Current Eye Research, Early Online, 1–8, 2015 ! Informa Healthcare USA, Inc. ISSN: 0271-3683 print / 1460-2202 online DOI: 10.3109/02713683.2014.999947

ORIGINAL ARTICLE

Recurrence After Primary Pterygium Excision: Amniotic Membrane Transplantation with Fibrin Glue Versus Conjunctival Autograft with Fibrin Glue* Ebru Toker and Muhsin Eraslan

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Department of Ophthalmology, Marmara University Medical School, Istanbul, Turkey

ABSTRACT Purpose: The aim of the present study was to compare the surgical results and recurrence rates of primary pterygium excision with conjunctival autografts versus amniotic membrane grafts fixated with fibrin glue. Materials and methods: In this prospective study, 73 eyes of 65 patients who had undergone conjunctival autograft group (CAG) (n:37) or amniotic membrane group (AMG) (n:36) after pterygium excision were evaluated. Fibrin glue was used for the fixation of grafts in both groups. The patients were followed up for 12 months. Postoperative complications were recorded. The rate of recurrence was defined as the primary outcome measure. Results: In the CAG, partial dehiscence of the graft was observed on the nasal edge on postoperative day 1 in two (5.4%) eyes that healed with secondary re-epithelialization at week 1. Twelve (32.4%) eyes showed a yellowish-orange or hemorrhagic edema of the graft on postoperative day 7 that spontaneously resolved in 1 to 3 weeks. In the AMG, partial dehiscence and folding of the amniotic membrane occurred in two (5.5%) eyes. Two eyes (5.4 %) in the CAG developed corneal recurrence and five eyes (13.8%) in the amniotic membrane graft group developed recurrence; one limbal (2.7%), four corneal recurrences (11.1%) (p = 0.25). Conclusion: Fibrin glue is a safe and effective method for attaching conjunctival or amniotic membrane grafts for wound closure following pterygium surgery. Although the results were not statistically significant, amniotic membrane grafting using fibrin glue seems to have a higher pterygium recurrence rate compared with conjunctival autografting. Keywords: Amniotic membrane, conjunctival autograft, fibrin glue, pterygium

INTRODUCTION

Alternatively, the defect can be covered with a conjunctival autograft, conjunctival limbal graft, conjunctival rotation autograft, conjunctival flap or amniotic membrane.2–4 Although lower recurrence rates have been observed with antifibrotic adjunctive treatments, they can be associated with severe sightthreatening complications, including late-onset scleral necrosis, corneal perforation, microbial infection, endophthalmitis, glaucoma and cataracts.5–8 Due to these potential complications, conjunctival autografting is widely used in the management of

Pterygium recurrence is a major complication after pterygium surgery. High recurrence rates (19.4–75%) observed after simple bare sclera excision require treatment with more complex surgical techniques. These include excision followed either by adjunctive treatment with beta-irradiation, mitomycin C, 5-flurouracil or daunorubicin. Recently, bevacizumab started being used as an adjuvant, regarding its antiangiogenic effects following ptergium surgeries.1

Received 12 December 2013; revised 4 December 2014; accepted 8 December 2014; published online 2 April 2015 *This study was presented in part at the American Academy of Ophthalmology Annual Meeting, Chicago, September 2010; USA. Correspondence: Dr Ebru Toker, Department of Ophthalmology, Marmara University School of Medicine, Istanbul, Turkey. Tel: +905326946212. E-mail: [email protected]

