Original Article Familial Exudative Vitreoretinopathy (FEVR). Clinical Profile and Management
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1 December 2003 Shukla et al Familial exudative retinopathy 323 Original Article Familial Exudative Vitreoretinopathy (FEVR). Clinical Profile and Management Dhananjay Shukla, MS; Jatinder Singh, MS; Sudheer G, MS; Manoj Soman, DNB, FRCS; Rajesh K John, MSc; Kim Ramasamy, DNB; Namperumalsamy Perumalsamy, MS, FAMS Purpose: To report our experience with the diagnosis and management of Familial Exudative Vitreoretinopathy (FEVR) in a predominantly older Indian population.. Methods: This prospective interventional non-comparative case series included 38 patients of FEVR and their 23 family members. The diagnosis was established by clinical examination, fluorescein angiography and family screening. Prophylactic photocoagulation/cryotherapy or surgical treatment was done depending on the severity of the disease. Results: The mean age of the patients was 23.6 years. The fundus/fluorescein angiographic findings in 116 eyes of our 61 patients (6 eyes phthisical) were as follows: forty eight (41.4%) eyes had only peripheral avascular zone, 8 (6.9%) eyes had peripheral new vessels, and 35 (30.1%) eyes had retinal detachments (RD) 10 (8.6%) exudative, 5 (4.3%) tractional and 20 (17.2%) rhegmatogenous. Prophylactic photocoagulation or cryotherapy was done in 34 eyes for retinal holes, local exudative detachments and bleeding new vessels. All the eyes retained stable vision over a mean follow-up of 16 months. Only 14 RDs were suitable for surgery: scleral buckling, vitrectomy or both. The reattachment rate was 85.7% (12 of 14) and the best-corrected visual acuity (BCVA) improved to 5/ 60 or better in 50% of these eyes over a 2-year follow-up. Conclusions: FEVR appears to be more common than reported. Timely diagnosis and intervention is essential in view of the lifelong progression of the disease, late exacerbations, frequent involvement of family members, and poor surgical results. A high index of suspicion, family screening and early prophylaxis are recommended to prevent avoidable blindness from this underdiagnosed disease. Key Words: Familial exudative vitreoretinopathy, fluorescein angiography, peripheral avascular zone, retinal detachment, prophylaxis Indian J Ophthalmol 2003;51: Familial exudative vitreoretinopathy (FEVR) is a hereditary retinal vascular disorder first described by Criswick and Schepens in They reported six patients from two families with fundus changes remarkably similar to those seen in retinopathy of prematurity (ROP), but had no history of premature birth or perinatal complications. The major ocular manifestations included peripheral neovascularisation, peripheral retinal traction with temporal dragging, falciform folds, retinal detachment and lipid exudation. Retina Vitreous Service (DS, JS, SG, MS, KR, NP), and Dept. of Biostatistics (RKJ), Aravind Eye Hospital & Postgraduate Institute of Ophthalmology, Madurai, India. Proprietary Interest: None Correspondence to Dr. Dhananjay Shukla, Aravind Eye Hospital & Postgraduate Institute of Ophthalmology, 1 Anna Nagar, Madurai , Tamil Nadu, India. <daksh@aravind.org> Manuscript received: ; Revision accepted: Two years later, Gow and Oliver reported a large pedigree of FEVR and concluded that the inheritance pattern was autosomal dominant. 2 They also proposed a three-stage classification. Canny and Oliver were the first to describe fluorescein angiographic findings in FEVR, and demonstrated that the primary abnormality was a cessation of peripheral vascular growth and not vitreoretinal traction as originally believed. 3 Laqua modified Gow and Oliver s classification by including fluorescein angiographic findings at each level. 4 In the largest published series to date, van Nouhuys reported the clinical features, complications and propensity for platelet aggregation in 106 patients of FEVR. 5 Because of its frequently asymptomatic course and diversity of signs, FEVR is often unrecognised or diagnosed incorrectly. It can resemble many ocular conditions, depending on the stage of the disease at presentation and the patient s age. Much has been learned about the natural history, genetics and phenotypic expressions of the disease. Despite many advances, the pathogenesis and management of this condition remains uncertain. We report the largest series 323
