Int Ophthalmol (2018) 38:1285–1293 https://doi.org/10.1007/s10792-017-0593-4 OR IGINAL PAPER Complete corneal ring (MyoRing) implantation versus MyoRing implantation combined with corneal collagen crosslinking for keratoconus: 3-year follow-up . . . Guzel Bikbova Gyulli Kazakbaeva Mukharram Bikbov Emin Usubov Received: 9 January 2017 / Accepted: 5 June 2017 / Published online: 15 June 2017 The Author(s) 2017. This article is an open access publication Abstract alone group; however, in 36 months there was no Purpose To estimate the effectiveness of complete difference between groups. Keratometry was reduced corneal ring (MyoRing) implantation compared with in both groups; after MyoRing implantation for 8.45 D MyoRing implantation combined with corneal colla- and MyoRing ? CXL for 9.43 D, the spherical equiv- gen crosslinking (CXL) for keratoconus treatment for alent decreased from 8.45 to 7.72 D and from 9.43 to 36 months follow-up. 6.25 D, respectively. The cylinder decreased to 3.33 D Design Retrospective cohort study. with MyoRing alone and to 3.31 D with MyoR- Materials and methods MyoRing implantation was ing ? CXL. Corneal thickness remained nearly performed in a series of 78 patients (80 eyes) with unchanged (from 433.69 ± 38.76 to 434.21 ± 34.98) keratoconus II–III Amsler classiﬁcation, of these 39 in MyoRing group and decreased from baseline (from eyes had MyoRing implantation combined with CXL. 426.93 ± 46.58 to 401.24 ± 39.12 lm) in MyoR- Implantation of a MyoRing in the corneal pocket was ing ? CXL group 36 months postoperatively, which performed using a PocketMaker microkeratome and corresponds with pachymetry reduction after conven- corneal intrastromal implantation system. During tional CXL. CXL, riboﬂavin solution 0.1% was injected into the Conclusion Both MyoRing implantation and MyoR- corneal pocket through the incision tunnel and stan- ing combined with CXL were effective for treating dard surface UVA irradiation (370 nm, 3 mW/cm ) keratoconus. At 36 months, there were slightly better was then applied from 5-cm distance for 30 min. outcomes in MyoRing ? CXL group; however, in Results Signiﬁcant improvements in uncorrected MyoRing alone group visual and refractive outcomes distance visual acuity and corrected distance visual were stable overtime. acuity were observed for both groups, which was relatively better 12 months after procedure in MyoRing Keywords Cornea Keratoconus Corneal collagen crosslinking MyoRing G. Bikbova G. Kazakbaeva M. Bikbov E. Usubov Introduction Ufa Eye Research Institute, Ufa, Russia G. Bikbova (&) Keratoconus is a noninﬂammatory corneal disease Department of Ophthalmology and Visual Science, Chiba characterized by progressive thinning of the cornea University Graduate School of Medicine, Inohana 1-8-1, that is accompanied by ectasia . Changing the Chuo-ku, Chiba, Chiba 260-8670, Japan volume of to the peripheral cornea by ring segment e-mail: Gbikbova@chiba-u.jp; Gbikbova@gmail.com 123 1286 Int Ophthalmol (2018) 38:1285–1293 implantation is reported to be useful for improving implant, with no disruption of continuity along its visual acuity and reducing the corneal steepening circumference, suggesting that it may act as an associated with keratoconus . artiﬁcial limbus and provide biomechanical support Different types of corneal segments may be used for to the cornea [12, 13]. keratoconus treatment, such as Intacs (Addition In a recent report by Daxer, it was indicated that no Technology, Inc.), Ferrara ring (Ferrara Ophthalmics signiﬁcant progression was observed after MyoRing Ltd.), and Keraring (Mediphacos Ltd.). A complete treatment during an average follow-up period of intrastromal ring, called MyoRing (Dioptex, GmbH, 5 years . Linz, Austria), suggested by Albert Daxer in 2007, is The aim of this study was to estimate the effective- relatively new and had been demonstrated to treat ness of complete corneal ring (MyoRing) implantation keratoconus safely and effectively [3–5]. With a alone compared with MyoRing implantation combined surgical system known as the corneal intrastromal with corneal collagen crosslinking (CXL) for kerato- implantation system (CISIS), the MyoRing (ﬂexible conus treatment with 36 months of follow-up. full-ring implant) is inserted into the corneal pocket, using a high-precision