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ORIGINAL ARTICLE
Ahead of print publication  

Fornix deepening reconstruction in conjunctivochalasis surgery


1 Department of Ophthalmology, Broward Health, Fort Lauderdale; Department of Ophthalmology, Florida International University, Herbert Wertheim College of Medicine, Miami, Florida, USA
2 Ocular Surface Center, Miami, FL, USA
3 Department of Ophthalmology, Florida International University, Herbert Wertheim College of Medicine; Ocular Surface Center; Department of Biochemistry and Molecular Biology, Miller School of Medicine, University of Miami, Miami, FL, USA
4 Ocular Surface Center; Ocular Surface Research and Education Foundation, Miami, FL, USA

Date of Submission17-Feb-2022
Date of Acceptance11-May-2022
Date of Web Publication15-Jul-2022

Correspondence Address:
Scheffer C G Tseng,
Ocular Surface Center and Ocular Surface Research and Education Foundation, 7235 Corporate Center Drive, Suite C, Miami, Florida 33126
USA
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/tjo.tjo_28_22

  Abstract 


PURPOSE: To assess the extent of inferior fornix shortening in conjunctivochalasis (CCh) and to evaluate whether fornix deepening reconstruction can restore the fornix tear reservoir in patients with CCh.
MATERIALS AND METHODS: This was a retrospective review of five patients (3 unilateral and 2 bilateral eyes, total 7 eyes) with CCh who underwent fornix deepening reconstruction with conjunctival recession and amniotic membrane transplantation. Postsurgical outcome measures included changes in fornix depth with correlation to basal tear volumes, symptoms, corneal staining, and conjunctival inflammation.
RESULTS: For the three patients with unilateral surgery, both the fornix depth (8.3 ± 1.5 mm) and wetting length (9.3 ± 8.5 mm) of the operative eyes were less than the fellow eyes (10.3 ± 1.5 mm and 10.3 ± 8.5 mm, respectively). At 5.3 ± 2.7 months (range 1.7–8.7) postoperatively, the fornix depth increased significantly by 2.0 ± 1.1 mm (P = 0.02). Deepening of the fornix depth was accompanied by overwhelming symptomatic relief (91.5%) that could be subdivided into complete relief (87.5%) and partial relief (4%) of symptoms, with blurred vision being the most notably relieved symptom (P = 0.03). Furthermore, superficial punctate keratitis and conjunctival inflammation were significantly improved at follow-up (P = 0.008 and 0.05, respectively).
CONCLUSION: Deepening of the fornix to restore the tear reservoir is an important surgical objective that may change the tear hydrodynamic state to provide a stable tear film and improve outcomes in CCh.

Keywords: Amniotic membrane, conjunctivochalasis, fornix deepening, fornix reconstruction, tear reservoir



How to cite this URL:
Cheng AM, Mead OG, Tighe S, Tseng SC. Fornix deepening reconstruction in conjunctivochalasis surgery. Taiwan J Ophthalmol [Epub ahead of print] [cited 2022 Sep 28]. Available from: https://www.e-tjo.org/preprintarticle.asp?id=351064




  Introduction Top


To maintain a stable tear film, the sensory input from the first branch of the trigeminal nerve triggers two neuronal reflexes that integrate both compositional (tearing) and hydrodynamic (blinking) factors to ensure ocular surface health and clear vision.[1],[2] Compositional factors include secretion of aqueous, lipid, and mucin tear components, while the hydrodynamic factors involve blinking and closure of the eyelids to promote tear distribution, clearance, and avoidance of evaporation.[1] The conjunctival cul-de-sac in the fornix serves as the tear reservoir, which holds and spreads tears (compositional) to the tear meniscus and then to the preocular tear film through blinking (hydrodynamic).

