Outcomes of the TissueTuck Surgical Technique for Recurrent Pterygium

Abstract

Purpose:

The objective of this study was to evaluate the clinical outcomes of the TissueTuck technique in the treatment of eyes with recurrent pterygium.

Methods:

A retrospective review was performed on patients with recurrent pterygium who underwent surgical excision, followed by the application of cryopreserved amniotic membrane, using the TissueTuck technique between January 2012 and May 2019. Only patients with at least 3 months of follow-up were included for analysis. Baseline characteristics, operative time, best-corrected visual acuity, and complications were assessed.

Results:

A total of 44 eyes of 42 patients (age 60.5 ± 10.9 yrs) with single-headed (84.1%) or double-headed (15.9%) recurrent pterygium were included for analysis. The average surgical duration was 22.4 ± 8.0 minutes, and mitomycin C was administered intraoperatively in 31 eyes (72.1%). During a mean postoperative follow-up of 24.6 ± 18.3 months, there was only 1 case of recurrence (2.3%). Other complications include scarring (9.1%), granuloma formation (20.5%), and corneal melt in 1 patient with preexisting ectasia (2.3%). Best-corrected visual acuity significantly improved from 0.16 Logarithm of the Minimum Angle of Resolution at baseline to 0.10 Logarithm of the Minimum Angle of Resolution at the last postoperative follow-up (P = 0.014).

Conclusions:

TissueTuck surgery with cryopreserved amniotic membrane is safe and effective for recurrent pterygium cases with a low risk of recurrence and complications.

Pterygium is characterized by abnormal fibrovascular tissue of the conjunctiva that often encroaches onto the cornea causing visual impairment. Surgical excision is the only effective treatment, although the rate of success defined by no postoperative recurrence varies greatly in the literature.^1–3 Removal of recurrent pterygium is especially challenging compared with primary excision, as these cases exhibit a more aggressive, fibrovascular growth pattern with distorted tissue planes and strong adherences to surrounding tissue, such as the rectus muscle or corneal stroma. The additional widespread excision in recurrent cases may potentially lead to conjunctival inflammation, symblepharon formation, scarring to recti muscles, motility restriction, corneal scarring, corneal thinning, and limbal stem cell deficiency.⁴ Aside from these potential complications, the incidence of recurrence after excision of recurrent pterygium (31.3%–33.3%)² is significantly higher compared with primary pterygium (1.9%–13.5%).^1,2 As such, there remains an unmet clinical need to reduce the likelihood of postoperative recurrence and complications in cases with recurrent pterygium.

Several techniques have been developed to reduce the rate of pterygium recurrence such as β-irradiation, anti-vascular endothelial growth factor injections, use of mitomycin C (MMC), and graft transplantation.^1,5 Although preferences vary from surgeon to surgeon, the common clinical practice is to cover the bare sclera with a graft such as amniotic membrane (AM) or conjunctiva. Recently, we reported the outcomes of the TissueTuck surgical technique in primarily primary pterygium cases that demonstrated a recurrence rate of 0.7% over a mean follow-up of 30.2 ± 22.2 months.⁶ This TissueTuck technique encompasses pterygium excision followed by cautery to seal the recessed Tenon's capsule and the resected edge of the fibrovascular root to prevent advancement of fibrovascular tissue and subsequently recurrence. A cryopreserved AM graft is then tucked deep between the remaining conjunctiva and Tenon's capsule to further seal the gap to prevent recurrence.⁷ Aside from acting as a physical barrier, the antiinflammatory and antiscarring properties of AM are beneficial to prevent excessive inflammation and subsequent fibrovascular growth, which make it an especially attractive treatment modality for recurrent cases. The cryopreserved membrane also provides a regenerative platform for the replacement of the scarred and deficient conjunctiva, typical of recurrences, with healthier and functional conjunctival integrity. Herein, we report the outcomes of the TissueTuck technique in the treatment of eyes with recurrent pterygium to determine the comparability with the outcomes after primary pterygium surgery.

MATERIALS AND METHODS

On Institutional Review Board approval, we retrospectively reviewed the medical records of all patients who underwent pterygium excision for recurrent pterygium using the TissueTuck technique by the same surgeon (N.R.D.) at The Eye Institute of West Florida (Largo, FL) between January 2012 and May 2019. Only patients with at least 3 months of follow-up were included for analysis.

