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TENT-SHAPED RETINAL DETACHMENTS IN OF PREMATURITY

MICHAEL J. SHAPIRO, MD, JOSHUA ALPERT, MD, RAHUL T. PANDIT, MD

Background: Most retinal detachments associated with retinopathy of prematurity (ROP) are radial, segmental, or circumferential with cicatricial extraretinal fibrovascular proliferation (EFP) at the apex of the detachment. This report describes peculiar tent- shaped retinal detachments that developed among with ROP. Methods: An observational case series consisting of 9 patients and 13 eyes with tent-shaped retinal detachments. Their morphology, clinical baseline, surgical course, and final retinal status were extracted from medical records. Results: Eight had simple tent-shaped retinal detachments, three had a double tent- shaped , one had a chevron-based retinal detachment, and one had a star-shaped retinal detachment. Each case had a disk based stalk that extended to the apex of the traction retinal detachment and continued anteriorly; 12 stalks inserted in the retrolental space and 1 terminated in the mid vitreous. Six eyes were stage 4A, two eyes were stage 4B, and five eyes were stage 5. surgery was performed on 11 eyes. Surgery resulted in retinal attachment in nine eyes, and two remained detached. Conclusion: Tent-shaped retinal detachments are seen in patients with ROP. A stalk should be sought in evaluation of these eyes. Vitreous surgery focused on relieving this traction is often successful. 26:S32–S37, 2006

n his description of the pathogenesis of late stages of been frequently noted.3–6 The dissection of the stalk Iretinopathy of prematurity (ROP), Machemer pre- was a well-documented step in membranectomy for sented observations about the development of retinal ROP. Eller et al. studied the association of the persis- detachments in ROP.1 He proposed a mechanical tent hyaloid artery with ROP and suggested that it was schema that showed that contraction of stage 3 ROP a likely part of the disturbance of vasculogenesis and could account for the progression to segmental, cir- angiogenesis that describe the advance stages of cumferential, and radial retinal detachments. He con- ROP.7 They also speculated that the hyaloid system cluded with a general statement that “All retinal could provide a scaffold for fibrovascular prolifera- changes seen in ROP can be explained by proliferation tion. The stalk also had practical implications since of tissue originating in the shunt area.” Extending when using the open sky technique this stalk may these observations, the international classification of increase the intraoperative hemorrhage,4 and using ROP further described the retinal detachment config- closed vitrectomy, aggressive surgery on the stalk urations.2 may lead to posterior retinal breaks.6 Recently, the The presence of a stalk originating on the optic disk stalk was identified as one of the many vectors of nerve in retinal detachments associated with ROP has traction involved in development of retinal detach- From the University of Illinois at Chicago, UIC Center. ment in ROP.8 Although frequently observed, the The authors have no proprietary interests in the material de- identification of a disk stalk as a sufficient cause of scribed. Reprint requests: Michael J. Shapiro, MD, UIC Eye Center, retinal detachment separate from the extraretinal fi- 1905 W. Taylor, Chicago, IL 60612; e-mail: [email protected] brovascular proliferation (EFP) was often impossible

S32 TENT-SHAPED RETINAL DETACHMENTS IN ROP ● SHAPIRO ET AL S33

Table 1. Case Summary Estimated Birthweight Gestational Detachment Structural Eye Patient (g) Age (wk) Location Eye Zone Treatment Morphology Stage Vitrectomy Outcome 1 1 692 25 Inborn L 1 Laser Tent 4B LSV Attachment 2 2 550 24 Inborn R 1 Laser Tent 4A LSV Attachment 3 Inborn L 1 Laser Tent 4A LSV Attachment 4 3 560 24 Inborn L 2 Laser Tent 4B LV Attachment 5 4 646 26 Outborn R 2 Laser Tent 4A None Attachment 6 L 2 Laser Tent 5 LV Attachment 7 5 620 23 Outborn L 2 None Star shaped 5 LV Attachment 8 6 1220 25 Outborn R 1 Laser Tent 5 LV Detachment 9 L 1 Laser Double tent 4A LSV Attachment 10 7 553 23 Outborn R 1 Laser Double tent 5 LSV Attachment 11 L 1 Laser Double tent 5 LSV Phthisis 12 8 655 26 Outborn R 1 Laser Tent 4A LSV Attachment 13 9 1800 NA Outborn L NA None Chevron 4A None Unchanged

