Orbit, 26:513, 2007 Copyright c 2007 Informa Healthcare ISSN: 0167-6830 DOI: 10.

1080/01676830600972724

CLINICAL RESEARCH

Comparison of Three Methods for the Treatment of Pterygium: Amniotic Membrane Graft, Conjunctival Autograft and Conjunctival Autograft plus Mitomycin C.
Yasemin Arslan Katrcoglu, Ugur Emrah Altparmak, and Sunay Duman Department of Ophthalmology, S.B. Ankara Research & Training Hospital, Ophthalmology Clinics, Ankara, Turkey

Received 1 November 2005; Accepted 7 March 2006. Address correspondence to Yasemin Arslan Katrcoglu, Turan Gunes Bulvar, Urdun cad. 48. sok. Akasya evleri Sitesi, 2. blok B-14, Oran-Ankara, Turkey. E-mail: yaslankatircioglu@yahoo.com

ABSTRACT Objective: To compare three techniques combined with excision in the treatment of primary and recurrent pterygium: amniotic membrane transplantation, conjunctival autograft, and conjunctival autograft plus mitomycin C. Materials and Methods: Forty-nine eyes of 49 subjects (30 primary, 19 recurrent pterygium) were included in this study. Combined with excision, 25 eyes (18 primary, 7 recurrent pterygium) were treated with conjunctival autografts (Group 1), and 16 eyes (12 primary, 4 recurrent pterygium) were treated with amniotic membrane transplantation for the closure of the defect (Group 2). In 8 eyes (all recurrent pterygium) low-dose mitomycin C (0.02%) was applied topically to the defect area and a conjunctival autograft was applied thereafter (Group 3). The three groups were compared with regard to the recurrence of pterygium and the defect area requiring treatment. Results: The number and percentages of recurrence seen in groups 1, 2 and 3 were as follows: 4 (16%), 4 (25%), and 0(), respectively. For the treatment of primary pterygium cases, amniotic membrane closure and conjunctival autograft closure were comparable in effectiveness (p > 0.05). In the treatment of recurrent pterygium, there was no signicant difference between the three techniques (p > 0.05). Amniotic membrane closure and conjunctival autografts were equally effective for the treatment of both primary and recurrent pterygium (p > 0.05). The graft size was signicantly larger in the cases with recurrent pterygium (p = 0.016). Conclusions: Amniotic membrane closure and conjunctival autografts seem to be equally effective in the prevention of recurrence of primary pterygium. Conjunctival autografts combined with mitomycin C are as effective as the above two techniques to prevent recurrence in the treatment of recurrent pterygium. Due to the larger area of subconjunctival brosis, a larger defect area is created after the excision of pterygium tissue and a larger graft is needed to close this defect in recurrent pterygium. This factor can guide the surgeon during the
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planning of the surgery to choose the most appropriate technique for closure of the defect.
KEYWORDS Pterygium surgery; mitomycin c, conjunctival autografts
amniotic membrane,

INTRODUCTION
Pterygium excision has a high recurrence rate unless accompanied by an approach designed to prevent them. Among the several adjunctive methods tried, the intra-operative application of a single dose of mitomycin C (MMC) seems to be the most commonly performed due to proven in-vitro ( Jampel, 1992) and in-vitro effectiveness and low complication rates in in-vitro studies (Cheng et al., 2001; Frucht-Pery & Ilsar, 1994; Frucht-Pery et al., 1994; Mastropasqua et al., 1994, 1996; Oguz et al., 1999; Sharma et al., 2000; Yanyali et al., 2000). Closure of the defect using conjunctival autografts with (Gris et al., 2000; Mutlu et al., 1999; Riordan-Eva et al., 1993; Shimazaki et al., 1998; Starck et al., 1991) or without the limbus (Allan et al., 1993; John, 2001; Prabhasawat et al., 1997; Sharma et al., 2000; Tan et al., 1997; Ti et al., 2000) and amniotic membrane transplantation (Ma et al., 2000; Prabhasawat et al., 1997; Shimazaki et al., 1998; Solomon et al., 2001) have also become popular techniques in recent years. There are also reports of combinations of two techniques for the treatment of primary and recurrent pterygium (Shimazaki et al., 1998; Wong & Law, 1999). The purpose of the present study was to compare the effectiveness of three adjunctive techniques: amniotic membrane grafts, conjunctival autografts and conjunctival autografts combined with intra-operative MMC, in the treatment of primary and recurrent pterygium. We compared amniotic membrane grafts and conjunctival autografts for primary pterygium and amniotic membrane grafts, conjunctival autografts and conjunctival autografts combined with intra-operative MMC for recurrent pterygium.