Conjunctivochalasis (CCh) presents as loose and redundant conjunctival folds interspersed between the globe and eyelids that disrupt tear film stability.[3] While the exact pathology remains unclear, CCh is associated with dissolution of the Tenon's capsule,[4] which leads to poor adhesion between the bulbar conjunctiva and the sclera, conjunctival laxity, and ultimately conjunctival folds. These conjunctival folds can disrupt the continuity of the tear meniscus and block the punctum, triggering hydrodynamic reflex tearing that manifests as epiphora in the presence of delayed tear clearance.[5],[6],[7],[8] In addition, dissolution of the Tenon's capsule leads to conjunctival folds extending from the lid margin to the fornix, which coupled with fat prolapse, obliterate the tear reservoir, and impede tear flow from the fornix reservoir to the tear meniscus.[9],[10] Mechanical friction between the lid margin and the loose conjunctiva during blinking can further exacerbate dry eye by inducing an inflammatory response, which also deteriorates CCh by activating degradative matrix metalloproteinases.[11],[12] Collectively, CCh can lead to tear film instability, i.e., the hallmark of dry eye disease, by impeding tear flow to the tear meniscus and altering hydrodynamic factors even in eyes with adequate (normal) compositional factors.

While a number of surgical approaches for the treatment of refractory CCh have been reported, there is no consensus on the best procedure (reviewed by Marmalidou et al., 2019[13]). Most surgical techniques involve eliminating conjunctival folds close to the tear meniscus, with little focus on restoring the fornix tear reservoir. Based on the notion that loose and redundant conjunctiva in CCh extends from the lid margin/meniscus locale to the fornix, we have formulated a surgical strategy that aims to deepen the fornix so as to ensure a continuous supply of tears from the reservoir to the tear meniscus and preocular tear film.[9] We previously demonstrated that the recession of the conjunctiva from the limbus to the fornix results in a significant increase in basal tear wetting and symptomatic amelioration, as well as a decrease in corneal staining, conjunctival inflammation, and use of topical medications.[9] In this retrospective review, we assessed the change in the fornix depth in CCh patients who underwent fornix deepening reconstruction with amniotic membrane transplantation (AMT).


  Materials and Methods Top


This retrospective study was granted exemption by Sterling Intuitional Review Board (IRB 8288-STseng) and adhered to the tenets of the Declaration of Helsinki. We reviewed the medical records of five consecutive patients (7 eyes) with symptomatic CCh who underwent fornix deepening reconstruction by conjunctival recession and AMT. The diagnosis of CCh was based on the criteria previously summarized by Meller and Tseng,[3] which was confirmed by measuring the recovery rate of the fluorescent inferior tear meniscus after depletion by a capillary tube with and without blinking.[10] All patients remained symptomatic despite prior use of conventional therapies, including artificial tears and steroids. Exclusion criteria included CCh patients who presented with ocular infection, trauma, symblepharon, sunken globe, inadequate blinking, and history of lower-lid surgery. Data retrieved from patients' medical records included demographics, ocular comorbidity, and clinical manifestations at presentation.