TissueTuck Surgical Technique

After topical anesthesia with tetracaine, a 7-0 Vicryl (Ethicon, Raritan, NJ) corneal traction suture was placed to achieve adequate exposure and put the medial rectus muscle under tension against the globe to prevent potential damage to the muscle sheath during dissection (Fig. 1). Subconjunctival injection of 2% lidocaine with epinephrine was performed to separate tissues along natural tissue planes, avoiding unnecessary damage to blood vessels and the need for excessive use of cautery. The pterygium head was excised from the corneal surface to a smooth and intact Bowman's layer using a crescent blade. The pterygium head was lifted straight up away from the scleral surface to provide visibility of tissue planes and enable blunt dissection of fibrovascular tissue and abnormal Tenon's down to the bare sclera. Relaxing incisions were created through the conjunctiva and Tenon's along the planned superior and inferior wound margins. Pterygium was allowed to retract freely to determine where the new semilunar fold should be naturally recreated. The fibrovascular tissue and Tenon's were resected from the subconjunctival space along the leading border of the new semilunar fold, with care to preserve as much the conjunctiva posteriorly as possible so as to allow adequate tissue for tucking of the cryopreserved amniotic membrane and reconstruction of the semilunar fold. Tenon's and the remaining fibrovascular tissue were then pulled anteriorly from under the conjunctival rim and excised until they naturally recessed at least 2 to 3 mm to allow the conjunctiva to lay flat and translucently against the bare sclera. Next, an angled bipolar cautery with the angled McPherson forceps (Storz, Tuttlingen, Germany) was used to cauterize the leading edge of the Tenon's capsule and fibrovascular tissue to seal the conjunctival–Tenon gap. This creates the first barrier to prevent the advancement of fibrovascular tissue, produces tissue contraction, and establishes a well-defined and lower-profile rim for reconstruction of the semilunar fold. It is important to avoid cauterization of the muscle belly, overlying the conjunctival rim, or to over aggressively cauterize the scleral bed. In some cases, sponges were soaked in 0.02% MMC and applied to the gap covering the fornix region for 10 to 20 seconds, avoiding unnecessary contact with the bare sclera. The eye was then thoroughly rinsed with a balanced salt solution to avoid prolonged exposure, necrosis, or scleral stromalysis.

FIGURE 1.

Representative surgical steps of the TissueTuck technique: A 7-0 traction suture placed (A) and the rectus muscle placed under tension (B). Lidocaine 2% with epinephrine (1:10,000) injected (C), the pterygium head excised using a crescent blade (D), relaxing incisions made at superior and inferior margins (E), tissue excised at the site of a planed semilunar fold (F), and the Tenon pulled forward and excised until recessed ∼2 mm under the conjunctival edge (G). Angled McPherson bipolar cautery used to cauterize the leading edge of the Tenon (H), AM is cut and lifted off the backing paper using the curved tying forceps (I), the scleral bed is dried and fibrin glue is applied (J), AM is swept into the gap (K), excess glue is pushed toward the cornea using the tying forceps (L), AM is tucked under superior and inferior conjunctival edges (M), and excess glue is removed (N). The AM is then trimmed at the limbus (O) and the traction suture removed and BCL applied (P).

The scleral bed was carefully inspected for any remaining Tenon's or fibrovascular tissue, and any remnants were removed. Cryopreserved AM (AmnioGraft; Bio-Tissue, Miami, FL) was trimmed to the shape of the exposed bed, oversizing the graft by at least 2 to 3 mm in width and 3 to 4 mm in length to allow for adequate tissue tucking and recreation of the semilunar fold. Using 2 curved tying forceps, the graft was removed from its backing and temporarily placed with the sticky stromal side down on the cornea. Three drops of the thrombin were dripped at the limbus to spread over the scleral bed and pool posteriorly. Excess pooled thrombin was blotted away to prevent sequestration of excess glue within the gap or behind the newly formed semilunar fold. Next, 3 drops of fibrinogen were applied at the limbus and allowed to spread posteriorly over the scleral bed with the assistance of the glue cannula. This order of glue components is intended to allow greater working time to manipulate and tuck the AM graft with care and precision. The graft was then slid over the bed using the curved tying forceps, coating the stromal side with glue, and placed 3 to 4 mm past the edge of the posterior conjunctival rim. Starting in the center of the new planned semilunar fold and moving toward the superior and inferior margins, the graft was swept and tucked under the conjunctival rim and into the gap using the smooth curve of the tying forceps. The center-out sweeping motion simultaneously tucked the graft into the gap in such a manner as to have it reflect on itself, exposing the stromal side of the graft to the stromal side of the conjunctival rim, while pushing glue laterally out of the gap. The forceps were then used to pinch the edge of the conjunctiva to the AM graft to create a wide margin of contact, and the glue was squeegeed in an anterior direction toward the limbus so that the glue was not sequestered posteriorly in the gap. This creates the second barrier to recurrence. The superior and inferior conjunctivae were glued 1 to 2 mm over the edge of the AM. The superior and inferior conjunctival margins were inspected to ensure that they were laying smooth and flat over the membrane with a smooth transition. If a raised transition was observed, the conjunctiva was again raised, additional Tenon's was removed, and the conjunctiva was smoothly reglued down. Any excess glue or tissue graft was removed, the tissue was trimmed at the nasal limbus, the traction suture was removed, and a bandage contact lens was placed.