LSV ϭ sparing vitrectomy; LV ϭ lensectomy vitrectomy. because the vitreoretinal relationships were dominated the standard. Preoperative evaluation focused special by the EFP. attention on the retinal examination. The form of the In this article, we describe infants with ROP that retinal detachment was studied. The EFP was consid- presented with tent-shaped retinal detachments rather ered for extent, location, vascularity, and its position than radial, segmental, or circumferential folds. This relative to both the retina and the lens. Postoperative tent-shaped morphology is associated with persistent follow-up ranged from 6 months to 6 years and in- fetal vasculature (PFV),9 and very different from the cluded patient history, examination with indirect oph- retinal detachments generally seen in ROP. Careful thalmoscope, and examination (when age inspection revealed that these retinal detachments appropriate). were not a result of the contraction of the extraretinal fibrovascular proliferation, but rather the contraction Results of a hyperplastic disk stalk probably related to the Tent-shaped retinal detachments were found in 13 hyaloid artery. Identification of these unexpected ret- eyes of 9 patients with ROP (Table 1). All patients inal detachment configurations is helpful for diagnosis were born prematurely and also had severe ROP in the by ophthalmologists who examine or treat ROP. contralateral eye. One was first examined as an adult; of the remainder, five infants were seen during the Materials and Methods active phase and three infants were referred during the Tent-shaped detachments were defined as a traction cicatricial phase of ROP. The birthweights ranged retinal detachment with five criteria: one, a well de- from 550 g to 1800 g. Among the pediatric cases fined small apex and relatively broad base; two, retinal (excluding Patient 9) the average birthweight was detachment apex well within the vascularized retina; 611 g. The infants were born at estimated gestational three, tubular fibrous stalk connected to the retinal ages that ranged from 23 to 26 weeks with a mean of apex; four, stalk emanating from the disk; 24.5 weeks. Three of the infants were inborn. Five and five, traction from the stalk directed into central were referred for treatment. The one adult, ex-prema- vitreous. Records of patients with traction retinal de- ture neonate, was referred for long-term observation. tachments from ROP seen in a pediatric retina practice The retinal detachments evolved under supervision were reviewed. Cases with a documented tent-shaped among the inborn patients. All but two eyes among the retinal detachment were selected. Eyes with a radial or infants reached threshold before development of reti- circumferential fold or detachment as the predominant nal detachment. Eight were in zone 1 and four were in morphology were excluded. All eyes that had an optic zone 2. All threshold eyes were treated with laser nerve disk stalk discovered during surgical dissection photocoagulation. were also excluded. There were four configurations of retinal detach- The baseline characteristics were recorded, includ- ments. Eight eyes showed simple tent-shaped retinal ing the estimated gestational age and birthweight. The detachment (Figure 1). In these eight eyes, fibrous history was reviewed using the postmenstrual age as elements originated on the optic disk and connected S34 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES ● VOL 26 ● NO 7 ● SUPPLEMENT 2006