Surgical fornix deepening reconstruction

All patients received surgery by the same surgeon (S.C.G.T.) using a previously reported operative technique [Figure 1].[4],[9] After instilling several drops of 1:1000 epinephrine for hemostasis and 2% lidocaine gel for anesthesia, a pair of forceps was used to identify loose and prolapsed conjunctiva in the inferior fornix. A 7-0 vicryl traction suture was placed 2 mm posterior to the limbus at the 3 and 9 o'clock position and used to rotate the eye upward. An arc-like conjunctival peritomy was created 1–2 mm posterior to the limbus in the area of CCh and extended to remove pinguecula, if present. Conjunctiva was rearranged by recessing it from the limbus to the fornix. The loose and wrinkled conjunctiva was readily separated from the sclera with blunt dissection due to underlying degeneration of the Tenon's capsule. The abnormal Tenon's capsule was dissected off from the overlying conjunctival epithelial tissue and thoroughly removed by a pair of sharp scissors toward the fornix region. The prolapsed fat distributed in the fornix was identified, and the gap was sealed using bipolar cautery to prevent fat herniation through the fornix, which obliterates the tear reservoir capacity. Two separate layers of cryopreserved amniotic membrane (Amniograft®; Bio-Tissue, Miami, Florida, USA) were used. The first membrane was placed over the inferior rectus muscle to serve as a new Tenon's capsule. The second membrane was placed over the bare bulbar sclera to replace the conjunctival tissue, fixed with fibrin glue, and further anchored to the sclera in the fornix by a double-armed 6-0 vicryl mattress suture, one per quadrant. The recessed conjunctival was reanchored back to the fornix with one mattress 8-0 vicryl to the sclera per quadrant. Postoperatively, all patients received topical ofloxacin 0.3% (Ocuflox; Allergan, Inc., Irvine, CA) 3 times a day and prednisolone acetate ophthalmic suspension 1% (Pred Forte; Allergan, Inc., Irvine, CA) four times a day for 3 weeks.
Figure 1: Surgical Procedure. An arc-like conjunctival peritomy is created 1–2 mm posterior to the limbus in the area of redundant conjunctival tissue (a). Rearrangement of conjunctiva by recessing from the limbus to the fornix (b, arrow). The recessed conjunctiva is lifted up by a forceps to identify the prolapsed fat (star) that is distributed in the fornix. The excess Tenon's capsule (asterisk) is grabbed and dissected off from the overlying conjunctival epithelial tissue and removed by a pair of sharp scissors (c). The prolapsed fat is cauterized to create a gap (d) for prevention of fat herniation through fornix. Two separate layers of cryopreserved AM are laid down to replace Tenon (e) and the conjunctival tissue (f) to help prevent recurrence and expedite patient's recovery. The conjunctiva is recessed to anchor at the fornix with 8-0 vicryl. AM transplantation with conjunctival recession and fornix deepening reconstruction restores normal fornix structure. AM: Amniotic membrane

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Evaluation and outcomes

Lower fornix depth assessment

Fornix depth was measured using a sterile, flexible metric ruler (Devon™, MA, USA) that had a millimetric scale [Figure 2]. After one drop of proparacaine hydrochloride 0.5% (Alcon, NSW, Australia), the patient was instructed to look up to the ceiling with the face in the primary position. The flexible ruler was gently inserted over the center of the pupil into the inferior conjunctival sac. The fornix depth was measured by identifying the mark aligned with the posterior lid margin. If the lid margin fell between 2 mm marks, an additional 0.5 mm was added to the total. Such fornix depth was measured by the same observer (A.C.) at baseline and 1-month postoperatively.
Figure 2: Fornix measurement by a ruler. The millimetric scale in this ruler (a) enables the measurement of fornix depth before (b) and after (c) surgery in a representative eye

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Fluorescein clearance test (FCT) was used to assess changes in basal tear volume. As previously described,[14] 5 μL of Fluoress® (Akorn Inc., Abita Springs, LA, USA) was applied to the inferior fornix for 5 min, after which a Schirmer paper strip (Alcon Laboratories, Inc., Fort Worth, TX, USA) was inserted for 1 min. This was repeated twice more for a total of 3 times over a 30-min period. Symptoms were assessed before and after treatment, and the degree of improvement was graded using four categories: (1) complete/remarkable relief, (2) partial relief, (3) persistent/unchanged, and (4) deteriorated. Superficial punctate keratitis (SPK) measured by fluorescein staining was graded as 0 (none), 1 (mild), 2 (moderate), and 3 (severe); conjunctival inflammation was graded in the same manner according to the conjunctival injection based on the National Eye Institute Scale, in which five areas of the cornea were assessed.[15]

Statistical analyses

Descriptive statistics for continuous variables are reported as mean ± standard deviation and analyzed using SPSS software, version 19.0 (SPSS Inc., Chicago, IL, USA). Continuous and ordinal outcome measures were compared before and after surgical intervention using the Wilcoxon signed-rank test. Significant differences between percentages and frequencies were assessed using Fisher's exact test. Relationships between variables were assessed using Kendall's Tau-b correlation. P < 0.05 was considered statistically significant.


