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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 34  |  Issue : 4  |  Page : 1505-1512

Corneal and lens densitometry after corneal collagen cross-linking with conventional versus enhanced protocol


1 Department of Ophthalmology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Ophthalmology, Damanhur Eye Hospital, Al Behera, Egypt

Date of Submission15-Oct-2020
Date of Decision03-Dec-2020
Date of Acceptance07-Dec-2020
Date of Web Publication24-Dec-2021

Correspondence Address:
Mahmoud M. S. Nassar
MBBCh, Damanhur Eye Hospital, Al Behera
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_381_20

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  Abstract 


Objective
To evaluate the changes in corneal and lenticular density following corneal cross-linking (CXL) with conventual versus enhanced protocol.
Background
Corneal stromal haze is common after CXL. This is related to the corneal stromal changes occurring after CXL. This can be detected clinically and graded subjectively at the slit-lamp, or measured objectively using Scheimpflug imaging densitometry.
Patients and methods
This is a prospective randomized controlled clinical trial including all patients with keratoconus undergoing CXL. It included 20 eyes with conventional versus 20 eyes with enhanced method. All patients attended the outpatient clinic unit of Menoufia University Hospital, Shebin El Kom, during the period study from August 2019 till June 2020. Full history; routine, physical examination; general topography; and Pentacam imaging were done.
Results
Mean corneal thinnest location thickness was significantly improved after 30 min (462 ± 15.6) than 10 min (431.23 ± 92.94). There were no statistically significant differences between the two studied groups regarding corneal densitometry and lens density (P > 0.05). The correlation between thinnest location and Kmax as well as corneal and lens density did not reach statistical significance level (P > 0.05). There was an exception was in group I, where thinnest location was significantly negatively correlated with Kmax preoperatively (P = 0.008) and 1 month postoperatively (P = 0.046). Moreover, thinnest location was significantly positive correlated with corneal density 180 at 6 months postoperatively (P = 0.001).
Conclusion
A significant improvement in corneal thinnest location thickness was observed at the final follow-up examination after 30 min (462 ± 15.6) than 10 min (431.23 ± 92.94). Moreover, thinnest location was correlated inversely with Kmax after 1 month postoperatively. However, thinnest location was significantly positively correlated with corneal density at 6 months postoperative. In addition, a significant improvement in contrast sensitivity at the final follow-up examination after 10 min than 30 min, but the different between them did not reach statistical significance.

Keywords: collagen cross-linking, corneal densitometry, enhanced protocol, keratoconus, lenticular density


How to cite this article:
El Sayed SH, Nassar MM, Basyoni A. Corneal and lens densitometry after corneal collagen cross-linking with conventional versus enhanced protocol. Menoufia Med J 2021;34:1505-12

How to cite this URL:
El Sayed SH, Nassar MM, Basyoni A. Corneal and lens densitometry after corneal collagen cross-linking with conventional versus enhanced protocol. Menoufia Med J [serial online] 2021 [cited 2024 Mar 28];34:1505-12. Available from: http://www.mmj.eg.net/text.asp?2021/34/4/1505/333246




  Introduction Top


Keratoconus (KC) is a bilateral, progressive, noninflammatory disease of the cornea, which often leads to high myopia and astigmatism, with an estimated prevalence of ∼1 in 2000 and an incidence between 50 and 230 per 100 000. It is a multifactorial disease with an unknown exact etiology which impairs the acuity and quality of vision secondary to thinning in and protrusion of the cornea, which ultimately affects both eyes [1].

In its early stages, KC can be managed conservatively via spectacles or rigid contact lenses. In more advanced stages, surgical treatment with deep lamellar keratoplasty and penetrating keratoplasty should be considered. However, potential complications and technical needs led to the race for an alternative [2].

