Fovea-Sparing Internal Limiting Membrane Peeling for Myopic Traction Maculopathy NORIAKI SHIMADA, YOSHIHARU SUGAMOTO, MANABU OGAWA, HIROSHI TAKASE, AND KYOKO OHNO-MATSUI ● PURPOSE: To investigate the effectiveness and safety of a new surgical technique of fovea-sparing internal limiting membrane (ILM) peeling for the treatment of foveal retinal detachments (RDs) in eyes with myopic traction maculopathy. ● DESIGN: Retrospective, consecutive, interventional case series. ● METHODS: Forty-five eyes of 45 consecutive patients who underwent vitrectomy and ILM peeling for the treatment of a foveal RD attributable to myopic traction maculopathy were studied. The patients were divided into 2 groups by the area of ILM peeled: complete macular ILM peeled group (30 eyes) and fovea-sparing ILM peeled group (15 eyes). A gas tamponade was used in all of the eyes. The main outcome measures were the rate of development of a full-thickness macular hole (MH) and the best-corrected visual acuity (BCVA). All of the patients were followed for more than 6 months. ● RESULTS: A full-thickness MH developed in 5 of 30 eyes (16.7%) in the complete ILM peeled group and in none of the 15 eyes in the fovea-sparing ILM peeled group. Postoperative OCT examination showed a contraction of the residual ILM on the fovea and reduction of the outer lamellar holes in the fovea-sparing ILM peeled group. The postoperative BCVA was significantly better than the preoperative BCVA in the fovea-sparing ILM peeled group (P ⴝ .04), but not in the complete ILM peeled group. ● CONCLUSIONS: Fovea-sparing ILM peeling results in better visual and anatomic outcomes for the treatment of foveal RD attributable to myopic traction maculopathy. These were accomplished by reducing the development of a full-thickness MH. (Am J Ophthalmol 2012;154: 693–701. © 2012 by Elsevier Inc. All rights reserved.)
M
YOPIC TRACTION MACULOPATHY IS A MAJOR
cause of visual impairment in eyes with pathologic myopia.1–3 Eyes with myopic traction maculopathy include those with vitreomacular traction, retinal thickening, macular retinoschisis (MRS), lamellar macular hole (lamellar MH), and foveal retinal detach-
Accepted for publication April 13, 2012. From the Department of Ophthalmology and Visual Science, Tokyo Medical and Dental University, Tokyo, Japan. Inquiries to Kyoko Ohno-Matsui, Dept. of Ophthalmology and Visual Science, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113, Japan; e-mail:
[email protected] 0002-9394/$36.00 http://dx.doi.org/10.1016/j.ajo.2012.04.013
©
2012 BY
ment (RD). The pathogenesis of myopic traction maculopathy is varied; however, the inflexibility of the internal limiting membrane (ILM) is considered to be an important cause of the maculopathy. In addition, vitreomacular traction from a perifoveal posterior vitreous detachment, from the epiretinal membrane, and from remnants of the cortical vitreous layer may cause myopic traction maculopathy.2,4 Earlier studies have reported on the progression of a MRS into more serious complications such as foveal RD or full-thickness MH during its natural course.5,6 Gaucher and associates5 reported that 6 of 18 eyes with MRS that did not undergo surgical intervention developed fullthickness MH during a mean follow-up of 34.7 months (range, 12 to 60 months). We6 also reported that 4 of 8 eyes with MRS progressed to foveal RD or full-thickness MH in a follow-up period of more than 2 years. Based on these natural course studies, the effectiveness of pars plana vitrectomy to treat myopic traction maculopathy has been evaluated,7–16 although its effectiveness has not been fully determined yet. The development of a full-thickness MH is a serious complication in highly myopic eyes with a foveal RD after vitrectomy. Hirakata and associates12 reported that the risk of the postoperative development of a full-thickness MH is higher in highly myopic eyes with severe foveal RD than in eyes without a foveal RD. This is important because a full-thickness MH is associated not only with reduced vision but also with a risk of developing a MH retinal detachment in highly myopic eyes. The mechanisms of why and how full-thickness MHs develop postoperatively in eyes with foveal RD have not been fully determined; however, we hypothesized that ILM peeling will increase the risk of developing a full-thickness MH. ILM peeling is a widely performed technique to treat foveal RDs,5,10 –12 although some studies with a limited number of patients reported that a foveal RD can be treated by vitrectomy without ILM peeling.13–15 The mechanical traction on such a thinned central fovea by peeling the ILM off of the fovea could induce a break of the central foveal tissue. These concerns prompted us to develop a new technique of ILM peeling for highly myopic eyes with a foveal RD, which we called fovea-sparing ILM peeling. Thus, the purpose of this study was to evaluate the safety and
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FIGURE 1. Schematic drawings of fovea-sparing internal limiting membrane (ILM) peeling. (Top left) Start ILM peeling away from the central fovea. (Top right) Proceed with the ILM peeling. (Second row left) When the peeled ILM flap comes close to the central fovea, stop and start ILM peeling from a new site. (Second row right) Proceed with ILM peeling from the new site with special attention not to peel the ILM around the central fovea. (Third row left) Start the ILM peeling from several new sites and proceed to peel ILM from the entire macular area away from the central fovea. (Third row right) Trim the ILM that remains on and around the fovea with a vitreous cutter. (Bottom left) Completed fovea-sparing ILM peeling.