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pterygium.9,10 Pterygium excision with conjunctival autografting has significantly reduced recurrence rates. It is also associated with fewer complications and has become the surgical procedure of choice.11–14 However, this technique has some limitations. It is technically more demanding than bare sclera excision, and learning curves or differing surgical skill levels may play a key role in the recurrence rates (ranging between 2 and 39%).15 In some cases, it is difficult to cover large defects with conjunctiva following extensive removal of large ptergia. Also, the need to reserve the conjunctiva for future filtrating surgery in glaucoma patients is another limitation of the CAG technique.16 The antiinflammatory, antifibrotic and antiangiogenic properties of the amniotic membrane, as well as its ability to promote the differentiation and migration of epithelial cells, make it useful in the surgical management of pterygia.17 For these reasons, amniotic membrane grafts are being used as an effective alternative to conjunctival autografts in pterygium surgery.18–23 On the other hand, AMG has its own limitations regarding procuring, processing, preserving amniotic membrane and the need for screening microbial inoculations.24 The most common method of securing conjunctival autografts or the amniotic membrane to the sclera is by suturing. Recently, fibrin glue was reported as being a successful alternative to conventional suturing in ocular surgery.25 Numerous previous studies suggested that the use of fibrin glue in pterygium surgery with a conjunctival autograft reduces surgery time, improves postoperative comfort, avoids suture-related complications, and results in a lower recurrence rate compared with suturing.25–42 The current literature contains only a few reports in which fibrin glue was used to attach amniotic membrane grafts in pterygium surgery.16,30,43,44 To the best of our knowledge, surgical results of these two sutureless grafting techniques have not been compared previously. Therefore, the aim of the present study was to compare pterygium recurrence rates and surgical results following primary pterygium excision with conjunctival autografts versus amniotic membrane grafts fixed with fibrin glue.

MATERIALS AND METHODS In this prospective study, we evaluated the recurrence rate and surgical results in patients with primary pterygium, who had undergone pterygium excision with conjunctival autografts or amniotic membrane grafts fixed with fibrin glue between February 2008 and January 2011. Forty-three eyes of 40 patients had undergone conjunctival autografting and 39 eyes of 34 patients undergone amniotic membrane grafting after pterygium excision but 37 eyes of 34 patients in

the CAG and 36 eyes of 31 patients in the AMG completed the one-year follow-up and were included in the study. Approval was obtained from the Ethics Committee of our institution, and full informed consent was obtained from all the patients in the study. The inclusion criteria were cosmetically significant pterygium or clinically significant pterygium presenting with ocular irritation, inflammation or reduced vision. Exclusion criteria included age 518 years, other concurrent ocular or lid pathology, glaucoma, ocular hypertension, pregnancy, and known hypersensitivity to any component of fibrin glue. After a full ophthalmological examination was performed, the patients were randomly assigned to one of the two groups. Randomization was accomplished using a random number table. After pterygium excision, fibrin glue was used to attach a conjunctival autograft in group 1 and an amniotic membrane graft in group 2. All surgery was performed by a single surgeon (E.T.). The pterygia were graded according to the system used by Tan et al.14: atrophic/grade 1, episcleral vessels under the body of the pterygium are not obscured and clearly visible; intermediate/grade 2, all other pterygia not falling into grade 1 or grade 3; fleshy/grade 3, episcleral vessels are totally obscured.

Fibrin Glue Preparation Tisseel (Baxter, Vienna, Austria) is a fibrin tissue adhesive consisting of a combination of fibrinogen and thrombin. When admixed, it forms an adhesive fibrin network. The Tisseel kit consists of two vials containing solvents and two vials containing powders. The fibrin glue was prepared according to the manufacturer’s instructions. Prior to surgery, the Tisseel vials were first heated to 37  C using a Fibrinotherm device (Baxter). Lyophilized sealer protein concentrate powder (72–110 mg/ml), which is composed of human-extracted fibrinogen, plasminogen, fibronectin and factor XIII, was reconstituted with bovine-derived aprotinin (2000–3750 KIU/ml) solvent and warmed. While this solution was stirred, the second component was prepared by injecting the contents of the calcium chloride solution (36–44 mmol/ ml) into the human-extracted thrombin (400–625 IU/ ml) powder, which was then warmed. In the presence of calcium, thrombin mediates the conversion of fibrinogen to fibrin to create a stable clot. Aprotinin prevents premature fibrinolysis. The solutions were placed in two separate syringes. The two components of the fibrin glue were applied sequentially during the procedure, instead of mixing with the Duploject syringe (dual injection system). The preparation time of this glue was about 20 min. A fibrin clot was formed within 10 s. Adherence was generally stable within 2–3 min. Current Eye Research