FIGURE 1 (a) Preoperative appearance of a patient planned for conjunctival autograft transplantation + mitomycin C application. (b) Preoperative appearance of a patient planned for amniotic membrane transplantation.

MATERIALS AND METHODS

Forty-nine eyes of 49 patients (mean age: 53.5 1.3 years, range 1773) who underwent pterygium excision consecutively between November 1999 and November 2001 at our clinic were included retrospectively in this study.
Y. A. Katrcoglu et al.

Preoperatively, all eyes had eshy pterygium tissue extending more than 2 mm beyond the limbus (Fig. 1). These cases were selected due to their higher predisposition to recur (Tan et al., 1997). Exclusion criteria were a history of any adjunctive therapy or closure of the defect by any technique other than primary closure during the prior surgery, or non-compliance with follow-up visits. The cases of primary pterygium were randomly assigned to two groups: in group 1, the defect was closed with autologous conjunctival tissue from the same eye; in group 2, the defect was closed with previously prepared amniotic membrane. The recurrent pterygium cases were classied as follows: eyes with only a rst recurrence were randomly assigned to conjunctival autografts (group 1) or amniotic membrane grafts (group 2). Eyes with two or more recurrences underwent topical
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administration of MMC and conjunctival autografts (group 3) from the same eye. The MMC + conjunctival autograft group included only recurrent cases in order to reserve this rather aggressive treatment for the recurrent cases only. The operations were approved by the Ethics Committee of the S.B. Ankara Research and Education Hospital. The same surgeon (YAK) performed all the operations. Patients were examined on postoperative days 1, 15 and 30 and then monthly for 3 months, continued for at least 6 months. They were documented by photographs of their preoperative and postoperative appearances and a masked observer (EA), who was not informed about the defect closure technique, graded the outcomes. During preoperative preparation of the patients, conjunctival anesthesia (0.4% oxybuprocaine, Benoxinate , Alcon, Couvreur, Belgium) was applied. The same surgical excision technique was used in all patients. Subconjunctival anesthesia (0.5 ml 2% lidocaine HCl and adrenaline 0.001%, Jetokaine , Adeka AS, Samsun, Turkey) was given into the body of the pterygium using a 27-gauge needle. Using a bevel-up crescent knife (Alcon 8065-9900-02 ), the pterygium head was initially lifted up from the corneal surface, then trimmed from the rest at 46 mm from the limbus. Westcott tenotomy scissors were used to excise the pterygium tissue (Fig. 2) together with a thorough removal of subconjunctival tissue. The scleral bed was protected from cautery in all cases. The amniotic membrane was prepared as follows: human placenta was obtained after elective cesarean

FIGURE 2 Pterygium body excised using Westcott tenotomy

scissors (the patient in Fig. 1a).