effectiveness of fovea-sparing ILM peeling in preventing the postoperative development of a full-thickness MH for the treatment of a foveal RD attributable to myopic traction maculopathy. 694
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PATIENTS AND METHODS ALL OF THE PATIENTS WHO UNDERWENT THE FOVEA-SPAR-
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TABLE 1. Baseline Characteristics of the Patients With Myopic Tractional Foveal Detachment Who Underwent Complete Macular Internal Limiting Membrane Peeling or Fovea-Sparing Internal Limiting Membrane Peeling Complete Macular ILM Peeling (30 Eyes)
Fovea-Sparing ILM Peeling (15 Eyes)
P Value
63.2 ⫾ 12.0 5/25 29.1 ⫾ 1.8 20/9/1 47.5 ⫾ 18.5
65.8 ⫾ 7.1 5/10 29.1 ⫾ 1.1 8/7/0 11.3 ⫾ 5.3
.81a .26b .86a .56b ⬍.001a
Age (y), mean ⫾ SD Sex (male/female) Axial length (mm), mean ⫾ SD Lens status, phakia/pseudophakia/aphakia Follow-up (mo), mean ⫾ SD
ILM ⫽ internal limiting membrane; SD ⫽ standard deviation; y ⫽ year. a Mann-Whitney U tests. b Fisher exact probability test.
TABLE 2. Anatomic and Visual Outcomes Before and After Surgery in Complete Macular Internal Limiting Membrane Peeling Group and Fovea-Sparing Internal Limiting Membrane Peeling Group
Surgeon, N.S./Y.S./M.O. Surgery combined with PEIOL, no. (%) Preoperative BCVA in logMAR, mean ⫾ SD (Average Snellen visual acuity) Postoperatove BCVA in logMAR, mean ⫾ SD (Average Snellen visual acuity) BCVA in logMAR on last visit, mean ⫾ SD (Average Snellen visual acuity) Visual improvement in logMAR, mean ⫾ SD Improved, ⬎0.2 logMAR Stable Worsened, ⬍-0.2 logMAR Postoperative FTMH with or without RD, no. (%)
CMIP Group (n ⫽ 30)
FSIP Group (n ⫽ 15)
P Value
8/20/2 19 (63.3%) 0.74 ⫾ 0.5c,d (0.18) 0.58 ⫾ 0.6c (0.26) 0.60 ⫾ 0.6d (0.25) 0.16 ⫾ 0.3 16 10 4 5 (16.7%)
2/12/1 8 (53.3%) 0.65 ⫾ 0.5e,f (0.22) 0.34 ⫾ 0.4e (0.45) 0.35 ⫾ 0.4f (0.44) 0.31 ⫾ 0.2 11 4 0 0 (0%)
.75a .54a .46b .23b .24b .24b .31a
.15a
BCVA ⫽ best-corrected visual acuity; CMIP ⫽ complete macular internal limiting membrane peeling; FSIP ⫽ fovea-sparing internal limiting membrane peeling; FTMH ⫽ full-thickness macular hole; logMAR ⫽ logarithm of minimal angle of resolution; PEIOL ⫽ phacoemulsification and implantation of intraocular lens; RD ⫽ retinal detachment; SD ⫽ standard deviation. a Fisher exact test. b Mann-Whitney U test. c P ⫽ .07 (Mann-Whitney U test). d P ⫽ .08 (Mann-Whitney U test). e P ⫽ .04 (Mann-Whitney U test). f P ⫽ .05 (Mann-Whitney U test).