Pterygium Recurrence After Grafting with Fibrin Glue 3

Surgical Technique

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After instillation of topical proparacaine HCl (AlcaineÕ ; Alcon Laboratories, Fort Worth, TX), 2% lignocaine HCl with 0.001% adrenaline (JetokaineÕ , Adeka IS, Samsun, Turkey) was injected subconjunctivally into the pterygium body. A limbal peritomy was performed approximately 3–4 mm posterior to the limbus and down to bare sclera. The limbal and then the corneal portions of the pterygium were removed with blunt and/or sharp dissection (no. 0064 Beaver blade). All the subconjunctival tissues were then removed and bleeding was controlled using minimal cautery. The denuded corneal surface and limbus were smoothed with a burr.

Conjunctival Autograft In the conjunctival autograft group, the dimensions of the scleral bed were measured with calipers. A sizematching conjunctival-free graft was harvested from the superior bulbar conjunctiva of the same eye. The intended graft area was marked with a gentian violet marker pen. Lignocaine HCl 2% with 0.001% adrenalin was injected under the conjunctiva to separate it from the underlying Tenon’s capsule to facilitate the sole dissection of the conjunctiva. The conjunctiva was carefully dissected away from the Tenon’s capsule, excised, and then placed epithelial side down on the corneal surface. After the scleral bed was dried, 1–2 drops of fibrinogen component was placed on the scleral surface. The graft was then flipped over and positioned onto the scleral surface with care to maintain the correct orientation (the anterior margin positioned directly adjacent to the limbus). Then, a thin layer of thrombin solution was injected under the graft. The graft was rapidly smoothed out against the episclera. Gentle pressure was applied over the graft, and the edges of the graft and the recipient conjunctiva were pinched with a non-toothed forceps for better attachment. Excess adhesive was squeezed out with a sponge. After the glue had dried, excess glue was excised with scissors and removed by forceps.

Amniotic Membrane Graft In the amniotic membrane graft group, a cryopreserved amniotic membrane, obtained from Istanbul University Lions Eye Bank, was first cut (oversized, approximately 4–6 mm larger than the size of the scleral bed) and then the nitrocellulose filter paper was peeled off. The fibrinogen solution was applied to the scleral surface. The amniotic membrane was spread over the denuded area with the stromal surface facing down, and the free margins of the membrane were tucked under the surrounding !

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recipient conjunctiva. A thin layer of thrombin solution was injected under the membrane with a cannula introduced from the sides. Finally, the edges of the recipient conjunctiva were attached to the membrane by applying the components of the glue sequentially.

Conclusion of the Surgery A combined antibiotic/corticosteroid ointment was applied to the ocular surface, and a pressure patch was applied. The patch was removed on the first day after the surgery, and steroid and antibiotic drops were administered 4–6 times daily, then tapered and discontinued during the following 4–6 weeks. The patients were instructed not to rub their eyes. The surgical time was recorded, starting from the insertion of the lid speculum to its removal at the end of the surgery.

Patient Evaluation and Follow-up Postoperative examinations were performed at 1, 7 and 14 days and then again at 1 month. Subsequently, the patients were followed monthly from the 1st month to the 4th month, then bimonthly from the 4th month to 1 year. The anterior segment, the integrity of the autograft and the amniotic membrane, and the donor site were evaluated by slit-lamp biomicroscopic examination. None of the patients used medications like doxycycline and/or cyclosporine A in the preoperative or postoperative period.45,46 Complications, such as graft dehiscence, graft retraction, subgraft hemorrhage and graft edema, were recorded. Recurrence was defined as any conjunctival fibrovascular extension to the limbus (limbal recurrence) or more than 1 mm onto the cornea (corneal recurrence). The rate of recurrence at 12 months was the primary outcome measure.

Statistical Analyses Statistical analyses were done with GrapPad Instat 6.0 software (La Jolla, CA, USA). Data are presented as mean (SD) or frequency (%). Fisher’s exact test was done to compare categorical data among the two groups. The Mann–Whitney U-test was used to compare continuous data. A p value less than 0.05 was considered statistically significant.