microkeratome (PocketMaker microkeratome) [3–5]. Materials and methods Corneal collagen crosslinking (CXL), introduced Study group and protocol by Wollensak et al. , has become a standard treatment for progressive keratoconus [6–9] to slow or possibly stop the progression of a disease. The This retrospective cohort study was performed in Ufa standard technique involves epithelial removal to Eye Research Institute from January 2010 to March enable appropriate penetration of riboﬂavin into the 2015 and included 3 years of follow-up. stromal tissue where highly reactive oxygen species All patients provided informed written consent. The trigger formation of crosslinks that consist of intraﬁb- study was approved by the ethics committee of Ufa Eye rillary and interﬁbrillary covalent bonds . Research Institute (reference number 462.29.9369) The formation of the stromal pocket during following the tenets of the Declaration of Helsinki and MyoRing implantation offers the opportunity for local laws regarding research involving human simultaneous introduction of 0.1% riboﬂavin into the subjects. pocket followed by UVA irradiation to provide Inclusion criteria were age older than 18 years, a combined treatment for patients with progressive diagnosis of keratoconus, intolerance of contact lenses keratoconus . The results of the combination of or glasses, and documented progression of a disease. CXL with MyoRing implantation with 12 months of This progression was deﬁned by the following changes follow-up were reported by Studeny et al. . over the course of 1 year: an increase of the steepest Nobari et al.  presented the comparative study of K by 1.0 diopter (D) or more in the manifest cylinder, MyoRing alone and MyoRing implantation for or an increase of 0.5 D or more in the manifest patients who previously had CXL within 12 months spherical equivalent (SE) refraction by repeated before MyoRing implantation. keratotopography ODP-scan ARK-1000 (Nidek, Some reports demonstrated that ring segments have Japan). the disadvantage of resulting in loss of visual acuity in Exclusion criteria were minimal pachymetry of less the long term [9, 10]. In contrast, it was reported that than 380 lm, a history of previous ocular pathology or MyoRing implantation itself may stop the progression ocular surgery, pregnancy or breastfeeding, and of disease due to the continuous ring shape design and corneal scarring. its ability to strengthen the biomechanical property of Of 115 patients who had MyoRing implantation cornea, and its ability to stabilize the corneal thickness alone or MyoRing implantation combined with CXL, [2, 11], e.g., Daxer in his study found that for ring 35 of them were not able to attend follow-up segments and incomplete rings, the strengthening examinations and therefore they were excluded from factor was 1.0 and that a intracorneal continuous the study. This study included 80 eyes from 78 patients complete ring (MyoRing) had a strengthening factor with progressive keratoconus of grade II–III according of up to = 3.2, because it is a continuous full-ring to the Amsler classiﬁcation (without stromal scarring). 123 Int Ophthalmol (2018) 38:1285–1293 1287 Measurements and devices a 5-cm distance for 30 min. During the UVA expo- sure, injection of the riboﬂavin solution into the pocket Patients were examined at baseline and at 12, 24 and occurred every 10 min. After UVA irradiation, a 36 months post-MyoRing implantation ? CXL. At ﬂexible MyoRing intracorneal implant was inserted each follow-up visit, a standard examination was done into the corneal pocket as described elsewhere [3–5]. to assess uncorrected distance visual acuity (UDVA), The diameters of the rings used in this study were corrected distance visual acuity (CDVA), refractom- 5 mm with a thickness of 240, 280, or 320 lm, etry, keratometry, corneal topography (ODP-scan according to the nomogram recommended by the ARK-1000 Nidek, Japan), and pachymetry (Visante manufacturer. Central corneal thickness recordings OCT, Carl Zeiss, Germany). To create a stromal were performed throughout the UVA irradiation and pocket for further MyoRing implantation, the Pock- shown were 400 lm or higher. The MyoRing place- etMaker microkeratome PocketMaker (Dioptex ment was adjusted in three patients 2 days after GmbH, Linz, Austria) was