risks. The risks included retinal toxicity from the dye used to make the ILM more visible and a need for a second vitrectomy to remove the residual ILM. Other risks included those caused by vitrectomy itself, such as RD or endophthalmitis. All patients understood and agreed to have the surgery. Forty-five eyes of 45 consecutive patients who underwent vitrectomy with ILM peeling to treat a foveal RD attributable to myopic traction maculopathy were studied retrospectively. The surgeries were performed from DecemVOL. 154, NO. 4
ber 6, 2005 to June 16, 2011 at the Tokyo Medical and Dental University. Pathologic myopia was defined as a myopic refractive error (spherical equivalent) of ⬎-8.00 diopters (D) or an axial length ⬎26.5 mm. The presence of a foveal RD was confirmed by spectral-domain optical coherence tomography (SD-OCT; Cirrus; Carl Zeiss Meditec, Dublin, California, USA). The eyes with a preoperative full-thickness MH, myopic choroidal neovascularization, or macular atrophy that could affect the central vision were excluded.
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FIGURE 2. Two representative cases that developed a full-thickness macular hole (MH) after vitrectomy with complete internal limiting membrane (ILM) peeling and gas tamponade to treat a myopic foveal retinal detachment (RD). (Top left) Preoperative fundus photograph of the left eye of a 69-year-old woman with axial length of 27.35 mm. The white arrow indicates the optical coherence tomography (OCT) scan line. The best-corrected visual acuity (BCVA) was 0.05. (Middle left) Preoperative OCT image shows the foveal RD with large outer lamellar macular hole (asterisk) and macular retinoschisis. (Bottom left) At 1 month after surgery, the retinoschisis and foveal RD are resolved, but a full-thickness MH is present. The BCVA was reduced to 0.03. (Top right) Preoperative fundus photograph of the right eye of a 63-year-old woman with axial length of 28.65 mm. The white arrow indicates the OCT scan line. The BCVA was 0.1. (Second row right) Preoperative OCT image shows the foveal RD with small outer lamellar macular hole (asterisk) and macular retinoschisis. (Third row right) At 2 months after surgery, a full-thickness MH with RD has developed. (Bottom right) A macular probe was implanted and the RD was resolved. The BCVA was reduced to 0.08.
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TABLE 3. Details of the Patients Who Developed Full-Thickness Macular Hole Postoperatively
Sex
Refractive Error (D)
Axial Length (mm)
Period of Developing MH After Surgery (wk)
Period of Developing MHRD After Surgery (wk)
69 63 59
F F F
⫺9 ⫺19.5 IOL
27.4 28.7 28.3
1 2 2
NA 8 5
25 50
M F
⫺9 ⫺17.5
28.1 30.1
2 2
10 NA
Patient
Age (y)
1 2 3 4 5
logMAR (Snellen Visual Acuity)
Second Surgical Procedure
Final Anatomic Status
NA Macular buckling Vitrectomy with silicon oil tamponade NA NA
Before First Surgery
Final Visit
MH MH MH
1.3 (0.05) 1 (0.1) 0.52 (0.3)
1.52 (0.03) 1.09 (0.08) 0.82 (0.15)
MHRD MH
1.69 (0.02) 0.3 (0.5)
2 (0.01) 0.52 (0.3)
D ⫽ diopters; F ⫽ female; logMAR ⫽ logarithm of minimal angle of resolution; IOL ⫽ intraocular lens; M ⫽ male; MH ⫽ macular hole; MHRD ⫽ macular hole with retinal detachment; NA ⫽ not applicable.