  Results Top


There were seven eyes of five patients (3 unilateral, 2 bilateral) with symptomatic CCh who underwent fornix deepening reconstruction with conjunctival recession and AMT. The mean age of patients (4 females, 1 male) was 74.4 ± 11.6 years. SPK was graded as “mild” in 5 eyes and “moderate” in 2 eyes. Furthermore, conjunctival inflammation was “absent” in 3 eyes, “mild” in 3 eyes, and “moderate” in 1 eye. The most prevalent symptoms at baseline included photophobia (n = 6), blurred vision (n = 6), grittiness (n = 5), and dryness (n = 4). Baseline characteristics are presented by case in [Table 1]. For the three patients with unilateral surgery, both fornix depth (8.3 ± 1.5 mm) and wetting length (9.3 ± 8.5 mm) of the operative eyes were less than the fellow eyes (10.3 ± 1.5 mm and 10.3 ± 8.5 mm, respectively).
Table 1: Baseline characteristics

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Pre- and post-operative outcomes are presented in [Table 2]. The average follow-up period was 5.3 ± 2.7 months (range 1.7–8.7). Following fornix reconstruction, the fornix depth significantly increased from 9.6 ± 1.5 mm to 11.6 ± 0.8 mm (P = 0.017). Furthermore, the wetting length increased from 7 ± 5.7 mm to 9 ± 3.9 mm; however, this increase was not statistically significant (P = 0.12). When excluding one outlier with a baseline wetting length of 19 mm, the wetting length significantly increased from 5 ± 2.4 mm at baseline to 7.7 ± 1.9 mm after surgery (P = 0.042). Deepening of the fornix depth was accompanied by overwhelming symptomatic relief (91.5%) that could be subdivided into complete relief (87.5%) and partial relief (4%) of symptoms, with the most notably relieved symptom being blurred vision (P = 0.03). Symptoms were entirely resolved in all but two patients after surgery; Case 1 had residual dryness and photophobia due to underlying aqueous tear deficiency confirmed by repeated FCT, and Case 4 had persistent itching presumably due to underlying allergy at follow-up. The improvement of symptoms was also accompanied by significant resolution of SPK and reduction of conjunctival inflammation (P = 0.008 and 0.05, respectively).
Table 2: Pre- and post-operative outcome measures

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  Discussion Top


A number of surgical methods have been utilized to treat CCh including crescent resection with direct closure,[5] resection combined with inferior peritomy and radial relaxing incisions,[16],[17] resection with AMT,[3],[18],[19],[20] cauterization/laser coagulation with or without resection,[21],[22] and subconjunctival fibrin sealant followed by resection.[23] However, most of these procedures focus on eliminating conjunctival folds that interfere with the tear meniscus using resection rather than recession of the loose conjunctiva. While these resection procedures may effectively restore the continuity of the tear meniscus, this is not always accompanied with the relief of symptomatic CCh. Yokoi et al.[24] reported that conjunctival resection successfully reconstructs the tear meniscus at the lower lid margin in nearly two-third of cases. However, they later reported that even if the tear meniscus was successfully reconstructed with a significant improvement in symptoms, others could not obtain a remarkable improvement.[17] We thus postulate that depletion of the fornix reservoir is a key missing link that may help explain the aforementioned discrepancy. Under normal circumstances, the fornix serves as the tear reservoir, which delivers tear fluids to the tear meniscus and the preocular tear film through blinking (i.e., hydrodynamic factors). In CCh, however, dissolution of the Tenon's capsule leads to loose conjunctiva that extends from the lid margin to the fornix along with fat prolapse, which obliterates and depletes the fornix tear reservoir.[9],[10] Consequently, this structural abnormality ultimately impedes the tear flow to the meniscus through blinking to replenish the depleted tear meniscus and spread over the preocular tear film. Collectively, CCh-induced dry eye differs from conventional dry eye caused by “compositional” deficiency in having a “mechanical” issue due to dysfunction of “hydrodynamic” but not compositional factors.