used. surgery because of insufﬁcient refractive improve- During CXL, pachymetry measurements were ment after the initial implantation. taken with a handheld ultrasound pachymeter (SP- 3000, Tomey, Japan). Statistical analysis To control the safety of the procedure, endothelial cell density was counted in all patients, and corneas Decimal visual acuity was converted to the logarithm were scanned using laser scanning confocal micro- of the minimal angle of resolution (logMAR). scope. Images of the endothelium and cornea were Statistical analysis was performed using GraphPad acquired with a confocal scanning laser ophthalmo- Prism 4 software for Macintosh (version 4.0c, GraphPad scope (Heidelberg Retina Tomograph III/Rostock Software, Inc.). Data were recorded as mean ± stan- Corneal Module; Heidelberg Engineering GmbH, dard deviation (SD). Baseline measurements (preoper- Germany). Endothelial cell density was assessed using ative and 1 year postoperative) between groups were the software provided by the system. compared using a two-tailed paired Visual acuity and The CXL device was used at a distance of 5 cm refractive test. Statistical signiﬁcance for differences with irradiation of 3 mW/cm (UFalink, Russian between preoperative and postoperative data was Federation). Before each treatment, a calibration was deﬁned as P\ 0.05 for all cases. performed to conﬁrm the correct UVA emission level. Surgical technique Results Implantation of a MyoRing in the corneal pocket was The patients included 54 men (70%) and 24 were women performed by using a PocketMaker microkeratome, as (30%), aged 18–48 years (average 27.06 ± 2.02). described elsewhere [3–5]. The device uses a guided, Table 1 shows the baseline characteristics. vibrating diamond blade to create a stromal pocket Group 1 with MyoRing implantation alone 9 mm in diameter at a 300-lm depth via a 4–5-mm included 41 eyes, group 2 included 39 eyes that had wide corneal tunnel. In the group of MyoRing MyoRing combined with CXL. combined with CXL group, 0.1% sterile riboﬂavin No intraoperative complications were observed. In solution was then continuously injected for 3 min into the MyoRing alone group, ﬁve patients (12.1%) the corneal pocket through the incision tunnel via reported glare and night-vision problems postopera- standard 0.3-mm cannula. tively. Additional 1% pilocarpine eye drops were The efﬁciency of riboﬂavin penetration into the prescribed for 1 month postoperatively. In the MyoR- corneal stroma was checked by slit-lamp examination ing ? CXL group, nine patients (23.1%) developed on a dark blue cobalt ﬁlter. An intense yellow glow in slight stromal edema at 1 month after surgery, which the anterior and posterior stroma conﬁrmed riboﬂavin was resolved within 3 months postoperatively. distribution throughout the cornea. Three patients underwent adjustment of the MyoR- Standard surface UVA irradiation (370 nm, 3 mW/ ing placement 2 days after surgery because of insuf- cm ; UFalink, Russian Federation) was then applied at ﬁcient refractive improvement after the initial 123 1288 Int Ophthalmol (2018) 38:1285–1293 Table 1 MyoRing implantation for keratoconus, baseline characteristics (n = 78) Parameter MyoRing alone (n = 41) MyoRing ? CXL (n = 39) UDVA, LogMAR 0.90 ± 0.28 1.06 ± 0.24 CDVA, LogMAR 0.45 ± 0.28 0.49 ± 0.26 Pachymetry thinnest point (lm) 433.69 ± 38.76 426.93 ± 46.58 SE (D) -9.03 ± 4.07 -7.86 ± 4.52 Cylinder (D) -4.87 ± 3.13 -3.98 ± 2.85 K1 (D) 48.67 ± 3.44 48.73 ± 3.87 K2 (D) 54.21 ± 6.27 53.83 ± .5.54 K Av (D) 51.56 ± 5.42 50.25 ± 4.32 UDVA uncorrected distance visual acuity; CDVA corrected distance visual acuity; SE spherical equivalent; K1 corneal dioptric power in the ﬂattest meridian; K2 corneal dioptric power in the steepest meridian; KAv mean corneal power; CCT corneal thickness at thinnest location; D diopter; CXL corneal crosslinking Spectacle corrected Values are mean ± SD implantation. Reposition of the MyoRing within signiﬁcant difference between two groups over 0.5 mm allowed an additional decrease of keratometry the time for all variables except for keratometry up to 4 D (Fig. 1). Table 2 summarizes the visual and (Table 2). refractive outcomes over time. All parameters Corneal thickness at the thinnest point remained improved signiﬁcantly as a result of