2 324 INDIAN JOURNAL OF OPHTHALMOLOGY Vol. 51 No. 4 on FEVR from India in a relatively older population, highlighting the clinical features of the disease, diagnostic dilemmas, and management options at various stages of the natural history. Materials and Methods Between February 1999 and July 2002, we examined 61 patients with FEVR. A careful history of premature birth and perinatal complications, ocular or systemic disease as well as family history were noted. A detailed pedigree chart was prepared for each patient and patients were asked to bring family members for examination. The best-corrected Snellen visual acuity and refractive status were recorded. The anterior segment was examined by slitlamp biomicroscopy and intraocular pressure was recorded with applanation tonometry. All patients were examined using the indirect ophthalmoscope with and without red free light and with scleral depression. The posterior pole was examined using a 78 or 90 dioptre lens. Fluorescein angiography was performed on all patients. Children who could not cooperate were examined under anaesthesia. Fluorescein angioscopy was done in these patients. Clinical staging of the eyes with FEVR was done according to the classification scheme proposed by Gow and Oliver, modified by Laqua. 2,4 Prophylactic laser photocoagulation or cryopexy was done for retinal holes, peripheral telangiectasia with exudative detachments, and bleeding peripheral new vessels. All rhegmatogenous retinal detachments (RRDs) were operated. Nonrhegmatogenous retinal detachments (NRRDs) were operated when they extended posteriorly towards the posterior pole. The surgical modality (primary scleral buckling, primary vitrectomy, or combined procedure) depended on the nature of detachment and the extent of proliferative vitreoretinopathy (PVR). After surgical or prophylactic intervention, patients were reviewed at 1, 3 and 6 months and further surgical intervention was done as and when required. All other patients who did not undergo any treatment were asked to follow up yearly. Results Sixty-one consecutive patients of FEVR belonging to 38 families formed the database of the study. Their mean age was 23.6 years (range 2 to 55 years), with 40 males and 21 females. Thirty-four of the 38 index (primarily presenting) patients came with diminution of vision in either or both eyes. One presented with a squint while 3 index patients came with unrelated complaints. The remaining 23 (37.7%) patients were detected by screening the families of 13 index patients. At presentation, 24 (63.2%) index patients and 21 (91.3%) family members had a best corrected visual acuity of 6/12 or better in at least one eye. Four patients (including one family member) had visual acuity of less than 6/60 in the better eye. The mean age of these patients with poor visual acuity was 16 years (Table 1). Six eyes were phthisical. Since the cause of phthisis could not be determined categorically, they were excluded from analysis. Of the Table 1. Age (in years) versus visual acuity in the better eye Age (in years) Visual acuity in the better eye 6/6 6/12 6/18 6/60 <6/ (n=12) (n=19) > 20 (n=30) Total (n=61) remaining 116 eyes, 2 were hypermetropic (> +1.0 D), and 46 (39.66%) were myopic ( -1.0 D). 