Corneal collagen cross-linking (CXL) is a relatively new technique to decrease the progression of KC and other corneal ectatic disorders such as post-laser in-situ keratomileusis ectasia [3]. CXL decreases corneal steepness and improves topographic indices, thus leading to improvement in uncorrected visual acuity (UCVA) and best-corrected visual acuity (BCVA), as the cornea is exposed to ultraviolet-A (UVA) after riboflavin (vitamin B2) is administered topically. The result of the exposure is the formation of free oxygen radicals that cause mechanical stiffness of the corneal stroma owing to the formation of chemical bonds within the stroma, and the resulting compaction of the collagen lamellae leads to the thinning of the cornea [4].

Accelerated or high-fluence protocols present a promising alternative to the time-consuming conventional cross-linking. The potential advantages include reduced exposure time, better patient compliance, and lower infection risk [5]. According to Bunsen-Roscoe's law of reciprocity, an increased intensity of UVA irradiation coupled with reduced exposure time theoretically delivers a total energy dose to the tissue equivalent to that in conventional treatment, with similar biological effect [3].

Corneal stromal haze is common after CXL. This is related to the corneal stromal changes occurring after CXL; this can be detected clinically and graded subjectively at the slit-lamp, or measured objectively using Scheimpflug imaging densitometry [6]. Therefore, this study aims to evaluate the changes in corneal and lenticular density following CXL with conventual versus enhanced protocol.


  Patients and methods Top


Study design

This is a prospective randomized controlled clinical trial including all patients with KC who underwent CXL. A total of 20 eyes with conventional versus 20 eyes with enhanced method were included. All patients attended the outpatient clinic unit of Menoufia University Hospital, Shebin El Kom, during the period study from August 2019 till June 2020.

All patients included in this study were divided into two groups as follow:

Group I (10 min) included 20 eyes with enhanced method, and their mean age was 26.73 ± 7.39 years.

Group II (30 min) included 20 eyes with conventional versus, and their mean age was 26.40 ± 3.90 years.

Ethical consideration

All procedures were carried out in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. Written informed consents were obtained from all patients, and the study was approved by hospital ethics committee of the Department of Ophthalmology, Faculty of Medicine, Menoufia University.

All patients were selected according inclusion and exclusion criteria

Inclusion criteria

Age between 15 and 40 years, phakic patients with clear lenses, confirmed bilateral keratoconus (KCN) based on clinical and topography findings, bilateral minimum corneal thickness of 400 μm as measured with the Pentacam, and maximum keratometry of 60 D in each eye based on Pentacam readings were the inclusion criteria.

Exclusion criteria

The following cases were excluded from the study: nonprogressive KC, pseudophakia or cataract, corneal thinnest point less than 400 μm, corneal scarring in either eye, previous eye surgery, ocular surface or tear problems, and coexistence of ocular pathology other than KCN.

All of the patients were subjected to the following.

Preoperative evaluation

It included the following.

Full clinical history

Age, complaint, ocular trauma or disease, optical correction: glasses or contact lenses, and any systemic medical diseases, for example, diabetes mellitus.

Ophthalmic examination

  1. The BCVA: after refraction, BCVA was estimated using Landolt's broken ring chart, which was recorded as its decimal equivalent.
  2. Slit-lamp biomicroscopy: the cornea was examined for evidence of corneal scars, corneal edema, or keratic precipitates; the anterior chamber was examined for depth, regularity, aqueous flare, and cells; and applanation tonometry to record baseline intraocular pressure.
  3. Fundus examination: auxiliary lenses (+78 D lenses) were used to examine central and midperipheral retina to exclude possible pathology, for example, cystoid macular edema, retinal breaks, and macular scars.


Special investigations

The Pentacam Scheimpflug system (WaveLight Oculyzer, New York, USA) was used to measure corneal thickness, thinnest location, steepest K, and measure objectively the corneal and lens densitometry values. The Scheimpflug system quantifies the density of the cornea and the lens on a scale from 0 to 100. Peak densitometry values at the nearest axis (90–270) and its perpendicular axis (0–180) are recorded directly from the line appearing in the Scheimpflug image.

The surgical technique

CXL procedure was carried out by the same surgeon to minimize the bias.