RESULTS Sixty-five patients [34 men and 31 women, with a mean age of 50.9 ± 13.8 years (range, 20–80 years)] completed the 12-month follow-up. All pterygia were

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nasally located. The preoperative patient data are summarized in Table 1. There was no statistically significant difference between the conjunctival autograft group and the amniotic membrane graft group regarding the age, sex, grade of pterygium and time of the year the surgery done.47,48 The mean surgical duration was 18.2 ± 3.4 (range, 14–26) min for the conjunctival autograft group and 15.9 ± 2.1 (range 12–22) min for the amniotic membrane graft group (p = 0.007). Two (5.4%) eyes in the conjunctival autograft group developed corneal recurrence at 4 and 8 months postoperatively, respectively (Figure 1). Both pterygia were graded as grade 2 before the surgery. Five (13.8%) eyes in the amniotic membrane graft group developed recurrence: 1 (2.7%) limbal at 2 months postoperatively and 4 (11.1%) corneal recurrences, 1 at 3 months, 2 at 4 months, and 1 at 8 months postoperatively. The recurrent pterygia were graded before the surgery as grade 2 in 2 eyes and grade 3 in 3 eyes. The difference in the overall recurrence rate and in the true corneal recurrence was not statistically significant (p = 0.26 and p = 0.42, respectively). All the patients with recurrences were followed for continued growth of fibrovascular tissue onto the cornea, and two of the patients had surgery again (conjunctival autograft with fibrin glue combined with intraoperative mitomycin C 0.02%). Pterygia did not recur again in any of the patients. There were no total graft dislocations or losses on the first postoperative day in either group. In two

(5.4%) eyes, partial dehiscence of the conjunctival autograft and conjunctiva were observed on the nasal edge on postoperative day 1 (Figure 2). Secondary re-epithelialization and spontaneous closure of the wound gap occurred in postoperative week 1. No recurrence was observed in these eyes. Twelve (32.4 %) eyes showed a yellowish-orange (three eyes) or hemorrhagic edema (nine eyes) of the autograft on postoperative day 7 that had not been present on postoperative day 1 (Figure 3). Spontaneous resolution of the edema occurred in 1–3 weeks. Mild graft retraction (1 mm) developed in one eye with autograft edema, and secondary re-epithelialization of the defect occurred, with no complications or recurrence. Complications, such as graft edema or subgraft hemorrhage, were not observed postoperatively in the amniotic membrane group. Partial dehiscence and folding of the amniotic membrane graft occurred in two cases. Excess membrane that folded over itself was trimmed off. Early retraction of the graft occurred at 2 weeks postoperatively in one eye and pterygium recurred at 3 months (Figure 4).

DISCUSSION Biological adhesives have been used in a wide range of ophthalmic procedures as an attractive alternative for sutures for many years. One of the major uses of these adhesives since their introduction in ophthalmic

TABLE 1 Preoperative data of conjunctival autograft and amniotic membrane graft groups. Conjunctival autograft with fibrin glue (n:37 eyes) Mean (SD) age Sex Male Female Pterygium grade Grade 1 Grade 2 Grade 3

52 (13.7) 18 16 4 (10.8%) 21 (56.7%) 12 (32.4%)

Amniotic membrane graft with fibrin glue (n = 36 eyes) 49.8 (14.1) 16 15 4 (11.1%) 18 (50.0%) 14 (38.8%)

p Value 0.45 0.78 0.68 0.96 0.70 0.70

FIGURE 1 Normal appearing conjunctival autograft on postoperative day 1 (A); fibrovascular tissue extending to the limbus on the inferonasal edge at postoperative month 2 (B); corneal recurrence at postoperative month 4 (C). Current Eye Research

