Peter Hovland,
Shizuo Mukai,
Tatsuo Hirose
INTRODUCTION
Retinopathy of prematurity (ROP) - the proliferation of abnormal retinal blood vessels that occurs in premature infants and its pathologic sequelae - has been and continues to be an important cause of childhood blindness. Since 1942 when ROP was first recognized by Terry,[1,2] advances have been made both in understanding the etiology and characterizing the pathological progression of ROP, as well as establishing interventions timed to prevent or even reverse visual loss. Progress in the field has been based on key observations, well designed studies, and improvements in surgical techniques and technology.
The pathophysiology, diagnosis and management of acute ROP are covered extensively in Chapter 318. In this chapter, the concentration will be on advanced stages of ROP, including retinal detachment and preretinal fibrovascular proliferation, and their management.
RETINAL DETACHMENT IN ROP
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Key Features: Forms of Retinal Detachment |
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Tractional RD - Most common form observed in acute ROP Exudative RD - More common in chronic forms Rhegmatogenous RD - rarely noted in acute ROP. May be iatrogenic |
Patients with ROP have an increased lifetime risk for various forms of retinal detachment. In acute ROP, the tractional RD is most commonly observed. Tractional RDs originate at the ridge, at which point myofibroblasts pull centripetally and anteriorly toward the lens in a purse-string configuration. Once retinal detachment occurs, it can progress rapidly. Peripheral detachments posterior to the ridge can proceed to total retinal detachment within a day, and total detachments can become closed funnels within a week in very active vasoproliferative ROP. Peripheral retinal cryoablation during the acute phase of ROP appears to reduce by half the incidence of childhood RD.[3] Despite prophylactic ablative therapy RD can occur. Hartnett and McColm report[4] that factors associated with progression to stage 4 RD following laser ablative therapy included the absence of clear vitreous, ridge elevation of at least six clock hours, and plus disease encompassing two or more quadrants.
In contrast, exudative retinal detachments occur less commonly in acute ROP. These occur as a result of plasma leakage from abnormal neovascular tufts, with subsequent subretinal fluid accumulation. Chronic vitreoretinal traction to the retinal vessels may play some role in causing exudation. Exudative RD may occur more frequently in the adult patient with ROP. The fundus usually shows smooth retinal detachment with yellow subretinal exudates. Abnormal vessels such as small angiomas with retinal hemorrhage can be seen. Focal and diffuse pigmentary changes indicate the chronic nature of the detachment. Chronic exudation may result in anterior segment pathology (ischemia, cataract, neovascularization) and posterior segment dysfunction by exudative RD or macular edema. Shallow exudative detachments of avascular retina anterior to the ridge do not normally require surgical intervention.[5] The abnormal neovascular tufts may be treated with cryotherapy to reduce fluid leakage (Fig. 136.1). Newer therapies such as intravitreal antivascular endothelial growth factor (anti-VEGF) compounds, which decrease vessel permeability may be of some use in treating this condition in the adult.