implantation in nearly unchanged (433.69 ± 38.76–434.21 ± 34.98) both groups. in MyoRing group and decreased from baseline values Signiﬁcant improvements in UDVA and CDVA (426.93 ± 46.58–401.24 ± 39.12 lm) in the MyoR- were observed in both groups, but relatively better ing ? CXL group 36 months postoperatively, which improvement was seen 12 months after procedure in corresponds with pachymetry reduction after conven- MyoRing alone. However, in 36 months there was no tional CXL [14, 15]. difference between groups (Fig. 2). It was not possible to assess the demarcation line Signiﬁcant central corneal ﬂattening was observed in because the stromal pocket was formed at a depth of both groups. Mean keratometry decreased to 8.45 D 300 lm. However, confocal microscopy clearly after MyoRing alone implantation and to 9.43 D after showed that the stroma had a ‘‘honeycomb’’ MyoRing ? CXL (Fig. 3). Statistically signiﬁcant appearance, with a reduced number of keratocyte reductions of spherical equivalent (SE) and corneal nuclei. The maximum depth of penetration mea- astigmatism (CA) were observed overtime, SE sured from the surface of the epithelium was decreased to 7.72 D with MyoRing alone compared to 237–302 lm. At about 6 months postoperatively, 6.25 D with MyoRing ? CXL, and CA was 3.33 D the corneal stroma had regained its normal conﬁg- with MyoRing alone and 3.31 D with MyoR- uration [16–19]. ing ? CXL. Further improvements in keratometry, Confocal microscopy also demonstrated the hyper- SE and CA had been observed in MyoRing ? CXL reﬂectivity of the epithelial layer in the MyoR- group; however, statistical signiﬁcance was not reached ing ? CXL group, and some slight hyperreﬂectivity (between 12 and 24 months P = 0.0511, and between of epithelial cells in the MyoRing alone group. Disrup- 12 and 36 months P = 0.6083 for keratometry, tion and irregularity of subepithelial nerves were between 12 and 24 months P = 0.4036, and between observed in both groups 3 months after surgery, and 12 and 36 months P = 0.594 for SE, between 12 and the recovery was achieved within 6–12 months. Addi- 24 months P = 0.2986, and between 12 and 36 months tionally, in the group of MyoRing alone group the P = 0.7015 for CA). There was no statistical hyperreﬂective keratocytes in the anterior and mid 123 Int Ophthalmol (2018) 38:1285–1293 1289 Fig. 1 1 Preoperative topography. The central cornea is was adjusted 0.5 mm. This resulted in an additional decrease of irregular, with the steepest point in the temporal inferior corneal refraction and astigmatism. 4 Differences in corneal quadrant. 2 Postoperative topography. The central cornea with a refraction between postoperative MyoRing placement and bow-tie pattern and fairly regular astigmatism compared to adjustment (-4.79 D) image 1. 3 Postoperative topography after MyoRing placement 2 2 stroma were noticed at 3 months postoperatively. By (2846 ± 67 cells/mm and 2912 ± 73 cells/mm , 6 months, the stroma had regained its normal conﬁg- respectively). uration. Reﬂective amorphous structures, located to inner and outer edges of the ring, were observed in some patients in both groups at 36 months after surgery. The Discussion haze in the MyoRing ? CXL group was observed as a hyperdensity of extracellular tissue, which had been Implantation of the MyoRing permits individualized resolved within 6–12 months. The endothelial cell treatment of keratoconus through control of the ring density remained nearly unchanged in both groups position as well as its diameter and thickness. The 123 1290 Int Ophthalmol (2018) 38:1285–1293 Table 2 Postoperative Parameter 36 months post-op P interaction data, 36 months after MyoRing ? CXL. Visual UDVA, LogMAR acuity and refractive MyoRing 0.31 ± 0.28, P \ 0.0001 0.2463 outcomes are shown MyoRing ? CXL 0.30 ± 0.23, P \ 0.0001 CDVA, LogMAR MyoRing 0.28 ± 0.26, P = 0.0491 0.5136 MyoRing ? CXL 0.23 ± 0.23, P \ 0.0001 Spherical equivalent (D) MyoRing -1.31 ± 3.15, P \ 0.0001 0.2818 MyoRing ? CXL -1.61 ± 3.18, P = 0.0279 Pachymetry thinnest point (lm) MyoRing 434.21 ± 34.98, P = 0.0931 0.1391 MyoRing ? CXL 401.24 ± 39.12, P = 0.0395 Corneal astigmatism (D) UDVA uncorrected distance MyoRing -1.54 ± 2.25, P = 0.0414 0.5112 visual acuity; MyoRing ? CXL -0.67 ± 1.89, P = 0.0441 CDVA corrected distance K1 (D) visual acuity; K1 