Fig. 3. Left, the ultrasound of a tent-shaped detachment with a stalk seen extending from nasal to the disk to the retrolental space. Right, an ultrasound corresponding to Figure 2 shows a hyperplastic hyaloid artery extending into the central vitreous. Fig. 1. A simple tent-shaped retinal detachment accompanied by a mild circumferential fold from cicatricial stage 3 retinopathy of pre- maturity. The stalk connects from the disk to the apex of the retinal detachment within the vascularized retina and then extends into the and 9 the EFP involuted and exerted no traction on the vitreous and retrolental space. retina. Since the media were clear, ultrasounds were only occasionally performed. In one eye the ultra- along the retina surface to the apex of the retinal sound showed the stalk extending from adjacent to the detachment within the vascularized retina, and in- nerve to the retrolental space and in the second eye it serted anteriorly in the central vitreous, anterior vitre- extended from the disk to the central vitreous (Figure ous, or posterior lens (Figure 2). In eight eyes there 3). Connection to the condensed anterior vitreous was were accompanying peripheral segmental folds due to noted in five eyes, and in one a connection to vitreous contraction of persistent stage 3 ROP. In Cases 1, 7, 8, that bridged across a circumferential fold was re- corded. Among all the eyes with tent-shaped retinal detachments, the area of retinal detachment was lim- ited by the disk and the laser induced chorioretinal atrophy. Some vascular and retinal dragging was al- ways present among cases with tent-shaped retinal detachment. In five eyes more complicated retinal detachment configurations developed. One eye presented with a tent-shaped detachment with a chevron-shaped base (Figures 4 and 5). This shape reflected the straighten- ing of the arcade blood vessels proximal and distal to the apex forming a chevron as a result of the anterior traction at the apex. Three eyes presented with a double tent with the stalk connected to two retinal detachment apices, one nasal and one temporal. A fifth eye showed a thick stalk with tight connection 360 degrees and presented with a star shape (Figure 6). Fig. 2. Preoperative 130 degree Retcam photograph of the right eye of Peripapillary fibrosis was noted in two eyes (Figure Patient 8. The retina within the dotted line was detached. The large arrow shows the apex of the simple tent-shaped retinal detachment. The 7). was seen in two eyes. Using small arrows show the path of the stalk from the optic disk to the retinal the international classification of ROP six eyes detachment apex and anterior into the midvitreous. The superior arcade reached stage 4A, two eyes reached stage 4B, and five vessels show mild dragging toward the apex. The periphery shows chorioretinal atrophy from laser ablation and complete involution of eyes reached stage 5. Initial was per- stage 3 Rush disease. formed on three eyes. In two cases the buckle reduced TENT-SHAPED RETINAL DETACHMENTS IN ROP ● SHAPIRO ET AL S35

Fig. 4. The artist presents a horizontal perspective of a tent-shaped detachment with a chevron shaped base also seen in Figure 5. The Fig. 6. A star-shaped retinal detachment with 360 degree connections stalk originated at the disk and inserted on the inferior arcade vessels of the retina elevated and drawn towards the stalk with draping of the with elevation and straightening of the blood vessels both distal and retina. proximal.

the peripheral component of the traction retinal de- tachment; however the central traction retinal detach- ment progressed in all three cases. Vitrectomy with membranectomy was performed on 11 eyes. Seven eyes underwent lens sparing vitrectomies; repeat lens sparing vitrectomies were performed in two eyes, and four eyes had combined lensectomy and vitrectomy