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FIGURE 136.1 (a) Fundus photograph of stage 3 moderate retinopathy of prematurity. A large ridge with extraretinal fibrovascular proliferation is visible. Peripheral to this ridge is a large area of avascular retina. (b) Fundus photograph of the same eye immediately after ablation of the avascular retina anterior to the ridge by diode laser coagulation. In this case, laser coagulation was applied in three to four contiguous rows anterior to the ridge without treating all the way up to the ora serrata. Treatment was as effective as cryotherapy. |
Rhegmatogenous detachments are seen only rarely in acute ROP and are usually iatrogenic at this age. In contrast, they are the most common retinal detachment seen in older children and adults with cicatricial ROP. During early adolescence, patients may be at an increased risk of developing RD.[6] Many of these cases are long-standing and are not noticed by the patient until subretinal fluid expands into a large enough area to produce visual symptoms. The detached retina is usually thin, with multiple small equatorial breaks hidden by the vitreous membrane. These late-occurring rhegmatogenous detachments may be repaired with scleral buckle (SB) or vitrectomy techniques,[7,8] though successful repair of late-occurring RD is more likely to require several procedures.[9] Because of the increased risk of developing RD, regular eye examinations are recommended in high-risk or preverbal children with a history of ROP.[8]
SCLERAL BUCKLING
Scleral buckling can be used to treat milder forms of traction retinal detachment in acute ROP.[10-13] Retinal detachment in posterior zone ROP in which the ridge is located very posterior to the equator showing a large attached avascular retinal anteriorly can not be treated with a buckle. Beyrau and Danis reported[14] that primary scleral buckling in 22 eyes of 14 infants with stage 4a ROP resulted in successful maintenance of attachment of the macula in 70% initially, and useful vision in 60%. Greven and Tasman[15] reported successful reattachment with scleral buckling in 13 of 22 eyes with stage 4b and stage 5 (open-open configuration) ROP. More than 50% of patients had satisfactory anatomic results in most other studies.[5,16-18] Prost reports[19] that a modified SB encircling procedure was used in 121 eyes of 68 infants with stage 5 ROP, resulting in a 52% total (and 24% partial) reattachment rate. However, only 20% of the operated eyes were judged by the author to have useful vision. Scleral buckling is also used in the treatment of rhegmatogenous detachment in ROP eyes.[20]
The timing or even indication of surgery in the management of stage 4a detachment is controversial because many cases of partial nonrhegmatogenous detachments often reattach spontaneously particularly when there is neither active vasoproliferation nor plus disease. However, since the duration of retinal detachment influences prognosis, as the retina becomes atrophic after relatively brief periods of detachment,[18] scleral buckling should be considered early in progressive traction detachments and in large exudative detachments. There is less agreement about surgery in traction detachments that do not involve the posterior pole. Until a randomized, controlled trial of surgery for stage 4 ROP is performed, the decision to undertake surgery in these controversial cases must be determined on an individual basis.
Cryotherapy or laser therapy is often performed at the time of retinal detachment surgery, especially in traction or exudative cases with continued active neovascularization. Cryotherapy can be applied to the active neovascular ridge if the detachment is shallow. The scleral depression made by a cryoprobe can reach the ridge. The laser can be applied on the ridge on the buckle after external drainage of subretinal fluid and after the retina is attached. Cryotherapy or laser is unnecessary if there is no active neovascularization. When the traction is effectively released additional treatment to create chorioretinal adhesive force is not required (athermal buckling). A silicone band is used to encircle the globe along the site of the ridge. External drainage of subretinal fluid is usually necessary to indent the sclera effectively without raising the intraocular pressure due to the SB. Greven and Tasman[15] recommended scleral dissection in some patients and fluid drainage in nearly all patients.
The silicone band in such small eyes may impair ocular growth. How the tightly applied band affects the intraocular circulation and future development of vision is not known. Yet there remains disagreement as to whether to cut or remove the band at some time after scleral buckling surgery. Machemer and deJuan[17] do not routinely remove the band unless there is clinically apparent retardation of ocular growth. Greven and Tasman[15] also leave the band in place in most cases. McPherson and coworkers[18] and Orellana[5] state that the band ideally should be transected 3-6 months postoperatively to permit normal ocular growth.
PROPHYLACTIC SB
The uniform loss of macular vision in infants who have undergone therapeutic scleral buckling for stage 4b or stage 5 ROP has been noted by Mintz-Hittner and Kretzer.[21] They proposed two reasons for the poor outcome in these infants. First, rapid ocular growth occurs after development of ROP in these infants, whereas the area of vascularized retina does not increase. The distance between the temporal optic disk and the center of the macula remains 4 mm from preterm to adulthood. Thus, traction is exaggerated with ocular growth. Second, the retinal interaction with retinal pigment epithelium is critical to normal retinal development. An interruption of the normal configuration for even a few days may result in irreversible dysmorphic changes. These considerations led to the proposal that these extremely low-birth-weight infants be treated with a prophylactic SB at the time of cryotherapy for threshold ROP. Macular detachment or ectopia did not develop in 80% of eyes in these infants with zone 1 disease who were treated with a prophylactic SB. This approach to managing ROP has not become widely adopted, however. When the ridge is located posterior to the equator, as in zone I ROP it is better to approach by vitrectomy.