corneal dioptric power in the ﬂattest MyoRing 41.64 ± 4.73, P = 0.0151 0.0491 meridian; K2 corneal MyoRing ? CXL 40.12 ± 4.11, P = 0.0179 dioptric power in the K2 (D) steepest meridian; MyoRing 45.01 ± 2.65, P = 0.00506 0.0913 KAv mean corneal power; CCT corneal thickness at MyoRing ? CXL 42.79 ± 3.15, P = 0.01179 thinnest location; D diopter; K Av (D) CXL corneal crosslinking MyoRing 43.11 ± 2.68, P \ 0.000001 0.0488 Values are mean ± SD MyoRing ? CXL 40.82 ± 3.11, P = 0.01 Spectacle corrected pocket technique allows postoperative adjustment of The possibility of adjusting the position, thickness the MyoRing postoperatively to achieve the best and diameter of the ring and the reversibility of position for it . The corneal pocket is created at a surgery provide the surgeon with advantages for depth of 300 lm, and it has a diameter of 9 mm. achieving optimal results for the patient. Compared to intracorneal ring segment nomograms, However, there are some reports for some disad- the MyoRing nomogram is simple and does not vantages of long-term ring segments implantation require consideration of the location and cone type. [9, 10]. Alio et al.  indicated that statistically Our study showed that MyoRing implantation signif- signiﬁcant regression up to 3.36 D in keratometric icantly improved both UDVA and CDVA and signif- readings occurred in progressive cases from 6 months icantly reduced SE and keratometry values. up to 5 years. No intraoperative complications were observed Daxer calculated the strengthening factor for the during this study. Postoperatively 12.1% of patients characterization of different ring-shaped corneal had night-vision problems and halo postoperatively; implant designs and concluded that the small lamellar however, these issues were corrected with pilocarpine incision during the pocket creation technique does not 1% eye drops for 1 month. affect the biomechanical stability of the corneal tissue Repositioning of the MyoRing was performed in . In addition, the geometry of the complete ring two cases. Adjustment within 0.5 mm can result in with full mechanical strength of the material along the much better outcomes, in contrast to ring segment entire circumference may be biomechanically consid- surgery, which involves the rings pacing in circular ered as a further (artiﬁcial) limbus, in contrast to ring tunnels; thus, repositioning of ring segment can be segments, because their incomplete ring geometry has achieved by changing the course of the tunnel . no strengthening effect on the cornea . 123 Int Ophthalmol (2018) 38:1285–1293 1291 Fig. 2 Uncorrected distance visual acuity (UDVA) over time [logarithm of the minimal angle of resolution (logMAR)]. The error bars represent standard deviation (SD) Fig. 3 Keratometry reading over time. The error bars represent standard deviation (SD) Our study showed stable outcomes in the group for into the pocket at once. Several studies have conﬁrmed the MyoRing implantation alone within 36 months. that after MyoRing implantation, the parameters Collagen crosslinking allows stabilization of disease. remained unchanged within 12 months [13, 27]. Our Results over the past 10 years are available conﬁrming study demonstrated slight improvement 24 and the effectiveness of CXL for halting the progression of 36 months after the combined procedure correspond- keratoconus; however, additional visual rehabilitation ing to the results of conventional CXL. Studeny et al. is needed, such as contact lenses, intracorneal ring used combination of MyoRing with CXL and a segments, or phakic intraocular lenses [21, 22]. Addi- 12-month follow-up for a group of 22 eyes with tionally, different transepithelial approaches exist keratoconus  and noted improvements in the results [23–26] to avoid epithelial debridement during CXL between 1 month and 1 year after surgery similarly to and to reduce pain and discomfort during the early our study. Slight improvements after CXL are well- postoperative period; therefore, the formation of the known ﬁndings after 1–2 years; therefore, it can be stromal pocket during MyoRing implantation is a concluded that further improvements after 24 months signiﬁcant advantage for simultaneous introduction of after the combined procedure are due to the effects of 0.1% riboﬂavin into the