delivery of seronegative patients (for human immune deciency, hepatitis B and C viruses and syphilis). Placenta was initially rinsed with sterile saline solution containing 50 g/ml penicillin, 50 g/ml streptomycin, 100 g/ml tobramycin and 2.5 g/ml amphotericin B and blood clots were removed. Amnion was separated from the chorion using blunt dissection and laid on cellulose acetate paper, with the epithelium/basement membrane surface up. The membranes were stored at 80 C in Dulbecco modied Eagle medium and glycerol in a ratio of 1/1 (v/v). During the operation, amniotic membranes were sutured to the defect area (Fig. 3) (basement membrane side facing up) with interrupted 7-0 polyglactin sutures (Vicryl , Ethicon, Edinburgh, UK). In eyes to which MMC was applied, the following technique was employed: Mitomycin C (Kyowa , Onko) was prepared as a 0.02% solution and a microsponge (Alcon 10000 ) was soaked in it for 1 minute. Then (in group 3 cases only), the microsponge was placed over the exposed sclera for 3 minutes (Fig. 4). A thorough irrigation of the ocular tissues was performed; using 100 cc balanced salt solution (Isolyte S , Eczacbas , Baxter, Turkey), after removal of the microsponge. During the conjunctival autograft technique, the donor area (superotemporal bulbar conjunctiva) was marked with Gentian violet, after measuring the recipient area with Castroviejo calipers (Fig. 5). The donor was marked 12 mm larger than the recipient area in all of its dimensions. Stay sutures of 4-0 black silk were inserted at 12 oclock and 3 oclock positions for better exposure of the surgical eld. Subconjunctival anesthesia was applied using a 27-gauge needle (0.5 ml 2% lidocaine HCl and adrenaline 0.001%, Jetokaine , Adeka AS, Samsun, Turkey). With blunt dissection, the conjunctiva was freed carefully from the underlying Tenons capsule and episclera. To help ensure correct tissue orientation, the free graft was spread out on the cornea and transferred to the excision area, as described by Allan et al. (1993). The graft was secured and approximated with the conjunctival edge by interrupted 7-0 polyglactin sutures (Vicryl , Ethicon, Edinburgh, UK), by paying attention not to leave any defect area uncovered (Fig. 6). The donor area was also approximated by interrupted sutures of the same type. In one of the eyes, a 6/0 polyglactin suture was applied to the lower fornix in order to correct
Three Methods for Pterygium Treatment

FIGURE 3 (a) Amniotic membrane is laid on the cornea before positioning (the patient in Fig. 1b). (b) Amniotic membrane is placed in the defect area (the patient in Fig. 1b). (c) Amniotic membrane is sutured to the conjunctiva in the recipient area (the patient in Fig. 1b). (d) The appearance at the end of the surgery (the patient in Fig. 1b).

FIGURE 4 Mitomycin C is applied to the defect area (the patient

in Fig. 1a).

FIGURE 5 The donor conjunctival site is marked with gentian violet (the patient in Fig. 1a).
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Y. A. Katrcoglu et al.

TABLE 2 Treatment of Primary Pterygium. (Fishers Exact Test; p > 0.05 between the Groups)
Treatment Conjunctival autograft (Group 1) Amniotic membrane (Group 2) Total Recurrence (+) [n(%)] 2 (11.1%) 2 (16.7%) 4 Recurrence () [n(%)] 16 (88.9) 10 (83.3%) 26

FIGURE 6 The appearance at the end of the operation, after the

conjunctival autograft has been sutured (the patient in Fig. 1a).

symblepharon formation and the suture was removed 3 weeks after the surgery. At the end of surgery, 0.3% tobramycin ointment (Tobrex , Alcon, Couvreur, Belgium) was applied and the eyes were patched for at least 1 day. All eyes in all 3 groups were treated with 0.3% ciprooxacin (Ciloxan , Alcon, Couvreur, Belgium), 1% prednisolone acetate (Pred-Forte , Allergan, Westport, Co. Mayo, Ireland) and tear substitute (Tears Naturale II , Alcon, Couvreur, Belgium) four times a day for 1 week. Prednisolone acetate was tapered once weekly until the end of the rst month and stopped together with tear substitute at the end of the rst month. Sutures were removed partially at the end of the rst week and totally at the end of the second week. At least 2 mm of brovascular tissue growth onto the cornea was accepted as recurrence (Fig. 7).
TABLE 1 Patient Characteristics ( Kruskal-Wallis Variance
Analysis). (Group 1: Conjunctival Autograft Transplantation, Group 2: Amniotic Membrane Transplantation, Group 3: Mitomycin C + Conjunctival Autograft Transplantation

