discrimination ellipses in choroideremia. Graefes Arch Clin Exp Ophthalmol 2018; 256: 665-673 doi:10.1007/s00417-018-3921-0
- 67 Freund PR, Sergeev YV, MacDonald IM. Analysis of a large choroideremia dataset does not suggest a preference for inclusion of certain genotypes in future trials of gene therapy. Mol Genet Genomic Med 2016; 4: 344-358 doi:10.1002/mgg3.208
- 68 Coussa RG, Kim J, Traboulsi EI. Choroideremia: effect of age on visual acuity in patients and female carriers. Ophthalmic Genet 2012; 33: 66-73 doi:10.3109/13816810.2011.623261
- 69 Renner AB, Kellner U, Cropp E. et al. Choroideremia: variability of clinical and electrophysiological characteristics and first report of a negative electroretinogram. Ophthalmology 2006; 113: 2066.e1-10 doi:10.1016/j.ophtha.2006.05.045
- 70 Jolly JK, Edwards TL, Moules J. et al. A qualitative and quantitative assessment of fundus autofluorescence patterns in patients with choroideremia. Invest Ophthalmol Vis Sci 2016; 57: 4498-4503 doi:10.1167/iovs.15-18362
- 71 Hariri AH, Velaga SB, Girach A. et al. Measurement and reproducibility of preserved ellipsoid zone area and preserved retinal pigment epithelium area in eyes with choroideremia. Am J Ophthalmol 2017; 179: 110-117 doi:10.1016/j.ajo.2017.05.002
- 72 Wang Z, Camino A, Hagag AM. et al. Automated detection of preserved photoreceptor on optical coherence tomography in choroideremia based on machine learning. J Biophotonics 2018; 11: e201700313 doi:10.1002/jbio.201700313
- 73 Gao SS, Patel RC, Jain N. et al. Choriocapillaris evaluation in choroideremia using optical coherence tomography angiography. Biomed Opt Express 2017; 8: 48-56 doi:10.1364/boe.8.000048
- 74 Dysli C, Wolf S, Tran HV. et al. Autofluorescence lifetimes in patients with choroideremia identify photoreceptors in areas with retinal pigment epithelium atrophy. Invest Ophthalmol Vis Sci 2016; 57: 6714-6721 doi:10.1167/iovs.16-20392
- 75 Nightstar Therapeutics. Natural History of the Progression of Choroideremia Study (NIGHT). ClinicalTrials.gov. ClinicalTrials.gov Identifier: NCT03359551. Im Internet: https://clinicaltrials.gov/ct2/show/NCT03359551 Stand: 18.02.2019
- 76 4D Molecular Therapeutics. Natural History Study of Choroideremia. ClinicalTrials.gov. ClinicalTrials.gov Identifier: NCT02994368. Im Internet: https://clinicaltrials.gov/ct2/show/NCT02994368 Stand: 18.02.2019