Also excluded were those with a history of ocular trauma and those with other retinal diseases that could affect the vision, such as diabetic retinopathy or retinal vein occlusion. Eyes with dense opacities of the media such as corneal opacities or dense cataracts were also excluded. All of the patients had follow-up periods of at least 6 months. All patients had a complete ophthalmic evaluation, including manifest refraction and measurement of bestcorrected visual acuity (BCVA). ● SURGICAL TECHNIQUES: A standard 25-gauge 3-port pars plana vitrectomy was performed on all eyes under local anesthesia. First, the central vitreous core was removed, and then the posterior hyaloid was removed by active suction using a vitreous cutter or a back-flash needle. The ILM was stained with indocyanine green (ICG; 0.025% concentration) for 30 seconds, and peeled over the complete macular area in all of the patients from December 6, 2005 to September 10, 2009. This group was called the complete ILM peeled group. From October 15, 2009 to June 16, 2011, fovea-sparing ILM peeling was performed on all of the patients. For this procedure, the ILM was grasped with an ILM forceps and peeled off in a circular fashion (Figure 1), but the ILM was not completely removed and was left attached to the fovea. After the ILM was peeled from the entire macula area except the foveal area (in a circular area with a diameter approximately that of the vertical extent of the optic disc), the peeled ILM was trimmed with a vitreous cutter. Finally, fluid-air exchange was performed, followed by an injection of 18% sulfur hexafluoride. The patients were instructed to maintain a prone position for at least 1 week postoperatively. The surgeries were performed by 3 surgeons (N.S., Y.S., and M.O.) at the Tokyo Medical and Dental University Hospital. ● STATISTICAL ANALYSES:
Statistical analyses were performed with SPSS for Windows version 11.5 (SPSS Inc, Chicago, Illinois, USA). The significance of the differ-
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ences in age, axial length, follow-up period, and preoperative and postoperative BCVAs between the 2 groups was determined by Mann-Whitney U tests. The significance of differences in the lens status, sex distribution, surgeon distribution, and rate of developing a full-thickness MH postoperatively was determined by Fisher exact probability tests. The significance of differences between preoperative and postoperative BCVA in each group was determined by paired t tests. A P value ⬍.05 was considered statistically significant.
RESULTS ● DEMOGRAPHICS OF PATIENTS:
The demographics of the 45 eyes of 45 patients are shown in Table 1. There were 30 eyes of 30 patients in the complete ILM peeled group and 15 eyes of 15 patients in the fovea-sparing ILM peeled group. The differences in the age, sex distribution, axial length, and preoperative lens status between the 2 groups were not significant. Because of the difference in when the 2 types of surgeries were begun, the average follow-up period was significantly shorter in the foveasparing ILM peeled group than that in the complete ILM peeled group. The distribution of surgeons for the 2 types of surgeries was not significantly different (Table 2). The number of eyes with simultaneous lens removal and insertion of an intraocular lens was 19 of 30 (63.3%) in the complete ILM peeled group and 8 of 15 (53.3%) in the fovea-sparing ILM peeled group. This difference in the percentages was not significant. Only 1 patient in the complete ILM peeled group did not receive simultaneous lens removal because this patient was younger than 50 years and had no cataract.