VITRECTOMY
Vitrectomy may be considered when scleral buckling fails, a high retinal detachment is present, media opacification by vitreous strands or hemorrhage occurs, or a fibrous membrane is observed behind the lens. Vitrectomy is considered as a primary procedure for retinal detachment in posterior zone ROP. With advances in surgical approaches to ROP, the retina can be reattached in an apparently unsalvageable eye (Fig. 136.2). Optimal results are achieved by meticulous removal of proliferative membranes; this may be assisted by intraoperative injection of triamcinolone into the eye to help in the visualization of the vitreous and membranes. Sometimes scleral buckling is combined with vitrectomy surgery.[18,22-36] There are two distinct approaches to vitrectomy in advanced ROP: the closed technique which is more commonly used for stage 4a, 4b, and stage 5 when the retina is well visible; and the 'open sky' method which is typically reserved for stage 5 ROP when the retina is pulled well behind the lens, including cases with leukocoria.
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FIGURE 136.2 (a) Photograph of the eye of a 16-month-old boy with stage 5 retinopathy of prematurity. The retina is totally detached and pulled forward toward the lens. The vessels of the detached retina are seen through the thin retrolental fibrous membrane. (b) A B-scan image of a stage 5 ROP detachment. (c) Interpretive drawing of the B-scan. (d) Fundus photograph of a former stage 5 ROP eye after successful open-sky reattachment. |
CLOSED VITRECTOMY WITH LENS REMOVAL
Charles,[22] Machemer and deJuan,[17,23] Trese,[28] and Fuchino and associates[34] pioneered closed vitrectomy (CV) techniques for management of ROP. The small size of the eye and extensive proliferation necessitated several modifications of the standard closed-vitrectomy approach used in adult eyes. When the retina is pulled so far anteriorly that it abuts the lens, the instruments must be inserted through the iris root or anterior ciliary body to avoid entering the subretinal space. Typically, a two-port system is used with an irrigating light pipe in one port. Alternatively, infusion can be placed in the anterior chamber after removal of the lens (three-port). Machemer and deJuan[17] recommended the corneal limbal approach to avoid tearing of the anteriorly pulled retina by the instrument as it is inserted through the pars plicata. This has the advantage of keeping the anterior chamber deep and the retina back, especially when instruments are exchanged through the surgical wound. The disadvantage of the anterior chamber infusion is that the infusion fluid can push the lens posteriorly and pressure the detached retina behind it causing a retinal dialysis. Sector iridectomy or iris spreading hooks may be required for visualization. After lensectomy, the epiretinal-retrolental membrane is dissected by delamination or segmentation with scissors or microvitreoretinal (MVR) blade and removed with the vitrectomy instrument. Additional ports may be made to allow for more complete dissection and removal of the membranes. Hyaluronic acid is used to aid in the dissection by Trese[28] and others.
LENS-SPARING VITRECTOMY
In recent years the lens-sparing vitrectomy (LSV)[37-43] technique has been advanced in the treatment of retinal detachment, particularly in posterior zone type ROP in which the ridge is located posterior to the equator. It usually is performed in eyes that have been treated previously by laser photocoagulation or cryotherapy. The technique usually can not be applied effectively in cases where the ridge is very anterior and the membrane to be cut is located very peripherally. The patient benefits by remaining phakic. This technique is more challenging if the membrane to be cut and cleaned is anterior to the equator due to the relatively large size of the crystalline lens at this age. In questionable cases, one may plan the LSV to start. The sclerotomy is through the pars plicata or pars plana and not through ablated retina. Occasional touch of the lens with an intraocular instrument does not lead to cataract postoperatively. However, if the membrane could not be removed effectively without lensectomy, the lens can be sacrificed at that point.