28 (24.14%) eyes had myopia of more than 6 dioptres. Anterior segment examination showed pseudoexotropia (positive angle Kappa) secondary to macular ectopia in 12 (10.3 %) eyes, clinically significant posterior subcapsular cataract in 4 eyes and neovascular glaucoma in two eyes. Forty eight (41.4%) of the 116 eyes had no abnormality except the peripheral avascular zone (Figures 1,2). Peripheral neovascularisation was observed in 8 (6.9%) eyes (Figure 3). These included two patients (aged 7 and 8 years) with bilateral involvement. Vitreous haemorrhage was seen in 2 eyes. Non-rhegmatogenous retinal detachments (NRRDs) involving the posterior pole were observed in 15 (12.9%) eyes. Ten of these 15 eyes had predominant exudative component (Figure 4), while 5 were predominantly tractional (Figure 5). Rhegmatogenous retinal detachment (RRD) was present in 20 (17.2%) eyes including 3 patients with bilateral involvement. In all the RRDs, causative breaks were atrophic holes in the peripheral avascular retina. Retinal breaks without RRD were present in 20 (17.2%) eyes, including both eyes of 3 patients. Macular ectopia ( Figure 6) was observed in 12 (10.3%) eyes (Table 2). Our 61 patients had the following stages of FEVR in the better eye: 31 (50.8%) stage 1, 12 (19.7%) stage 2 Table 2. Salient clinical features of FEVR (n=116)* Features No. of eyes (%) Avascular zone only 48 (41.4%) Extraretinal neovascularisation 08 (6.9%) Exudative RD 10 (8.6%) Tractional RD 05 (4.3%) Rhegmatogenous RD 20 (17.2%) Retinal breaks without RRD 20 (17.2%) Retinoschisis 01 (0.9%) Macular ectopia 12 (10.3%) *6 eyes with phthisis were excluded 324
3 December 2003 Shukla et al Familial exudative retinopathy Figure 1. Fundus photograph of the periphery showing the characteristic peripheral avascular zone with abrupt cessation of the vasculature; Figure 2. Fluorescein angiogram showing the peripheral avascular zone, acute-angle branching of peripheral vessels, brush-like anastomosis and shunts at the border of avascular zone, representing stage I disease; Figure 3. Fluorescein angiogram of the periphery showing leaking new vessels, representing stage II disease; Figure 4. Fundus photograph showing exudative retinal detachment. Note the underlying massive exudation and the straightening of the vessels; Figure 5. Fundus photograph of the posterior pole showing tractional retinal detachment with underlying exudation; Figure 6. Fundus photograph of the posterior pole showing temporal dragging of the macula and the disc /8/03, 12:14 PM
4 326 INDIAN JOURNAL OF OPHTHALMOLOGY Vol. 51 No. 4 and 18 (29.5%) stage 3. Of the presenting patients (index cases), 16 (42.1%) had stage 1, 10 (26.3%) had stage 2 and 12 (31.6%) had stage 3 FEVR in the better eye. Six patients were 10 years, 21 patients were 20 years and the remaining 11 patients were in the intermediate age range. Incidence of severe disease (stage 3) in the better eye was 50% (3/6) in the youngest and 24% (5/21) in the oldest age group. Asymmetrical presentation of FEVR (eyes in different stages of disease in same patient) was observed in 19 (31.2%) patients but there was no difference in incidence of asymmetry among the various age groups. Twenty-nine patients (34 eyes) needed treatment for the sequelae of FEVR. Seventeen patients (20 eyes) required prophylactic laser photocoagulation or cryopexy; and 12 patients (14 eyes) required surgical treatment (scleral buckling / vitrectomy / combined surgery). Photocoagulation was the preferred prophylactic modality (15 eyes) and cryotherapy was reserved for patients with hazy media and non-dilating pupils (5 eyes). Prophylactic treatment was done for retinal breaks (16 eyes), peripheral exudative detachment with telangiectatic vessels, either alone (2 eyes) or with new vessels (1 eye), and for new vessels with vitreous haemorrhage (2 eyes). One patient had a retinal hole as well as new vessels that required peripheral scatter laser photocoagulation. Four patients were lost to follow-up after treatment. The others remained stable for the duration of follow-up (mean: 16.4 months; range, 2-40 months) (Table 3). A total of 35 retinal detachments were seen: 20 rhegmatogenous, 5 tractional (TRD), and 10 exudative (ERD) detachments (Table 2). Ten RRDs and 4 ERDs were considered inoperable. Four detachments (2 TRDs; 2 ERDs) had spontaneously settled and were limited anterior to the equator. Of the 14 retinal detachments which underwent surgical intervention, 10 were rhegmatogenous, 3 tractional and one exudative. Seven eyes underwent primary scleral buckling alone, 3 underwent primary pars