The surgical technique was as follows:

The corneal CXL procedure was performed using CCL-365 vario (PESCHKE Trade GmbH, Huenenberg, Switzerland) applied every 3 min for 30 min and VEGA (AMD Radeon RX Vega 8, Italy) applied every 3 min for 10 min. The procedure began with instilling a topical anesthetic agent. The epithelium was mechanically scraped within the central 7.0-mm diameter area. Riboflavin (0.1% solution, 10 mg riboflavin 5-phosphate in 10 ml dextran 20% solution) was applied every 3 min for 30 min until the stroma was completely saturated and aqueous was stained yellow. UVA irradiation was performed using UVA system. Before treatment, the intended 9 mW/cm2 surface irradiance was calibrated (5.4 J/cm2 surface dose after 10 min). During treatment, riboflavin solution was applied every 3 min to ensure saturation and balanced salt solution was applied every 5 min to moisten the cornea. A drop of topical antibiotic was instilled, and a bandage contact lens is applied at the end of the surgery. Postoperative treatment included topical antibiotic eye drops four times daily and topical artificial tears were also used four times daily for 1 month, and in case of stromal haze, fluoroethylene eye drops were used three times daily for 2 weeks. Vega CSO constructed the Vega device with solid-state diode-emitting UVA rays peaking at 370 nm. The system has an integrated ¼ camera. The distributor, Sooft Italia, produced Ricrolin (riboflavin 0.1% solution) in 1-ml syringes for the standard CXL procedure and Ricrolin-TE in 1-ml syringes for the transepithelial CXL procedure.

Postoperative evaluation during the follow-up visits at 1, 3, and 6 months included BCVA and UCVA, which were clinically assessed; slit-lamp examination was done by the same examiner to detect changes in corneal haze; and cornea densitometry and lens densitometry are measured using the Scheimpflug image taken at the same axes as at the baseline visit. Moreover, the Pentacam Kmax and the thinnest pachymetry were recorded.

Concerning the complication of corneal cross-linking

There were no intraoperative complications in our study, whereas for the postoperative complications, corneal haze is seen in all cases. There were no reported cases of infectious keratitis, vascularization, or cases of decreased BCVA.

Statistical analysis

Results were tabulated and statistically analyzed using a personal computer using Microsoft Excel 2016 and SPSS, version 21 (SPSS Inc., Chicago, Illinois, USA). Statistical analysis was done using descriptive statistics: for example, percentage (%), mean, and SD, and analytical statistics: Student's t test, χ2 test, paired t test, Fisher's exact test, and correlation coefficient test and cutoff values by receiver operating characteristic curve. A value of P less than 0.05 was considered statistically significant.


  Results Top


The mean UCVA and BCVA preoperatively were 0.21 ± 0.11 and 0.49 ± 0.16, respectively, in group I and 0.4 ± 0.1 and 0.5 ± 0.06, respectively, in group II. After 1 month postoperatively, it changed to 0.12 ± 0.07 and 0.38 ± 0.15, respectively, in group I and 0.35 ± 0.2 and 0.4 ± 0.1, respectively, in group II. After 3 months, it changed to 0.21 ± 0.09 and 0.48 ± 0.15, respectively, in group I and 0.38 ± 0.2 and 0.55 ± 0.1, respectively, in group II, and after 6 months, it changed to 0.28 ± 0.09 and 0.58 ± 0.14, respectively, in group I and 0.45 ± 0.3 and 0.6 ± 0.2, respectively, in group II. The preoperative mean spherical equivalence (SE) was − 5.23 ± 0.51 and − 5.75 ± 0.7, which decreased to − 5.25 ± 0.41 and − 6.25 ± 1.1 at 1 month postoperatively and to − 5.90 ± 0.67 and − 5.8 ± 0.4 after 3 months postoperatively, and to − 5.28 ± 0.45 and − 5.5 ± 0.6 after 6 months postoperatively, in groups I and II, respectively [Table 1].
Table 1: Uncorrected visual acuity, best-corrected visual acuity, and spherical equivalence preoperatively and after 6 months among the two studied groups