Despite technical difficulties, several groups have reported successful case series. Trese and coworkers reported[37] a series of successful LSV treatment of Stage 4a. They report that of 23 eyes tested in an average follow-up of 3.5 years, 83% had normal appearance of the macula, and most patients had an average visual acuity of 20/80. Moshfeghi and coworkers report[38] that a single LSV for treatment of stage 4a resulted in complete retinal reattachment in 30 of 32 eyes (94%). In a nonrandomized retrospective comparison of SB to LSV for treatment of stage 4a, Harnett[39] found that LSV was a more successful initial procedure (72%), than SB (31%). Hubbard and coworkers reported[40] that a two-port LSV performed in 37 eyes of 24 patients with a stage 4 ROP resulted in complete retinal reattachment in 84% of 4a and 92% of 4b at a median follow-up of 13 months. Capone and Trese performed a two-port, LSV in 40 eyes of 31 patients with a reported 90% reattachment at a follow-up mean of 12 months.[41] Holz and coworkers report[42] that a three-port LSV technique allowed for a 85% successful reattachment in 108 eyes of 102 consecutive patients with stage 4a and 4b. They also report[43] 94% sustained lens clarity on a mean follow-up of 32 months. Despite these successes, many of the stage 4a cases may not advance and may not require surgery.
OPEN-SKY VITRECTOMY
The open-sky vitrectomy (OSV) technique was developed by Schepens in 1981.[25] It addresses the difficult surgical scenario of stage 5 ROP where the retina is drawn anteriorly by the retrolental membrane, which makes CV difficult. It also allows for an approach to cases with corneal opacification. To initiate the OSV, A Flieringa ring is sewn in place to preserve the shape of the globe during surgery. Then the cornea is removed with a 7- to 8-mm trephine and stored in culture medium during surgery.[44] The eye is irrigated with chilled balanced salt solution during the procedure to minimize fibrin formation.
Iridotomies made at the 12 and the 6 o'clock positions in the past have been replaced by iris retractors (e.g., 'perfect pupil' designed by John Milverton). Intracapsular extraction of the crystalline lens is performed using a cryoprobe. This allows direct visualization of the transparent anterior hyaloid and the fibrous, white, retrolental membrane. Incision on the retrolental fibrous (RLF) membrane starts far in the periphery usually in front of the ciliary body until the surface of the retina is reached. The RLF membrane is circumcised. Then the dissection is continued centrally to the opening of the funnel of the detachment. In order to make space inside of the funnel larger and make the location of the adhesion of the membrane to the retina visible hyaluronic acid is injected into the mouth of the funnel. In order to view the inside of the funnel better, flat round coverglass, 5 mm in diameter, is used to touch the surface of the hyaluronic acid filling the funnel. The dissection continues toward the disk. The fibrous mass filling the funnel of detached retina is cut near the optic nerve head and removed en bloc.
The iridotomies, if made, are closed with 10-0 polypropylene sutures, and the corneal button is replaced with 10-0 nylon sutures. Hyaluronic acid is injected to deepen the anterior chamber, as well as into the open mouth of the funnel. When the intraocular pressure goes up and the retina is found to be still highly elevated, the subretinal fluid is drained externally and hyaluronic acid is further injected into the vitreous cavity. At the end of the surgery the detached retina should be placed away from the back of the iris. No effort is made to directly reattach the retina by intravitreous injection.