Data were collected by chart review and presented as mean (SD) or frequency (%). Chi-square, Fishers exact and Kruskal-Wallis variance analysis tests were used to analyze categorical variables such as age, recurrence rate and graft size. The Mann-Whitney U-test was used to compare graft size between primary and recurrent pterygium cases. P-values below 0.05 were considered signicant and Kaplan-Meier survival analysis was performed to evaluate the cumulative incidence of recurrence. SPSS 9.05 (SPSS Inc., Chicago, IL) and Statistica 5.5 (Statistica Inc., Tulsa, OK) were used as computer software.

RESULTS
The demographic data on the eyes are seen in Table 1. The mean age of the patients was 53.5 11.3 years (range 1773). Thirty patients had primary and 19 patients had recurrent pterygium. The mean age of the patients in the three study groups was similar (Kruskal-Wallis variance analysis; p > 0.05, Table 1). The mean follow-up periods were also similar (Kruskal-Wallis variance analysis; p > 0.05, Table 1). The overall recurrence rate was 16.3% (8 eyes). With regard to the treatment of primary pterygium, there was no signicant difference between conjunctival autografts and amniotic membrane grafts (Fishers exact test; p > 0.05, Table 2). With regard to the treatment of recurrent pterygium, all three treatment modalities showed a
TABLE 3 Treatment of Recurrent Pterygium. (*Mitomycin C,
Chi-Square Test; p > 0.05 between the Groups)

Characteristics

Group 1

Group 2

Group 3

p value

Number of eyes 16 25 8 Age (years) 54.0 8.8 51.3 15.3 56.2 9.8 p > 0.05 (mean SD) (4170) (1773) (4573) (Range) Follow-up (months) 19.2 7.0 19.0 6.3 23.5 3.9 p > 0.05 (mean SD) (630) (626) (1927) (Range) Graft size (mm2 ) 61.5 31.0 52.8 29.3 105.25 8.6 p < 0.05 (mean SD) (15144) (24120) (91120) (Range)

Treatment Conjunctival autograft (Group 1) Amniotic membrane (Group 2) MMC + Conjunctival autograft (Group 3) Total

Recurrence (+) [n(%)] 2 (28.6%) .2 (50.0%) 4

Recurrence () [n(%)] 5 (71.4%) 2 (50.0%) 8 (100%) 15

Three Methods for Pterygium Treatment

FIGURE 7 (a) The patient in Fig. 1a: appearance of the excision site 2 weeks postoperatively. (b) The patient in Fig. 1a: appearance of the donor site 2 weeks postoperatively. (c) The patient in Fig. 1a: appearance of the excision site 8 months postoperatively. (d) The patient in Fig. 1a: appearance of the donor site 8 months postoperatively. (e) The patient in Fig. 1b: appearance of the excision site 6 months postoperatively; note the recurrence.
Y. A. Katrcoglu et al. 10

TABLE 4 Intragroup Comparison of Amniotic Membrane Transplantation and Conjunctival Autograft Transplantation between Primary and Recurrent Pterygium. (Fishers Exact Test; p > 0.05 for both Treatment Methods)
Treatment Treatment before Conjunctival autograft [n(%)] Primary Recurrent Amniotic membrane [n(%)] Primary Recurrent

Recurrence (+) 2 (11.1%) 2 (28.6%) 2 (16.7%) 2 (50.0%) Recurrence () 16 (88.9%) 5 (71.4 %) 10 (83.3%) 2 (50.0%)

similar effectiveness (Chi-square test; p > 0.05, Table 3). When the effectiveness of amniotic membrane grafts was compared between primary and recurrent pterygium, no signicant difference was found (Fishers exact test, p > 0.05, Table 4). The recurrence rates after conjunctival autografts were also compared between primary and recurrent pterygium, but again, there was no signicant difference between the groups (Fishers exact test, p > 0.05, Table 4). The cumulative size of the graft was compared in primary and recurrent cases. Recurrent cases required the application of larger grafts for closure of the defect area (Mann-Whitney U-test, p < 0.05, Table 5).