stromal pocket for further CXL , as conﬁrmed by our study. Nobari et UVA irradiation. Daxer et al.  described the compared MyoRing alone and MyoRing implantation combined technique of MyoRing implantation and for patients who underwent CXL within 12 months CXL with the intrastromal application of riboﬂavin before MyoRing implantation . The follow-up 123 1292 Int Ophthalmol (2018) 38:1285–1293 period was 12 months. They did not ﬁnd signiﬁcant efﬁcient approach for treating keratoconus. Both differences between groups except for CDVA, and methods were safe and effective for treating moderate better outcomes were found for the MyoRing alone and severe keratoconus. After 36 months, there had group. In our study, CXL procedure was performed slightly better outcomes in MyoRing ? CXL group; during MyoRing implantation, and similar to the however, visual and refractive outcomes for the Nobari et al. study, UDVA and CDVA were slightly MyoRing alone group were stable over time. How- better for those in the MyoRing alone group. However, ever, a longer follow-up and randomized prospective at 36 months there were no differences between studies with bigger number of patients are needed to groups. The difference in the CDVA can be explained conﬁrm the effectiveness of both methods. by the haze formation in the group who had combined Limitation of the current study was that there was procedure . However, in our study, slight differ- no evaluation of aberrations, the small group sizes, ences in keratometry and pachymetry values were non uniformity of patients at each stage of found, corresponding to conventional CXL results, but keratoconus. no statistical signiﬁcant differences were found Compliance with ethical standards between groups 36 months after surgery except for keratometry (P = 0.0488). Conﬂict of interest All authors certify that they have no Reports of the combined technique using ring afﬁliations with or involvement in any organization or entity with any ﬁnancial interest (such as honoraria; educational segments for CXL are available. Coskunseven et al. grants; participation in speakers’ bureaus; membership, reported the results of combined KeraRing implanta- employment, consultancies, stock ownership, or other equity tion and CXL. Their group 1 underwent ICRS ﬁrst and interest; and expert testimony or patent-licensing arrangements) then CXL, and their group 2 underwent CXL ﬁrst and or non-ﬁnancial interest (such as personal or professional rela- then ICRS. The interval between treatments was tionships, afﬁliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript. approximately 7 months. They found that these methods combined provided better outcomes, espe- Ethical approval All procedures performed during studies cially when CXL was performed after ICRS implan- involving human participants were in accordance with the eth- tation . Renesto et al.  reported a prospective ical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its study with a 2-year follow-up period; they found no later amendments or comparable ethical standards. difference between patients with ICRS implantation alone and patients treated with CXL followed by ICRS Informed consent Additional informed consent was obtained implantation 3 months later. However, Chan et al.  from all individual participants for whom identifying informa- tion is included in this article. performed a retrospective comparative study of Intacts alone compared to Intacs implantation followed by Open Access This article is distributed under the terms of the CXL and demonstrated that combined surgery resulted Creative Commons Attribution 4.0 International License (http:// in signiﬁcantly greater reductions in the cylinder (2.73 creativecommons.org/licenses/by/4.0/), which permits unre- vs. 1.48 D) and the maximum k value (1.94 vs. stricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original 0.89 D) than did Intacs implantation only. author(s) and the source, provide a link to the Creative Com- There are some advantages using CXL with mons license, and indicate if changes were made. MyoRing implantation in contrast with ring segments. 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International Ophthalmology – Springer Journals
Published: Jun 15, 2017
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