Scleral buckling was performed by Hirose and colleagues[45] 4-8 weeks later if the retina showed no sign of reattachment. They reported a 39% anatomic success rate using this technique. Eyes with the closed-closed configuration had a 29% reattachment rate; all other eyes had reattachment rates of greater than 60%. McPherson and coworkers[30] had a 22% anatomic success rate with open funnels and an 11% success rate with closed funnels using the open-sky technique, whereas Tasman and associates[31] had a 35% anatomic success rate.
The preoperative presence of subretinal hemorrhage in stage 5 confers a poor prognosis. Ultrasonographic evaluation of stage 5 eyes should be performed prior to OSV. Steidl and Hirose, in a retrospective review[46] of 426 eyes of 263 patients who underwent OSV for stage 5 ROP, identified the presence of subretinal organization (bands, plaques, or diffuse hemorrhage) to be associated with incomplete retinal reattachment or retinal attachment without any useful vision.
COMPARISON OF OSV TO CV
The relative rates of success of CV versus OSV depend in part on the selection of cases. The advantage of the closed technique is the avoidance of removal and replacement of the corneal button. The disadvantages include the need for a pars plicata or iris root entry site because of the extreme anterior displacement of the retina and the difficulty maneuvering vitrectomy instruments within the small closed space of the premature infant eye. The use of multiple ports may allow for more complete removal of membranes. Incomplete removal of residual peripheral membranes results in only 'partial' reattachment.
Reported disadvantages of the open-sky technique include increased complexity of postoperative management because of the need for a corneal graft, prolonged hypotony, and a longer operating time. In experienced hands, however, operative time is less than 2 h.[45] Choroidal detachments are rare, and corneal endothelial cell-density changes little.[47] The advantages of the open-sky technique are the excellent visualization of the pathologic process and the direct access to the retrolental membrane. This makes more complete removal of peripheral membranes possible and less residual traction on the retina when it is reattached at the posterior pole. Some cases that would be inoperable by the closed technique can be repaired using the open-sky method. The main drawback of open-sky vitrectomy is the difficulty in exposing the posterior pole in eyes with a narrow funnel. The use of additional hyaluronic acid can be helpful in these situations.
TIMING OF VITRECTOMY
The optimal timing of vitrectomy remains to be determined. In patients with stage 5 ROP, a session of cryotherapy or laser therapy before surgery may promote quiescence of the vasoproliferative process, allowing earlier repair of the detachment, but this is difficult to perform with the presence of partial retinal detachment, and impossible when the detachment is total or nearly total.[48] Chong and colleagues[49]recommended operating as soon as plus disease has regressed. At this stage, although the traction retinal detachment is typically still an open funnel, adhesion of the membrane to the retina is very strong, making complete removal of the fibrous tissues from the retina extremely difficult. There is also an increased chance of reproliferation because the membrane is still continuing to form and there is a higher chance of hemorrhage.
Thus, the potential functional advantage of operating early must be weighed against the increased difficulty of extracting adherent membranes and the increased postoperative hemorrhage and fibrin production (with development of secondary membranes) if vitrectomy is performed too soon. Use of the recently available anti-VEGF agents may serve as a useful adjuvant in reducing neovascularization and vascular permeablility prior to vitrectomy. Perhaps an approach consisting of intraocular anti-VEGF injection followed few to several days later by vitrectomy and membrane removal may work. One must always weigh the risk of systemic absorption of any anti-VEGF drug used in the eye.
The timing of vitrectomy in relation to the progression of stage 4a and 4b disease is likely very important as well. Hartnett[50] identified preoperative factors which correlated with outcome of vitrectomy and SB procedures performed on stage 4 and 5 eyes which had received previous laser ablation. In eyes which failed first procedures, vitreous haze or organization and plus disease were found to be significant in stage 4 eyes, while 6 clock hours of ridge elevation and plus disease were found to be significant in stage 5 eyes. Hartnett recommends additional laser be performed before surgery in eyes manifesting neovascularization or plus disease. The optimal timing of LSV with respect to laser ablation is unknown. An Argentine group[51] reports in a small series of eight patients, that those patients who had received laser treatment prior to LSV had more organization of the vitreous which made surgery more difficult, with the previously untreated patients faring better.