DISCUSSION
The successful treatment of pterygium remains a challenge for the clinician. To prevent recurrence, various techniques for closure of the defect and a number of adjunctive techniques have been developed, as summarized by Prabhasawat et al. (1997). Mitomycin C has been administered in pterygium surgery due to its antiproliferative effect, via the inhibition of DNA synthesis, on cells showing the highest rate of mitosis (Mahar & Nwokora, 1993). Although it was initially used in the form of eyedrops for several days postoperatively (Frucht-Pery & Ilsar1994; Mahar & Nwokora, 1993), intra-operative application of a single dose has proven equally effective (Oguz et al., 1999) and safer (Hayasaka et al., 2000). A report by Raiskup et al. (2004) demonstrated the long-term safety and efTABLE 5 Mean Graft Size in Relation to Treatment. (MannWhitney U-test, p = 0.016

Graft Size Treatment Conjunctival autograft Amniotic membrane MMC + conjunctival Graft Cumulative mean Primary Recurrent (mean SD)(mm2 ) (mean SD)(mm2 ) 55.8 25.6 56.6 32.6 56.2 28.0 76.1 40.7 41.5 13 105.2 8.7 63.5 36.7

cacy of a single intra-operative dose of MMC, even after 125 months. Conjunctival autografts prevent recurrence by contact inhibition of abnormal residual tissue and restoration of the limbal barrier by transplanting healthy limbal cells (when limbal tissue is transplanted together with conjunctiva) (Riordan-Eva et al., 1993). It has been observed that conjunctival autografts are as effective as beta-irradiation (De Keizer, 1998), topical MMC (Mahar, 1997), intra-operative low-dose MMC (Sharma et al., 2000) or amniotic membrane transplantation (Ma et al., 2000) for the prevention of pterygium recurrence. Furthermore, combination with another technique (e.g., intra-operative MMC (Wong & Law, 1999)) is possible and results in a high success rate. Such a combination may decrease possible complications of MMC by allowing a lower dosage, establish an immediate coverage of the defect area, and avoid avascular complications in the sclera. In this study, the effects of conjunctival autografts have been observed both alone and combined with MMC. The combination treatment was reserved for the more rmly attached subconjunctival tissue present in the recurrent cases. In a similar study, combination of conjunctival autografts with MMC was also found to be more effective in the treatment of more severe cases of primary pterygium (Wong & Law, 1999). To the best of our knowledge, this is the rst study to compare the effects of the above two procedures for the treatment of recurrent pterygium. The conjunctival autograft + MMC group had a lower recurrence rate, although the difference was not signicant (p > 0.05). Despite the successful reports in the literature about limbal-conjunctival autografts (Gris et al., 2000; Mutlu et al., 1999; Shimazaki et al., 1998), this method was not preferred in our study due to the lack of instrumentation and experience with this technique. Amniotic membrane serves as a substrate for conjunctival epithelization and therefore has been used successfully to reconstruct large conjunctival defects due to various causes (Shimazaki et al., 1997; Tseng et al., 1997), including pterygium excision (Ma et al., 2000; Prabhasawat et al., 1997; Shimazaki et al., 1998; Tseng et al., 1997). It has the advantages of being immune privileged (no human leukocyte antigen expression) and having antimicrobial, antiproliferative and anti-adhesive activity, probably due to the cytokines it posesses (Shimazaki et al. 1997). Finally, since it is covered by conjunctiva during the follow-up period, it is indistinguishable and cosmetically acceptable (Shimazaki
Three Methods for Pterygium Treatment