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Moreover, we assessed the changes of Kmax with CXL. The preoperative mean Kmax was 52.10 ± 4.73 and 50.2 ± 2.01, which changed to 50.64 ± 4.64 and 48.7 ± 1.8 after 1 month postoperatively, to 49.62 ± 11.03 and 49.5 ± 1.9 after 3 months, and to 51.83 ± 4.70 and 50.1 ± 1.9 after 6 months postoperatively, in groups I and II, respectively. Regarding corneal thickness, the preoperative mean corneal thinnest location thickness was 457.77 ± 28.39 and 466 ± 23.8, which decreased to 437.81 ± 29.12 and 426.5 ± 20.7 after 1 month, to 444.81 ± 26.79 and 446.1 ± 16.2 after 3 months, and became 431.23 ± 92.94 and 462 ± 15.6 after 6 months postoperatively, in groups I and II, respectively. Mean corneal thinnest location thickness was significantly improved after 30 min (462 ± 15.6) than 10 min (431.23 ± 92.94) [Table 2].
Table 2: Mean Kmax and thinnest location at 1, 3, and 6 months after corneal cross-linking among the two studied groups

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We assessed the changes of corneal densitometry with CXL before as well as at 1, 3, and 6 months after. The mean corneal density 0–180 and corneal density 90–270 preoperatively were 17.44 ± 0.49 and 17.36 ± 0.95, respectively, in group I, and 17.3 ± 1.8 and 17.4 ± 2.06, respectively, in group II, which changed after 1 month postoperatively changed to 25.30 ± 0.76 and 27.20 ± 0.63, respectively, in group I and 26.9 ± 2.6 and 28.9 ± 3.1, respectively, in group II; after 3 months changed to 21.01 ± 0.79 and 20.66 ± 0.66, respectively, in group I and 22.6 ± 2.3 and 22.6 ± 2.4, respectively, in group II; and after 6 months changed to 19.22 ± 0.74 and 18.45 ± 0.69, respectively, in group I and 20.7 ± 2.01 and 19.9 ± 2.4, respectively, in group II. The mean lens density 0–180 and lens density 90–270 preoperatively were 12.67 ± 0.94 and 13.10 ± 0.90, respectively, in group I and 12.9 ± 2.3 and 13.2 ± 2.3, respectively, in group II, which changed after 1 month postoperatively to 12.76 ± 0.95 and 13.51 ± 0.88, respectively, in group I and 12.9 ± 2.3 and 13.6 ± 2.3, respectively, in group II; after 3 months changed to 12.85 ± 0.92 and 13.51 ± 0.88, respectively, in group I and 13.0 ± 2.4 and 13.6 ± 2.6, respectively, in group II; and after 6 months changed to 13.01 ± 0.92 and 13.04 ± 0.86, respectively, in group I and 13.2 ± 2.4 and 13.1 ± 2.3, respectively, in group II [Table 3].
Table 3: Corneal and lens densitometry at 1, 3, and 6 months after corneal cross-linking among the two studied groups

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Moreover, Pearson's correlation was conducted between thinnest location and Kmax as well as corneal and lens density. The correlation between them did not reach statistical significance level (P > 0.05). There was an exception in group I, where the thinnest location was significantly negatively correlated with Kmax preoperatively (P = 0.008) and at 1 month postoperatively (P = 0.046). Moreover, thinnest location was significantly positively correlated with corneal density 180 at 6 months postoperatively (P = 0.001) [Table 4].
Table 4: Plots the correlation for all variables among the two studied groups

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Regarding contrast sensitivity after 10 min using Pelli Robson contrast sensitivity Test, the average 1-month CS for all patients was 1.41 ± 0.07 log CS, which increased to 1.49 ± 0.05 log 3 months postoperatively and then increased to 1.55 ± 0.05 log at the final follow-up examination, whereas the contrast sensitivity after 30 min, the average 1-month CS for all patients was 1.40 ± 0.06 log CS, which increased to 1.34 ± 1.80 log 3 months postoperatively and then increased to 1.52 ± 0.48 log at the final follow-up examination. [Table 5] summarizes the CS data and demonstrates that there was no significant difference throughout the study period between the studied groups.
Table 5: Contrast sensitivity before and after cross-linking between the studied groups