Postoperative Management and Follow-up

Postoperative treatment included antibiotics and difluprednate 0.05% (Durezol, Alcon, Geneva, Switzerland) 4 times a day for the first week, the latter of which was tapered over 4 weeks. The bandage contact lens was removed 1 week after surgery. Patients who were observed to have conjunctival injection at the operative site or any apparent fibrovascular tissue regrowth in the area of the gap or reconstructed semilunar fold postoperatively were administered an injection of ∼0.3 mL triamcinolone acetonide (Kenalog; Bristol-Myers Squibb, New York, NY), which was performed after concentrating the triamcinolone acetonide solution by allowing the 40-mg particulate in 1 cc to settle out of solution and decanting off the diluent. For patients with granuloma formation in the postoperative recovery period, the granuloma was excised, and triamcinolone was also injected. Recurrence was the primary outcome measure and was defined as postoperative fibrovascular regrowth on the conjunctiva or growth that extended across the limbus to the cornea. Complications such as pyogenic granuloma, scar formation, and epithelial defects were also recorded.

Statistical Analysis

Continuous outcome measures were described using mean ± SD (median, range). Categorical variables were described using frequencies (percentages). The Fisher exact test was used to compare in the incidence of postoperative complications by intraoperative MMC use, and the independent-samples Mann–Whitney U test was used to compare continuous best-corrected visual acuity (BCVA) and operative time by MMC use. Changes in preoperative and postoperative BCVA (Logarithm of the Minimum Angle of Resolution [logMAR]) were assessed using the Wilcoxon signed-rank test. All statistical analyses were performed in SPSS 20.0 software (SPSS Inc, Chicago, IL). A P value of <0.05 was used to determine statistical significance.

RESULTS

Forty-four eyes of 42 patients (16 females and 26 males; mean age 60.5 ± 10.9 yrs) who underwent excision of recurrent pterygium with AM using the TissueTuck technique met the eligibility criteria and were included for analysis. Of the 44 eyes, 35 (79.5%) underwent prior pterygium excision by physicians outside our institution, and the remaining were operated on by the study author (N.R.D). One eye underwent 2 previous pterygium excisions, whereas all other eyes underwent 1 prior excision. Pterygium was single headed in 37 (84.1%) eyes and double headed in 7 (15.9%) eyes. Common patient comorbidities included keratoconjunctivitis sicca or dry eye disease (23.8%), conjunctivochalasis (9.5%), glaucoma (7.1%), thyroid disease (7.1%), ocular surface neoplasia (7.1%), and conjunctival cysts (7.1%) (Table 1). Other comorbidities included ectasia, diplopia, ocular trauma, band keratopathy, scleromalacia perforans, and retinopathy (n = 1).

TABLE 1.

Baseline Characteristics

Patient Characteristics
Age (yrs)	60.5 ± 10.9 58 (32–83)
Sex, n (%)
Male	26 (61.9)
Female	16 (38.1)
Morphological features, n (%)
Single head	37 (84.1)
Double head	7 (15.9)
Comorbidities, n (%)
Keratoconjunctivitis sicca/dry eye disease	10 (23.8)
Conjunctivochalasis	4 (9.5)
Ocular surface neoplasia	3 (7.1)
Thyroid disease	3 (7.1)
Glaucoma	3 (7.1)
Conjunctival cysts	3 (7.1)
Preoperative BCVA (logMAR)	0.16 ± 0.16 (0.1, −0.12 to 0.48)
Postoperative BCVA (logMAR)	0.12 ± 0.15 (0.1, −0.12 to 0.48)
Follow-up (mo)	24.6 ± 18.3 (18, 4–71)

The average duration of surgery was 22.4 ± 8.0 (median: 20, range: 10–39) minutes. MMC was administered in 31 eyes (72.1%), resulting in significantly longer operative time compared with eyes that underwent the TissueTuck procedure alone (24.6 ± 7.9 vs. 15.7 ± 4.1 min, respectively; P < 0.001). Surgery was uneventful in all cases, and the AM graft remained secure to the ocular surface postoperatively without any cases of graft dislodgement.