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Pterygium Recurrence After Grafting with Fibrin Glue 5 surgery has been in pterygium surgery. Fibrin glue accelerates the normal process of fibrin formation by creating strong adherence of the graft to the underlying episclera within minutes of application. The strength of this adherence is maintained by the fibrous tissue that replaces the bridge between the transplanted tissue and the host.25 Evidence suggests that increased ocular surface inflammation during the postoperative period may increase the risk of pterygium recurrence.49,50 Suturing may cause additional trauma to the surgical site and up-regulate the post-operative reparative inflammation.37,51 Koranyi et al.28 proposed that the immediate adhesion of the entire graft provided by the glue may help to inhibit the proliferation of the fibroblasts of adjacent Tenon’s tissue and therefore contribute to reducing the recurrence rate. The extensive contact of the grafted tissue with the entire underlying surface, provided by the use of fibrin glue, facilitates earlier vascularization of the graft, and hence its viability. This more rapid healing process may prevent further fibroblast migration from adjacent tissues. We used a clinical slit-lamp grading scale developed by Tan et al. which is the most frequently used method for pterygium classification in literature.1,14–16,22,41,44

In the current study, patients were followed-up for one year, as nearly all postoperative recurrences occur within this time. Hirst52 reported that recurrences occur within 4 months in 50% of cases and within 1 year in 97% of cases. The recurrence rate we report for conjunctival autografts (5.4%) compares well with rates reported in previous studies.10,11,13,15,22 Pterygium recurrence rates after excision with sutured conjunctival autografting vary widely, but they range from 2 to 39%.2,3 The first prospective randomized study of pterygium recurrence rates that compare fibrin glue to suturing technique by Koranyi et al.27 showed lower recurrence rates when the conjunctival autograft was secured to sclera with fibrin glue (8%), rather than with a suture (20%) in a small group of patients. They later published a large retrospective study of 461 eyes with a longer follow-up (6–12 months). They reported a recurrence rate of 5.34% for the glue group and 13.8% for the suture group.28 Several other studies reported a recurrence rate of 0–4.5% with fibrin glue,31,34–36,38–42 and prospective randomized controlled studies showed lower longterm recurrence rates with fibrin glue compared to polyglactin or nylon sutures.31,35,38,41 However, in a prospective randomized study comparing long-term results of conjunctival closure with fibrin glue or sutures in pterygium surgery with a bare sclera

FIGURE 2 Partial dehiscence of the conjunctival autograft on the nasal edge (A); secondary re-epithelialization and closure of the wound gap at post-operative week 1 (B).

FIGURE 3 Edema of the conjunctival autograft on postoperative day 7. Yellowish-orange (A) or hemorrhagic (B) edema. !

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FIGURE 4 Early retraction of the amniotic membrane graft at postoperative week 2 (A) that progressed to recurrence (B) at 3 months.

technique combined with intraoperative mitomycin C, Bahar et al.33 reported a higher recurrence rate with fibrin glue (11.9%) compared to sutures (7.7%). The use of fibrin glue for attachment of amniotic membrane grafts has not been studied extensively. There is large variability among studies in reported recurrence rates of sutured amniotic membrane grafting for primary pterygium. Prabhasawat et al.13 noted that the recurrence rate for primary pterygium with amniotic membrane grafting was much higher than that obtained with conjunctival grafting: 10.9% versus 2.6%, respectively. A modification of the technique by Solomon et al.,18 with extensive removal of fibrovascular tissue combined with intra- and postoperative depot steroid injections, yielded a low recurrence rate of 3%. Some studies have reported unacceptably high recurrence rates (25%53, 40.954, 64%55) with the use of amniotic membrane grafting for the management of primary pterygium. However, other studies have observed no statistically significant difference in recurrence rates between amniotic membrane grafts and conjunctival autografts in the treatment of primary pterygia.19,22,23 The use of fibrin glue in attaching the amniotic membrane has been reported by Pfister and Sommers30 in two cases of primary and one case of recurrent pterygium. Later, in a prospective noncomparative case series, Jain et al.43 reported the use of fibrin glue for securing amniotic membrane grafts in 12 patients with primary pterygium. They noted that fibrin glue was successful in attaching the amniotic membrane grafts and reducing both the surgical time and postoperative discomfort. They observed grade 3 (limbal) recurrence in one patient within a follow-up of 1 year. More recently, Ku¨cu¨kerdo¨nmez et al.16 compared the results of amniotic membrane transplantation using fibrin glue versus vicryl sutures in primary pterygium surgery. The recurrence rate in the fibrin glue group (9.4%) was similar to that achieved by conventional suturing (10.5%). Our recurrence rate of 13.8% is slightly higher than that reported in the aforementioned studies with fibrin glue, but still lower than the rate observed in studies utilizing sutures for fixation. This reduction in recurrence may be attributed to less postoperative inflammation observed with