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  Discussion Top


This study showed that there were no statistically significant differences between the studied groups regarding age, sex, eye side, BCVA, and SE. This agreed with Ng et al. [7], who reported there were no significant differences in all baseline parameters between the two groups (P ≥ 0.11). Moreover, our results were confirmed by Woo et al. [8], who found the mean age of the patients was 29.16 ± 7.3 and 27.88 ± 7.1 years in the corneal CXL and accelerated cross-linking (KXL) groups, respectively. Most patients in each group were males, with 37 (78.7%) male patients in the KXL group and 21 (72.4%) male patients in the CXL group. There was no statistical difference between the two groups in terms of demographic parameters. Moreover, our results were close to those found by Helaly and Osman [9]. They found the postoperative follow-uP values for BCVA and the steepest K, where at baseline, the BCVA was 0.51 ± 0.21, and at 1 month postoperatively, the BCVA decreased to 0.38 ± 0.43 (a decrease of 0.13). It correlated with cornea densitometry values at 1 month. The BCVA improved in the following visits until it reached 0.75 ± 0.15 at 12 months postoperatively (increase from baseline by 0.24). This agreed with the study conducted by Woo et al. [8], who revealed that the CXL and KXL groups showed improvement in BCVA of 0.11 and 0.08 log MAR units, respectively, at 12 months compared with baseline. Moreover, Shetty et al.[10] found that although there was an improvement in the corrected distance visual acuity in all groups at 12 months, the change was not significant in the 30 mW/cm2 group, and the most improvement occurred in the 18 mW/cm2 group. However, no such intergroup difference was found in our study. Various authors have reported a reduction in SE and cylinder error in both accelerated and conventional cross-linking but with no significant difference between the two groups [11]. In contrast to our results, Woo et al.[8] showed no difference between the two groups at 12 months when the change in SE value was considered. In addition, there was a conflict with Böhm et al. [12], as they found that the UCVA and BCVA showed no significant changes 3 months after accelerated CXL.

Regarding the assessment of the changes of Kmax with CXL, our results agreed with majority of earlier studies, which demonstrated a decrease in Kmax after CXL [13]. These results were confirmed by Böhm et al. [12], who reported that maximum keratometry and simulated keratometry showed no significant changes, which is in line with the findings of Toker et al. [14], reporting that 30 mW/cm2 accelerated CXL treatment modalities appeared to be effective in stabilizing KC progression. However, they were less effective in achieving topographic improvement, showing no changes in keratometric values compared with baseline. In contrast to prior studies, Chatzis and Hafezi [15], in a retrospective study on 49 eyes of 42 patients with 3-year follow-up of 11 eyes, reported the initial stabilization but late progression, with increase in the mean Kmax during months 24 and 26, emphasizing the transient effect of CXL in pediatrics. Moreover, a study by Mita et al.[16] found a significant reduction in maximum keratometry 6 months after 30 mW/cm2 accelerated cross-linking with the KXL system, and this disagreed with our results. This difference may be owing to the different length of follow-up periods after treatment.

Regarding the thinnest pachymetry, our results are confirmed by Helaly and Osman [9], who indicated that the mean thinnest pachymetry decreased markedly at 1 month postoperatively by 51 μm. It increased gradually to reach a near baseline level at 12 months postoperatively. This is in agreement with a previous report on transient thinning of the cornea with ultrasound pachymetry after CXL treatment [17]. Moreover, our results were in accordance with Gutiérrez et al. [18], who reported detectable densitometry changes in the absence of concomitant clinical haze beyond grade 1. However, they did not report densitometry changes on the basis of separate layers and concentric zones. This also agreed with Shen et al. [19], who reported a dramatic decrease in the densitometry values over 12 months following accelerated (320 s) transepithelial CXL. However, the latter retrospective cohort study enrolled only 17 KC eyes, of older age group (22.4–31.4 years), exposed to 45 mW/cm2 (total energy: 7.3 J/cm2) irradiance of epithelium-on ACXL. Our results were conflicting with Eissa et al. [20], as the pachymetry map in their study showed a nonstatistically significant decrease in preoperative thinnest location by a mean of 0.32 ± 0.85 D, and also in contrast with Gutiérrez et al.[18] and Pircher et al. [21], who reported a peak of corneal densitometry in the first months after standard CXL that returned to preoperative values ∼1 year after CXL. Changes in the corneal thickness seem to reflect a compactness of the corneal stroma. The reduction in corneal thickness between 1 and 3 months may be a result of progressive reepithelization and compaction of stromal lamellae after cross-linking. There is also evidence that pachymetry with Scheimpflug imaging system may underestimate corneal thickness in the early postoperative period owing to stromal haze and changes in reflectivity.