During a mean follow-up of 24.6 ± 18.3 (median: 18, range: 4–71) months, only 1 case of recurrence (2.3%) developed 12 months after excision in an 83-year-old male patient with preexisting diplopia and a history of recurrent pterygium. A second surgical excision was performed using the same TissueTuck technique that resulted in resolution of pterygium without recurrence at the last follow-up visit at 12 months. The patient did not receive MMC with either surgery. Aside from recurrence, other complications included granuloma formation in 9 eyes (20.5%), scarring in 4 eyes (9.1%), and corneal melt in 1 eye with preexisting ectasia (2.3%). Complications are reported in Table 2. Granuloma formation occurred at 3.1 ± 2.6 (median: 2, range: 1–9) months, with 8 of these patients undergoing subsequent treatment with Kenalog injection at 4.3 ± 3.2 (median: 3.5, range: 1–9) months. There was no significant difference in the incidence of granuloma formation (19.4% vs. 25%) or scarring (9.7% vs. 8.3%) when comparing eyes that did and did not receive intraoperative MMC, respectively (P > 0.05). BCVA significantly improved from 0.16 logMAR at baseline to 0.12 logMAR at the last postoperative follow-up (P = 0.014).

TABLE 2.

Postoperative Complications After Pterygium Excision With or Without Intraoperative MMC

Complication	N (%)
Granuloma	9 (20.5)
Scarring	4 (9.1)
Recurrent pterygium	1 (2.3)
Corneal melt with ectasia	1 (2.3)

DISCUSSION

Together with our previous report of eyes with primary pterygium,⁶ this study of 44 eyes with recurrent pterygium shows that the application of cryopreserved AM using the TissueTuck technique is safe and effective in the management of both primary and recurrent pterygium, resulting in an overall recurrence rate of 2.1% and 2.3%, respectively. By contrast, a 2016 Cochrane review of published studies on pterygium found an average recurrence rate of 9.6% in primary cases and 15.2% in recurrent cases treated with a conjunctival autograft.⁸ The recurrence rate in this study is also substantially lower than the range of recurrence reported in the literature with a bare sclera technique (30%–90%)⁹ and MMC without use of the autograft (6.7%–22.5%).^10–12

The benefits of the TissueTuck technique compared with other techniques are multifold. The use of AM delivers its innate biological properties known to reduce inflammation, scarring, and angiogenesis^13–16; promote conjunctival epithelialization^17–20; promote goblet cell regeneration²¹; and aid in the expansion of limbal epithelial stem cells.²² Together, these actions collectively facilitate limbal stem cell expansion to address partial limbal stem cell deficiency that is invariably present in all pterygium cases. Furthermore, the antiinflammatory properties may aid in curtailing postoperative inflammation that is known to be increased in recurrent cases and contributes to pterygium recurrence. The use of fibrin glue in lieu of sutures is beneficial in reducing surgical trauma and subsequent postoperative conjunctival inflammation.²³ A larger conjunctival defect is generally created after the excision of recurrent aggressive pterygium. Therefore, the use of AM as opposed to the conjunctival autograft avoids donor site morbidity and preserves the conjunctiva in case of future glaucoma surgery. In particular, this surgical technique uses minimal targeted bipolar cautery to the resected edge of the fibrovascular root and recessed Tenon's to seal the conjunctival–Tenon gap, which serves as the first barrier to recurrence. This resembles previous reports of sealing the gap using a running 9-0 nylon suture to restore ocular surface integrity and regain full ocular motility in cases with recurrent pterygium and pathogenic symblepharon.^7,24 In addition, AM is tucked in the gap in such a way to reflect it on itself, exposing the stromal side of the AM to the stromal side of the overlying conjunctival rim. This strong stroma-to-stroma glued bond is the second major barrier to recurrence because it further seals the gap and reforms a functional semilunar fold. This creates a durable, sealed barrier to help prevent recurrence of pterygium in both primary and recurrent cases as demonstrated in our studies. Finally, the TissueTuck technique using cryopreserved AM facilitates regeneration of otherwise deficient and scarred conjunctiva typical of recurrent pterygium, wherein harvesting of an adequate conjunctival autograft may be difficult or impossible.