Fig. 5. A tent-shaped retinal detachment with a chevron base. The origin is seen at the disk and the stalk is connected to the vessels near the disk. The apex is seen along the inferior arcade blood vessels labeled as “on end view of anterior extent of stalk.” The proximal and Fig. 7. Fibrosis of the optic nerve head with infiltration of vitreoretinal distal portions of the vessels are elevated, straightened, and dragged so interface. Striae as seen inferiorly are a common manifestation and may that the detachment base forms a chevron. The blood vessel distal to indicate the alterations that precede the connection of the stalk to the apex forms the crest of the detachment more peripherally. retina. Inferior nasal there was a disk stalk. S36 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES ● VOL 26 ● NO 7 ● SUPPLEMENT 2006 procedures. Two eyes failed treatment and nine reat- months gestational age. The hyaloid artery itself tached. The two cases with surgical failure were pre- closes at 8 months and regresses soon afterwards.12 operatively classified as stage 5 ROP. The neonatal cases in this report evolved in the setting of extreme prematurity, generally followed complete Discussion laser treatment, and were either inborn or early refer- rals. In our cases both retinal vasculogenesis and hya- Machemer identified the key factors in the devel- loidal artery involution were disturbed. opment of retinal detachments from ROP as the con- The development of the normal eye in humans and traction of the circumferential shunt with stretching most mammals includes a chronological overlap and and elevation of the retina, the traction from intravit- proportional relationship between retinal vasculariza- real proliferation, and the position of the shunt along tion and vascular involution of the primary vitreous. the anterior posterior axis of the eye.1 The resultant In many animal models of ROP the hyaloidal system vitreoretinal configurations in eyes with a radially persists and in some the hyaloidal blood vessels pro- symmetric distribution of disease centered on the disk liferate. Bischoff et al displayed persistent hyaloidal are circumferential folds and funnel-shaped detach- vessels in the mouse models of ROP using scanning ments. In eyes with radially asymmetric distributions electron microscopy.13 They described the hyaloid of fibrovascular shunt tissue the retina developed ra- vasculature as a high resistance passive system and the dial folds, segmental folds, incomplete funnels, eccen- retinal vasculature as a low resistance active system. trically displaced funnels, and spiral funnels.10 Rec- They suggested that oxygen exposure constricts the ognizing the additional pathologic forces responsible retinal vasculature and raises the hydrostatic pressure for retinal detachment and understanding the vector in the retinal vessels, driving the blood into the func- combinations that lead to the different patterns of tionally closed hyaloidal vasculature. This diversion detachment is especially important in determining the of blood causes a persistence and distention of the effective surgical approach since the membranes often tunica vasculosum lentis and vasa hyaloidea propria. obscure much of the retina.8 In this report, we de- Larrazabal and Penn showed the arborizing hyaloid scribed eyes with ROP that developed tent-shaped system with fluorescein angiography of newborn rats retinal detachments. Recognition of this uncommon recovering in room air after 14 days of 80% oxygen pattern of retinal detachment may help during moni- exposure.14 They demonstrated an extensive and tor- toring of the ROP patient and surgical management. tuous hyaloid vascular system as well as tortuosity of The tent-shaped retinal detachments reported were the major retinal vessels. This model may be the most most similar to the typical radial folds described in similar to the neonatal human condition. Berkowitz et ROP. However, they presented distinct features. First, al used a noninvasive method, carbogen enhanced in each case the tractional element was a stalk ema- MRI, to study the hyaloidopathy in newborn rats.15 nating from the disk rather than a flat, pleated, or They found that the functional volume of hyaloidal bunched sheet that originated from the EFP. Second, circulation occupies a larger volume of the vitreous in the apex of the tent-shaped retina detachment was well ROP rats compared with controls. These findings con- within the vascularized retina rather than at the junc- firm and refine the essential finding of Patz16 and tion of the vascular and avascular retina. Third, the although not in complete agreement, build on the stalk extended from the apex centrally into the mid- work of Ashton.17 Bischoff also suggested a role for vitreous, anterior vitreous, and posterior lens rather the persistent vasculature in some cases of retinal than the peripheral vitreous, , and periph- detachment. Indeed, the cicatrization of the hyaloid eral lens. Some of the cases revealed retinal traction vascular system was a major contributor in the beagle from both the disk stalk and extraretinal fibrovascular model of ROP retinal detachment.18 proliferation. However, we excluded the cases in Finally, we reported special cases in which the which major EFP was associated with extensive relationship between the stalk and the tent-shaped opaque vitreous proliferation to emphasize the stalk retinal detachments were isolated and easy to appre- component as a sufficient cause of retinal detachment. ciate. More frequently, a complex mix of forces must Sporadic persistent fetal vasculature syndrome is be analyzed and treated. We believe that early refer- quite rare, but findings of PFV are common among rals for failure of laser treatment may reduce the premature neonates.11 In normal eyes the primary complexity of the retinal detachments. If this is the vitreous vasculature stops growing at 10 weeks, and case, observation of the hyperplastic disk stalk as a the branch vessels slowly atrophy. The posterior vector contributing to retinal detachment may achieve branches of the hyaloid trunk, vasa hyaloidea propria, greater importance for diagnosis and treatment of late regress first and are completely atrophic by 8.5 stages of ROP. TENT-SHAPED RETINAL DETACHMENTS IN ROP ● SHAPIRO ET AL S37

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