The optimal time for surgery may be after 6 months of age but before the patient is 1 year old. One may operate earlier if the eye has been treated with cryotherapy or photocoagulation and the fundus shows no sign of active vasoproliferation. Even when surgery is delayed for years, it may be worth attempting repair in some cases because ambulatory acuity has been obtained postoperatively in patients with long-standing retinal detachment up to 3 years of age.[45]
COMPLICATIONS OF VITRECTOMY
Iatrogenic retinal breaks produced during vitrectomy surgery are extremely difficult to close. Some peripheral breaks may be closed by scleral buckling, but breaks formed posterior to the ridge or in the posterior pole in infants with ROP are impossible to close either with scleral buckling or with air-fluid exchange and internal drainage of subretinal fluid probably due to the inability to completely release the traction by vitrectomy or retinal foreshortening, or a combination of both. Other factors that can make ROP surgery more difficult and associated with higher risk include the presence of a persistent hyaloid artery,[52] intraocular bleeding, multiple circular retinal folds, and tilting of the funnel toward one quadrant.[45]
Although anatomic reattachment can be achieved in eyes with severe disease using either technique, vision has been disappointingly poor.[49,53] Machemer and deJuan[17] reported an anatomic success rate of 64% and a functional success rate of 43% in stage 4 cases. Patients with stage 5 ROP do not fare as well. Stage 5 cases with the open-open configuration have the best prognosis; the closed-closed configuration is least likely to result in recovery of useful vision.[26,32-36] However, the limited vision, which may detect the movement of objects, for example, which develops after reattachment of stage 5 ROP, is very useful for activities of daily life and as such very enhancing to the quality of life in the affected young children.
In the cryo-ROP study, the visual outcome of infants who progressed to stage 5 retinal detachment was studied retrospectively.[35,54] Surgery was performed by several different surgeons using different techniques. There were no standardized preoperative criteria for undertaking vitrectomy, and patients were not randomized. The configuration of detachment (open vs closed funnel) was not specified. The anatomic success rate was 28% at 1 year and 21% at 5.5 years in operated eyes, with a functional success rate of 1-3%. Although data were not specified for all eyes that did not undergo vitrectomy, one of the 10 eyes described had spontaneous resolution of the retinal detachment. Eyes that underwent vitrectomy had a lower incidence of glaucoma and shallow anterior chamber compared with unoperated eyes. The rates of corneal opacity, hypotony, and vitreous hemorrhage were similar in the two groups. Thus, although surgical approaches to ROP are meeting with improved rates of retinal reattachment in ROP, the visual outcomes to date indicate that the emphasis must remain on prevention of retinal detachment.[35,54]
SUMMARY
Interest in ROP has grown along with the increasing incidence of the disease resulting in many advances for treament of acute ROP. Treatments of advanced stages of acute ROP have also been refined, with properly timed cryotherapy or laser photocoagulation preventing retinal detachment and meticulous vitrectomy techniques successfully removing traction forces. Smaller gauge (25 G and 23 G) vitrectomy techniques are being pioneered, yet have not been widely adapted to ROP surgery, though ultimately they may be found to be advantageous when operating on the smaller eyes of infants. Adjuvant to surgery such as the use of recently developed anti-VEGF agents may make surgical success higher in addition to being potentially useful in treating the acute stages of ROP.
The improved anatomic success rates of vitreoretinal surgery have been confounded by disappointingly poor visual function. Still, surgery should be pursued when indicated, as even attaining hand-motion visual acuity allows many patients to remain ambulatory, and anatomic success may avoid the need for enucleation. Further modifications of treatment protocols, with an emphasis on preventing retinal detachment, will be necessary before significantly better acuity can be retained in eyes with severe stages of this devastating disease.
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