Moreover, in the same line with our results regarding mean densitometry, Helaly and Osman[9] reported the mean Scheimpflug corneal densitometry at baseline was 16.30 ± 1.90. At 1 month postoperatively, the corneal densitometry increased to 28.81 ± 4.33. At 1 month, there was a statistically significant increase in the clinical haze by 1.40. Between 6 and 12 months postoperatively, there was a decrease in the corneal densitometry values by 4.78, which was statistically significant. At 12 months postoperatively, the corneal densitometry did not return to baseline levels. In contrast, Koc et al.[22] found that corneal densitometry values increased after accelerated corneal CXL and did not return to preoperative values 12 months after CXL [21]. Moreover, the study by Böhm et al.[12] revealed an increase of corneal densitometry in all three stromal layers (anterior, middle, and posterior) 3 months after accelerated CXL, though only a significant increase in the anterior stromal layer (120 lm). Different irradiation procedures and their effect on densitometry distribution may be the cause of the variation in results.

Regarding lens densitometry, there were no statistically significant differesnces between the two studied groups. This was in line with Vinciguerra et al. [23], who studied 12 eyes with a 36-month follow-up and evaluated a 1.2-mm diameter cylindrical-shaped central section of the lens. The authors did not find any deterioration of the crystalline lens transparency or permanent negative adverse effects on the cornea and endothelium. Grewal et al.[24] also agreed with these results and reported no change in crystalline lens density 12 months after CXL in 102 patients. On the contrary, another study showed that there was a noticeable difference at the mean lens density reported by Baradaran-Rafii et al. [25], where the mean lens density in the CXL group was 6.68 ± 0.58% at baseline and 6.77 ± 0.53% at the last visit. The corresponding values of the control group were 6.53 ± 0.27 and 6.39 ± 0.31%, respectively. However, there was no significant difference between the study groups at baseline or 6 months later.

This noticeable difference in the mean density values may be explained by the inherent variations encountered with age, sex, and race as well as different method of examination. In the current study, Pearson correlation was conducted between thinnest location and Kmax as well as corneal and lens density. Our results agreed with Kasai et al. [26], who reported that there was a positive correlation between Kmax and the preoperative thinnest corneal thickness (TCT). In another study performed by Soliman et al. [27], Pearson correlation was conducted between thinnest location and Kmax as well as corneal and lens density, and no significant correlations were encountered between the study variables. To extend the reliability of obtained results, the value of the change from baseline was calculated for each variable.

Moreover, in the study conducted by Wang et al. [28], they found a significant medium negative correlation between keratectasia area (KEA) and TCT preoperative. TCT is one of important signs of KC progression, and TCT in a suspect KC is significantly lower than normal eyes and higher than the KC group. Therefore, the more serious KC led to the lower TCT and larger KEA. We suspect that the KEA may be beneficial in monitoring KC as TCT.


  Conclusion Top


Our results showed a significant improvement in corneal thinnest location thickness at the final follow-up examination after 30 min than 10 min. Moreover, thinnest location was correlated inversely with Kmax after 1 month postoperatively. However, thinnest location was significantly positively correlated with corneal density at 6 months postoperatively. Moreover, a significant improvement in contrast sensitivity was found at the final follow-up examination after 10 min than 30 min, but the difference between them did not reach statistical significance.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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