● ANATOMIC RESULTS: A full-thickness MH developed postoperatively in 5 of the 30 eyes in the complete ILM peeled group (16.7%; Figure 2, Table 3) and in none of the 15 eyes in the fovea-sparing ILM peeled group (P ⫽ .15, Fisher exact probability tests). Three of the 5 eyes developed a RD
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FIGURE 3. Changes in optical coherence tomographic (OCT) findings after vitrectomy with fovea-sparing internal limiting membrane peeling and gas tamponade to treat myopic foveal retinal detachment (RD). (Top left) Preoperative fundus photograph of the right eye of a 66-year-old woman with an axial length of 27.98 mm. Arrow indicates the OCT scan line. The best-corrected visual acuity (BCVA) was 0.2. (Top right) Preoperative OCT image of the same eye. Foveal RD with large outer lamellar macular hole (asterisk) and macular retinoschisis can be seen. (Second row left) At 1 month after fovea-sparing ILM peeling, the retinoschisis is decreased along with the intraocular gas absorption. The foveal RD is still present, although reduced. The rolled edges of the ILM (arrow) can be seen. The BCVA was 0.3. (Second row right) At 3 months after surgery, the residual ILM (between arrowheads) appears to have contracted and thickened. The retinoschisis is slightly increased and foveal RD is still
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around the full-thickness MH and underwent surgical treatment. The BCVA (in logarithm of the minimal angle of resolution [logMAR] units) was reduced or unchanged in the 5 eyes that developed a full-thickness MH. The preoperative foveal RD or macular retinoschisis disappeared in the other 25 eyes that did not develop a full-thickness MH postoperatively in the complete ILM peeled group. In the fovea-sparing ILM peeled group, the foveal RD and retinoschisis were resolved in all 7 eyes whose follow-up was ⬎12 months. In the other 8 eyes whose follow-up was ⱕ12 months, the foveal RD and retinoschisis were reduced but were not completely reattached. At the final examination, a focal retinoschisis was observed at the site of retinal vascular microfolds in 14 of 30 eyes (46.7%) in the complete ILM peeled group and in 8 of 15 eyes (53.3%) in the fovea-sparing ILM peeled group. The difference in the percentages of focal retinoschisis was not significant (Fisher exact probability tests, P ⬎ .05). An increase of foveal RD or macular retinoschisis was not observed in any of the eyes that did not develop a full-thickness MH postoperatively. However, a transient increase of macular retinoschisis at the time of the resorption of the intraocular gas was observed: 4 of 30 eyes (13.3%) in the complete ILM peeled group and 2 of 15 eyes (13.3%) in the fovea-sparing ILM peeled group. Representative OCT images of the postoperative course of eyes that had fovea-sparing ILM peeling are shown in Figures 3 and 4. The ILM remaining on the fovea was not obvious in the OCT images at 1 month postoperatively except in 1 case (Figure 3). At 3 months after foveasparing ILM peeling, a contraction of the remaining ILM at the fovea was observed as an irregular thickening of the retinal surface in 10 of the 15 eyes (Figures 3 and 4), and the outer lamellar hole was smaller or indistinct in all 15 eyes. These changes were not observed in any eyes in the complete ILM peeled group. No further contraction of the remaining ILM in those eyes was obvious after 3 months. ● VISUAL RESULTS: The differences in the preoperative, postoperative, and final BCVA between the complete ILM peeled group and the fovea-sparing ILM group were not significant (Table 2). However, the postoperative BCVA was significantly better than the preoperative BCVA in eyes treated with fovea-sparing ILM peeling but not in the eyes that had a complete ILM peeling (Table 2). Although there was no significant difference in the distribution of the changes in the BCVA (Table 2), none of the eyes treated with fovea-sparing ILM peeling had a reduction of
the BCVA postoperatively. There was a reduction in the BCVA in 4 of the 30 eyes (13.3%) that had a complete ILM peeling, and these 4 eyes developed a full-thickness MH postoperatively.