No standardized method has been reported for the evaluation of fornix depth. Some studies devised aluminum rod,[25] stainless steel metric rod,[26] or polymethylmethacrylate measurer;[27] however, all these rigid measurers can displace tissues to some extent. In contrast, we modified the validated central fornix measurement with flexible ruler to minimize the amount of external force applied. Furthermore, because the assessment of fornix depth was performed by the same clinician (A.C.), this study design eliminates interexaminer variability. We were surprised to find that the baseline inferior fornix depth of the eye undergoing surgery (8.3 mm) was shorter than that of the contralateral eye (10.3 mm), which appears similar to previously reported epidemiologic studies in Caucasian[28] or South Asian eyes,[27] according to age and gender. Nevertheless, we speculate that obliteration of the fornix reservoir in eyes with symptomatic CCh is accompanied by a subclinical foreshortening of the fornix. Herein, we noted that surgical reconstruction aimed at fornix deepening resulted in a significantly deeper fornix 1 month after surgery, which was accompanied with symptomatic improvement and reduction of SPK and conjunctival inflammation. The aforementioned clinical benefits were associated with improved postoperative wetting length (~2 mm) measured by the Schirmer test, which uses a paper strip bent over the tear meniscus to reach the tear reservoir in the fornix. The 2 mm improvement in the wetting length is equal to about 1 μl or 25% of the normal tear reservoir volume, which is estimated to be around 50% of the total tear volume, i.e., 7–10 μl.[29] Thus, we suspect that a low wetting length by the Schirmer test in eyes with CCh might not be indicative of aqueous tear deficiency. Deepening of the fornix changes the tear hydrodynamic state, leading to a stable tear film, explaining why there was notable resolution of blurred vision after surgery. The above finding is consistent with our previous report, which showed a significant increase in the basal tear volume following fornix reconstruction with conjunctival recession and AMT in all 18 eyes with CCh, whether or not ATD was present.[9] In contrast, both Hara et al.[30] and Qiu et al.[31] found no observed changes in tear quantity following conjunctival resection despite significant improvement of tear film stability. We wonder if such a discrepancy could be due to their surgical methods, which utilized resection rather than recession and did not aim to deepen the fornix tear reservoir. While further studies with larger sample sizes are warranted to verify our findings, these results demonstrate the potential importance of fornix deepening reconstruction via recession in CCh surgery to restore the tear reservoir, increase basal tear volume, and eliminate symptomatic dry eye and ocular irritation. Further pathophysiological studies are needed to determine whether dissolution of the Tenon's capsule not only induces loose and wrinkled conjunctiva but also incites inflammation and scarring in the deep fornix.


  Conclusions Top


Deepening of the fornix to restore the tear reservoir may change the tear hydrodynamic state to provide a stable tear film and improve outcomes in CCh.

Financial support and sponsorship

This study was supported by an unrestricted grant from Ocular Surface Research and Education Foundation, Miami, Florida, USA.

Conflicts of interest

S.T. has obtained a patent for the method of preparation and clinical uses of amniotic membrane and has licensed the rights to TissueTech, Inc., which procures and processes, and to Bio-Tissue, Inc., which is a subsidiary of TissueTech, Inc., to distribute cryopreserved amniotic membrane for clinical and research uses. S.T.O.M. and S.T. are employees of BioTissue, Inc. Dr. Scheffer C.G. Tseng, an editorial board member at Taiwan Journal of Ophthalmology, had no role in the peer review process of or decision to publish this article. The other authors declared no conflicts of interest in writing this paper.



 
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