fibrin glue. Kheirkhah et al.44 evaluated the role of conjunctival inflammation at the 3rd or 4th week after intraoperative application of mitomycin C and amniotic membrane transplantation and showed that conjunctival inflammation was significantly reduced in eyes in which fibrin glue was used to attach the amniotic membrane grafts instead of sutures. To the best of our knowledge, our study is the first to compare the results of these two sutureless grafting techniques. The meta-analysis of Li et al.,56 which included five prospective randomized control studies, showed that the recurrence rate and postoperative unacceptable appearance rate observed in an amniotic membrane group seemed to be higher than in a conjunctival autograft group. Although not reaching statistical significance, the amniotic membrane group in our study seemed to have higher recurrence rates than the conjunctival autograft group. In our study, no sight-threatening complications developed. Previous studies have reported rare graft dehiscence or graft loss after using fibrin glue to secure conjunctival autografts. We observed partial dehiscence of the conjunctival autograft and conjunctiva on the nasal edge in two eyes, but this did not cause any problem. We believe that it is not necessary to reattach these nasal gaps with sutures or fibrin glue, as rapid re-epithelialization and closure of the wound gap occurred in one week, and no recurrence was observed during the follow-up. This belief is supported by the study of Dupps et al.57 They reported that a 2-mm wide (narrow strip) conjunctival autograft sutured to the sclera leaving a 2–3 mm zone of bare sclera between the graft and the anterior margin of the conjunctiva is effective in preventing pterygium recurrence. They proposed that an intervening bare sclera promotes active migration of epithelium over the bare sclera instead of passive implantation of epithelium on the donor conjunctiva that still retains Tenon’s tissue. The migrated epithelium over the bare sclera provides a barrier to fibrovascular proliferation by augmenting epithelialscleral adhesion. Fibrin glue has an extra advantage in this context because it produces a more continuous, smooth surface for the migration of normal epithelium. Current Eye Research

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Pterygium Recurrence After Grafting with Fibrin Glue 7 We observed conjunctival graft edema in 12 (32.4%) eyes at the 1-week postoperative visit that had not been present on postoperative day 1. This type of transient postoperative graft edema has been reported previously in 11.2–40.5% of cases.28,42,58 The appearance of edema coincides with the breakdown of the biodegradable fibrin glue and does not seem to adversely affect the healing process or cause recurrence. Previous comparative studies reported that the average surgery time for conjunctival autografts with fibrin glue ranges from 9.7 min to 27.8 min, which is significantly shorter compared to the time taken with sutures.27,29,33,35,36,38,41,58 The mean operation time in our study was 18.2 ± 3.4 min for the conjunctival autograft group and 15.9 ± 2.1 min for the amniotic membrane graft group (p = 0.007). The mean operation time was 2 min shorter, on average, with the amniotic membrane grafting. The time saving with the lack of need to harvest the donor conjunctiva is reasonable. A limitation of this study is the relatively small number of patients. The difference in the recurrence rate between the two groups did not reach statistical significance. The study might have been more robust with a larger number of patients. In conclusion, fibrin glue is a safe and effective method for attaching conjunctival or amniotic membrane grafts for wound closure following pterygium surgery. Although not found to be statistically significant, amniotic membrane grafting using fibrin glue seems to have a higher pterygium recurrence rate compared with conjunctival autografting.

DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. The authors have no financial interest on any of the materials mentioned in the study.

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Current Eye Research

Recurrence After Primary Pterygium Excision: Amniotic Membrane Transplantation with Fibrin Glue Versus Conjunctival Autograft with Fibrin Glue.

The aim of the present study was to compare the surgical results and recurrence rates of primary pterygium excision with conjunctival autografts versu...
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