plana (lens sparing) vitrectomy and 4 underwent combined scleral buckling and vitrectomy with gas/oil tamponade. One progressive TRD was treated by only scleral buckling to relieve the vitreoretinal traction. This patient maintained 6/6 vision in the operated eye over a long follow up (30 months). Four eyes (3 patients) required two or more surgeries. The reattachment rate was high (10/12 cases). One patient was lost to follow-up. For the duration of followup (23.8 months, range 4 40 months), the retina remained attached in the rest of the patients. The final corrected Snellen visual acuity was 5/60 or better in 7 of 14 eyes (Table 3). Discussion We describe a prospective interventional noncomparative case series of 38 patients with FEVR and their family members. The diagnosis was suspected clinically and confirmed angiographically by the typical features of the disease (Table 2). Family history of disease and screening of family members aided the diagnosis in Table 3. Prophylaxis and surgical treatment Treatment Mean age Presenting Indication (n) Mean follow up Final retinal Final visual modality (Range) visual acuity (Range) status (n) outcome Laser 26.9 yrs 6/6 6/36 Break (12) 13.8 months Stable Stable (Barrage/scatter) (13-55 yrs) ERD+NVE (1) (2-40 months) (n= 15) NVE+VH (1) No follow up (4) Break+NVE+VH (1) Cryopexy 14.8 yrs 6/6 5/60 Break (3) 24 months Stable Stable (n= 5) (9-30 yrs) ERD (2) (8-36 months) SB 23.7 yrs 6/9 PL RRD (5) 23.6 months Attached (5) 6/6 3/60 * (n= 6) (8-46 yrs) TRD (1) (4-36 months) Detached (1) No Follow up (1) PPV 26 yrs 6/18 PL TRD 23 months Attached 1/60, 6/9 (n= 2) (22-30 yrs) (6-40 months) SB+PPV 27.5 yrs 6/24 PL RRD 6 months Attached PL (n= 2) (9-46 yrs) ERD 40 months Attached 6/12 Multiple surgeries 24.3 yrs 4/60 PL RRD 20.8 months Attached (3) 6/18 PL* (n= 4) (8-35 yrs) (11-38 months) Detached (1) * Visual outcome in successful reattachments n number of eyes; ERD exudative retinal detachment; TRD tractional retinal detachment; RRD rhegmatogenous retinal detachment; SB scleral buckling; PPV pars plana vitrectomy; NVE peripheral neovascularisation; VH vitreous hemorrhage; PL perception of light 326
5 December 2003 Shukla et al Familial exudative retinopathy 327 some cases. There are 3 major classifications of FEVR. The classification proposed by Gow, Oliver 2 and Laqua 4 is most often quoted. 6-8 Hence, we used this staging system. Miyakubo et al 9 described a grading scheme based on the retinal vascular pattern. They divided FEVR into five types depending on the size and shape of avascular zone, neovascular and cicatricial complications. The third classification is by Pendergast and Trese. They proposed a system similar to the International Classification for Retinopathy of Prematurity (ICROP) with five stages in the progression of the disease and three zones to describe the extent of the disease. 10 This was essentially a surgically oriented grading system with emphasis on more severe stages. None of these classifications is without limitations. In the classification of Miyakenbo et al, 9 the first three types appeared very similar. In classification of Pendergast and Trese, the early features of disease are omitted. Additionally, Schepens argues that the disease, with its variable penetrance and protean presentations arrested at different stages, does not lend itself to classification. 11 While any classification of FEVR does have inherent difficulties, we believe that a grading system is better than no system at all. The differential diagnosis of FEVR essentially depends on the stage of the disease. The important differential diagnoses are retinopathy of prematurity (ROP), high myopia, Eales disease, Coat s disease, juvenile retinoschisis, persistent hyperplastic primary vitreous (PHPV), and toxocariasis. Patients with ROP will have a history of prematurity and perinatal complications and will develop vascularisation of the retinal periphery in the majority of eyes after involution of the disease. 