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et al., 1997). Solomon et al. (2001) found amniotic membrane to be signicantly more successful for the treatment of recurrent pterygium. Prabhasawat et al. (1997) studied the effectiveness of amniotic membrane in primary and recurrent pterygium and found a higher recurrence rate with recurrent pterygium (although the difference was not statistically signicant). In our study, despite the difference in percentages (16.7% in primary and 50% in recurrent cases), the difference between primary and recurrent pterygium was not signicant. Similarly, two previous studies (Prabhasawat et al., 1997; Ti et al., 2000) designed to compare the effectiveness of conjunctival autografts in primary and recurrent pterygium also found no signicant difference. Ma et al. (2000) compared three techniques for the treatment of primary pterygium and found no significant difference between amniotic membrane transplantation, conjunctival autografts and topical MMC. Prabhasawat et al. (1997) compared conjunctival autografts with amniotic membrane transplantation and primary closure and found conjunctival grafts to be superior to amniotic membrane transplantation and the latter to be better than primary closure. In our study, conjunctival grafts were compared to amniotic membrane closure for the treatment of primary pterygium and no signicant difference was found. Mutlu et al. (1999) compared the effectiveness of limbal-conjunctival autografts with the MMCconjunctival ap combination for the treatment of recurrent pterygium and found similar recurrence rates. Prabhasawat et al. (1997) compared conjunctival autografts, amniotic membrane and primary closure for the treatment of recurrent pterygium and found conjunctival autografts to be superior to the other two approaches (amniotic membrane transplantation was again superior to primary closure). In our study, despite the difference in percentages, no signicant difference was found between conjunctival autograft transplantation, amniotic membrane transplantation and the conjunctival autograft-MMC combination for the treatment of recurrent pterygium. We speculate that preoperative knowledge about the previous treatments the patient has undergone may be very important, especially in recurrent cases, because, as was also found in this study, a larger graft is necessary to close the defect area in such cases. An excessively large conjunctival graft may be difcult to obtain and amniotic membrane transplantation may be a better option for some of the eyes. Besides, an adequate
Y. A. Katrcoglu et al.

coverage of the defect seems to be vital for the prevention of recurrence by preventing outgrowth of the residual pterygium tissue from the graft/membrane barrier (Starck et al., 1991). Nevertheless, in this study, the mean graft size in the eyes treated with the combination of conjunctival autograft + MMC was signicantly larger than in the eyes treated with amniotic membrane transplants and the postoperative follow-up of all eyes in the former group revealed no problems whatsoever. The recurrence rate among eyes with recurrent pterygium treated with amniotic membrane grafts was 50% (4 eyes, 2 recurrences) in this study. These two eyes had had an uneventful follow-up period (4 months and 5 months, respectively) until they both went to Saudi Arabia (which is at a more southern latitude) and on their next follow-up visits, they presented with the beginning of a recurrence, which did not respond to any topical treatment. Although UV-protection via sunglasses during the postoperative follow-up period has not been prescribed for our patients, we believe that this is a very important point that should be mentioned to the patients. We suggest that this kind of postoperative precaution should be recommended as standard in similar studies. We would like to mention three steps from which we beneted in all of our cases and which we believe should be performed as standard procedures during pterygium surgery: thorough excision of the subconjunctival tissue, larger than the pterygium body (Barraquer, 1980), absolute avoidance of cautery to the scleral bed to enable revascularization of the graft from the episcleral bed (Chan et al., 2001), and suturing of the donor conjunctiva site in eyes undergoing conjunctival autograft transplantation to prevent postoperative scarring of the donor area (Chan et al., 2001). In summary, amniotic membrane and conjunctival autograft transplantation seems to be equally effective for the prevention of recurrence in primary pterygium. Combination of MMC with conjunctival autografts seems to be at least equally effective as conjunctival autografts and amniotic membrane transplantation for the treatment of recurrent pterygium. We believe that the combination technique can better be reserved for the more recurrent or resistant cases and that either one of the other two procedures should be used for the treatment of primary cases. The size of the pterygium and the number of recurrences may be a guide for the surgeon to keep amniotic membrane in mind as a surgical tool during the planning of the surgery.
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Three Methods for Pterygium Treatment