DISCUSSION OUR RESULTS SHOWED THAT NONE OF THE EYES THAT
underwent fovea-sparing ILM peeling developed a fullthickness MH postoperatively, but 5 of 30 eyes (16.7%) that underwent complete ILM peeling developed a full-thickness MH. Although the follow-up period was relatively short (average, 11.3 months) and the patient number was not high in the fovea-sparing ILM peeled group, these results are promising for the prevention of postoperative full-thickness MH formation. Postoperative OCT examinations showed that the remaining ILM on and around the central fovea was obviously contracted at 3 months after the fovea-sparing ILM peeling. This contraction was observed in the OCT images as an irregular thickening of the ILM in the fovea (Figures 3 and 4). The combined release of macular traction and less surgical trauma to the central fovea led to a centripetal contraction of the remaining ILM, which is most likely why a full-thickness MH did not develop. The BCVA was significantly better than the preoperative BCVA in the fovea-sparing ILM peeled group, whereas the change was not significant in the complete ILM peeled group (Table 2). A lack of significant improvement of BCVA in the complete ILM peeled group was most likely because some of the patients in this group developed full-thickness MH and reduced vision. There are several concerns on the safety of fovea-sparing ILM peeling surgery. One would be that a late contraction of the remaining ILM could cause vision reduction because of a mechanism similar to the formation of an epiretinal membrane. Although no further contraction of residual ILM was noted 3 months after the fovea-sparing ILM peeling, a longer follow-up is necessary to examine this. There are several limitations to our study. This was not a prospective study, and the vitrectomies were performed by multiple surgeons. Also, the difference in the follow-up periods in the 2 groups needs to be considered. The period when we performed complete ILM peeling was before we did fovea-sparing ILM peeling. Thus, the effect of surgical learning curve cannot be completely ruled out. In addition, the timing and indications of vitrectomy against myopic traction
present. However, the outer lamellar hole has become small (asterisk). The BCVA was 0.3. (Third row left) At 6 months after surgery, the retinoschisis and foveal RD are still present, but decreased. The BCVA was 0.3. (Third row right) At 12 months after surgery, the foveal RD is completely resolved and the retinoschisis is also decreased except at the lower macular area around the retinal artery, which is observed as a retinal vascular microfold (arrow). The BCVA was 0.4. (Bottom) At 18 months (left) and 24 months (right) after surgery, the retinoschisis has been absorbed. The BCVA has improved to 0.7 at 24 months after the fovea-sparing ILM peeling.
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FIGURE 4. Changes in optical coherence tomographic (OCT) images after vitrectomy with fovea-sparing internal limiting membrane peeling and gas tamponade to treat myopic foveal retinal detachment (RD). (Top left) Preoperative fundus photograph of the right eye of a 70-year-old woman with axial length of 29.80 mm. The arrow indicates the OCT scan line. The best-corrected visual acuity (BCVA) was 0.5. (Top right) Preoperative OCT of the same eye. Foveal RD and macular retinoschisis with both inner (arrow) and outer lamellar macular hole (asterisk) can be seen. (Second row left) At 1 month after surgery, retinoschisis and foveal RD are decreased after the absorption of the intraocular gas. The edges of the residual ILM were not obvious. The BCVA is 0.4. (Second row right) At 3 months after surgery, the residual ILM appears to have contracted centripetally and to be thickened (between arrows). The outer lamellar hole is smaller or indistinct, although the retinoschisis and foveal RD have not changed. The BCVA is 0.4. (Third row left) At 6 months after surgery, the retinoschisis and foveal RD have further decreased. The BCVA is 0.6. (Third row right) At 12 months after surgery, the foveal RD has been completely resolved. The BCVA has improved to 0.8. (Bottom left) At 18 months after surgery, the retina has remained attached and no further contraction of the residual ILM is noted. The BCVA is 0.8.
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maculopathy have not been consistently set, although there are some risks caused by vitrectomy itself against highly myopic eyes. However, in spite of all of these limitations, we consider that fovea-sparing ILM peeling has the benefits of preventing the postoperative formation of full-thickness MH in patients with myopic foveal RD.
In summary, vitrectomy with fovea-sparing ILM peeling and gas tamponade resulted in better visual and anatomic outcomes when treating foveal RD attributable to myopic traction maculopathy. Longer-term follow-up studies will be necessary to clarify the usefulness and safety of foveasparing ILM peeling.
ALL AUTHORS HAVE COMPLETED AND SUBMITTED THE ICMJE FORM FOR DISCLOSURE OF POTENTIAL CONFLICTS OF Interest and none were disclosed. Publication of this article was supported in part by research grant 22390322 and 23659808 from the Japan Society for the Promotion of Science, Tokyo, Japan. Involved in design of the study (K.O.M., N.S.), conduct of the study (K.O.M., N.S., Y.S., M.O., H.T.), writing the article (K.O.M., N.S.), critical revision of the article (K.O.M., N.S.), obtaining funding (K.O.M.), statistical expertise (N.S.), and literature search (N.S., K.O.M.). Approval was obtained from the Ethics Committee of the Tokyo Medical and Dental University to perform this retrospective study, and the procedures used during the examinations conformed to the tenets of the Declaration of Helsinki. Written informed consent was obtained from all participants. The authors thank Professor Duco Hamasaki for his critical discussion and final manuscript revision.
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