7 High myopia may mimic stage 2 of FEVR; fluorescein angiography however does not show the typical peripheral fundus features of the latter (vide infra). The vessels in Eales disease show inflammatory sheathing; exudation and macular ectopia are not seen. 12 Coat s disease is typically unilateral, has male predilection and shows no evidence of vitreoretinal traction. 6 Juvenile retinoschisis is usually bilaterally symmetrical, affects only male children, has typical foveal schisis, and peripheral new vessels with exudation are rare. 7,8 PHPV is also unilateral, and usually associated with microphthalmia. 6 Toxocara granuloma in children is typically unilateral and there is associated vitritis and uveitis. Other less common differential diagnoses are incontinentia pigmenti and Norrie s disease. It has been proposed that the phenotypes of X-linked FEVR and Norrie s disease may result from the defects in the same gene. 13 The classic and most common mode of inheritance of FEVR is autosomal dominant, 2,4,8,14-16 with near 100% penetrance but with marked variation in expressivity. 14,16 Li and colleagues recently mapped the locus for dominant FEVR to the long arm of chromosome X- linked recessive inheritance and sporadic cases have also been reported. 5,9,13 An autosomal dominant trait was manifest in 8 of 36 familial cases in our series. Our patient profile, with mean age of 23.6 years (range, 2-55 years), was older than most other studies with a mainly pediatric population. 1,8-10 Only 12 of 61 (19.7%) total patients [and 6 of 38 (15.8%) index patients] were younger than 10 years. The higher age of patients explains good presenting visual acuity in at least one eye (6/12 or better) in 75% of our patients. Also, asymmetric disease is known to be more common in older patients (30% patients in our series). 7,14 A peripheral zone of avascular retina is the sine qua non for the diagnosis of FEVR. 7 Presence of bilateral peripheral avascular zones, at least temporal, was the minimum criterion for the diagnosis of FEVR in our series. In 41% of our cases, they were the only manifestation of FEVR. Rhegmatogenous retinal detachment was more common than nonrhegmatogenous retinal detachment in our series. All the retinal breaks, with / without retinal detachment, were atrophic holes, with one exception of a horse-shoe break. Though these lesions do not warrant prophylactic treatment, 18 we considered it safe to prophylactically treat most of the retinal holes. No treated break progressed to detachment during the follow-up. Despite the universal finding of peripheral avascular zone, all eyes don t require prophylactic scatter laser photocoagulation or cryopexy. Peripheral neovascularisation (NVE) or exudative detachments are reported to be the main indication for prophylaxis by most investigators. 6,8,10,11 But the results of treatment have not been consistent. The value of prophylactic treatment remains controversial and most authors suggest treatment only for progressive lesions (NVE / NRRD), mainly for young children. 5-8, 14 We considered bleeding new vessels in adults and angiographically leaking new vessels in young children, a firm indication for peripheral scatter photocoagulation. The high incidence of retinal detachment (35/116, 30% of the eyes) was surprising in view of the older patient population. Fourteen (40%) of these were inoperable. This underlines the importance of prophylactic treatment for retinal holes in these cases. Though overall anatomical success rate was high for both scleral buckling and vitrectomy (83%), visual outcome was superior following scleral buckling. This could probably be due to presence of less severe disease in these eyes as suggested by others. 5, 8, 11 Most recent studies show comparable reattachment rates, the visual outcome depends on the type of RD, severity of disease and patient age. 10,19,20 This case series draws attention to the adult presentation of FEVR. We confirm the observation of some authors that FEVR is a lifelong disease, and events like neovascularisation, vitreous haemorrhage and retinal detachments may occur at any age after varying periods of apparent quiescence. 7,8,11 327
6 328 INDIAN JOURNAL OF OPHTHALMOLOGY Vol. 51 No. 4 The study has certain limitations. The genetic pattern of the disease could not be ascertained due to incomplete family screening. Due to referral patterns of our clinic, our study had no infants and very few children. This also led to imbalanced groups so that statistically significant conclusions could not be drawn from intergroup analysis. A longer, well balanced study with comparable paediatric and adult patients is required to draw valid conclusions on the effect of age on the progression and prognosis. The follow up was not consistently long in cases that did not require intervention. Since FEVR is a lifelong disease, a much longer follow-up would be preferable to study the natural history of the disease. Finally, the staging system was unsatisfactory. A more broad-based and universal classification system is needed which places adequate emphasis on both juvenile and adult patterns of the disease. This study reports the largest Indian series of FEVR. Our experience suggests that FEVR may be more common than reported, and careful family screening may reveal asymptomatic cases. Early detection by a high index of suspicion is essential in view of its progressive nature, unfavourable visual outcome of surgery, and efficacy of prophylactic measures in forestalling disease progression. References 1. Criswick VG, Schepens CL. Familial exudative vitreoretinopathy. Am J Ophthalmol 1969;68: Gow J, Oliver GL. Familial exudative vitreoretinopathy: an expanded view. Arch Ophthalmol 1971;86: Canny CL, Oliver GL. Fluorescein angiographic findings in familial exudative vitreoretinopathy. Arch Ophthalmol 1976;94: Laqua H. Familial exudative vitreoretinopathy. Graefes Arch Clin Exp Ophthalmol 1980;213: van Nouhuys CE. Signs, complications and platelet aggregation in familial exudative vitreoretinopathy. Am J Ophthalmol 1991;111: Ebert EM, Mukai S. Familial exudative vitreoretinopathy. Int Ophthalmol Clin (Vol 33, Spring, No. 2) 1993;23: Regillo CD. Familial exudative vitreoretinopathy. In: Guyer DR, Yannuzzi LA, Chang S, Shields JA, Green WR (editors). Retina Vitreous Macula, Philadelphia. W.B. Saunders Company; Vol 1, pp Benson WE. Familial exudative vitreoretinopathy. Trans Am Ophthalmol Soc 1995;93: Miyakubo H, Hashimoto K, Miyakubo S. Retinal vascular pattern in familial exudative vitreoretinopathy. Ophthalmol 1984;91: Pendergast SD, Trese MT. Familial exudative vitreoretinopathy : Results of surgical management. Ophthalmol 1998;105: Schepens CL. Non-rhegmatogenous retinal detachment from other causes. In: Schepens CL, Hartnett ME, Hirose T (editors). Retinal detachment and allied diseases, 2nd edition., Butterworth Heinemann, pp Biswas J, Sharma T, Gopal L, Madhavan HN, Sulochana KN, Ramakrishnan S. Eales disease an update. Surv Ophthalmol 2002;47: Fullwood O, Jone J, Bunday S. X-linked exudative vitreoretinopathy: Clinical features and genetic linkage analysis. Br J Ophthalmol 1993;77: Ober RR, Bird AC, Hamilton AM, Sehmi K. Autosomal dominant exudative retinopathy. Br J Ophthalmol 1980;64: Feldman EL, Norris JL, Cleasby GW. Autosomal dominant exudative vitreoretinopathy. Arch Ophthalmol 1983;101: van Nouhuys CE. Dominant exudative vitreoretinopathy and other vascular developmental disorders of the peripheral retina. Doc Ophthalmol 1982;54: Li Y, Fuhrmann C, Schwinger E, Gal A, Laqua H. The gene for autosomal dominant familial exudative vitreoretinopathy (Criswick Schepens) on the long arm of chromosome 11. (Letter). Am J Ophthalmol 1992;113: Wilkinson CP. Evidence-based analysis of prophylactic treatment of asymptomatic retinal breaks and lattice degeneration. Ophthalmology 2000;107: Ikeda T, Fujikado T, Tano Y, Tsujikawa K, Koizumi K, Sawa H et al. Vitrectomy for rhegmatogenous or tractional retinal detachment with familial exudative vitreoretinopathy. Ophthalmology 1999;106: Glazer LC, Maguire A, Blumenkranz MS, Trese MT, Green WR. Improved surgical treatment of familial exudative vitreoretinopathy in children. Am J Ophthalmol 1995;120:
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