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Sulfur Hexafluoride (S[F.sub.6]) versus Perfluoropropane ([C.sub.3][F.sub.8]) in the Intraoperative Management of Macular Holes: A Systematic Review and Meta-Analysis.

1. Introduction

Macular hole surgery was first described by Kelly and Wendel in 1991 [1]. Although their 5-step technique has remained largely unchanged, debate still exists concerning several key aspects of the procedure [2]. These include whether to peel the internal limiting membrane (ILM), the use and type of dye, and the duration of face-down positioning following surgery [3, 4].

Another heatedly debated aspect is the choice of tamponading agent [3, 5, 6]. The most commonly used compounds are sulfur hexafluoride (S[F.sub.6]) and perfluoropropane ([C.sub.3][F.sub.8]). However, hexafluoroethane ([C.sub.2][F.sub.6]), room air, and silicone oil are also employed [7]. Although the procedure was initially described with use of S[F.sub.6], subsequent clinical trials used [C.sub.3][F.sub.8] further adding to the debate [1, 8-10]. To the authors' best knowledge, no systematic review or metaanalysis has yet been published, comparing the two agents.

The aim of this study was to systematically review the literature for studies that compared S[F.sub.6] to [C.sub.3][F.sub.8] as a tamponade agent in the intraoperative management of macular hole surgery, perform a pooled meta-analysis of the data, and discuss any differences found with respect to clinical outcomes and adverse effects.

2. Materials and Methods

2.1. Literature Search. A systematic literature search was conducted using MEDLINE, Scopus, Google Scholar, and The Cochrane Library, reviewing all available published clinical studies up to October 2018. The following keywords were used, in various combinations: macular hole, MH, sulfurhexafluoride, sulfur hexafluoride, S[F.sub.6], per fluoropropane, [C.sub.3][F.sub.8], gas, short-acting, long-acting, tamponade, bubble, pneumatic, and retinopexy. A bibliographic search of relevant studies identified additional publications. A flow diagram of the screening and inclusion process is illustrated in Figure 1.

2.2. Eligibility Criteria. Full publications in English that directly compare S[F.sub.6] and [C.sub.3][F.sub.8] in the intraoperative management of macular hole surgery, in terms of primary closure, complication rates, and clinical outcomes were included (not abstracts or letters to the editor). Studies performed on animal or cadaver eyes, as well as case reports and nonempirical opinion articles, were excluded.

2.3. Screening and Synthesis. The review process was conducted under the guidance of the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) criteria to support reporting [11]. Two reviewers (IH and MM) independently implemented the search strategy for relevant publications. Selected publications were then approved by the senior investigator who also devised the search strategy (YB).

2.4. Statistical Analyses. To better illustrate the main anatomical outcome of primary closure, forest plots were created using a weighted summary of proportion meta-analysis. Analysis was performed separately for S[F.sub.6] and [C.sub.3][F.sub.8]. A random effects model was used (as implemented by Der-Simonian and Laird, 1986 [12]), and corresponding [I.sup.2] heterogeneity estimates were generated. Data were tabulated and analyzed using SPSS for Windows version 22.0 software by IBM Inc. (Armonk, NY, USA). Graphs were created using MedCalc software version 16 (Mariakerke, Belgium).

3. Results

Data comparing the use of S[F.sub.6] and [C.sub.3][F.sub.8] for macular hole surgery were extracted from nine studies published during 2000 to 2017 (Table 1), studying a total of 4,715 patients. Two of the studies were randomized by design and included a total of 206 patients. Two studies prospectively enrolled patients without randomization (170 patients), and the remaining five were retrospective or registry based. Figure 1 illustrates the flow of the inclusion process.

3.1. Intraoperative Management. Several differences existed between the studies with respect to the surgical technique. The first relates to ILM removal as a routine part of the operation.

ILM peeling was routinely performed in six of the nine studies. In two studies (Essex et al. [4] and Tognetto et al. [7]), a majority of patients (97.7% and 67.7%, respectively) underwent ILM peeling while the remainder did not. The authors elected not to routinely perform ILM peeling of prospectively enrolled patients in only one study (Mulhern et al.) [16].

Tognetto et al. expanded their investigation, comparing the outcomes of patients who underwent ILM peeling with those who had not [7]. They analyzed the retrospective data of 1,627 patients from different countries, who had been operated on for idiopathic macular hole. They found that ILM peeling improved hole closure only for longstanding macular holes or those in advanced stages [7].

A second aspect in which studies differed was the choice of gas concentration. The S[F.sub.6] concentration was 20% in four of the nine studies. Mulhern et al. used 23%, Kumar et al. used 25%, and Briand et al. used between 20 and 25% S[F.sub.6]. The [C.sub.3][F.sub.8] concentrations similarly varied, ranging from 13% used by Modi et al. to 18% by Kumar et al. However, most used concentrations ranged between 14% and 16% [C.sub.3][F.sub.8] (Table 1).

3.2. Postoperative Management. Face-down positioning varied between studies. Most studies recommended two to seven days of prone positioning; however, some (e.g., Mulhern et al.) requested patients who received S[F.sub.6] maintain a prone head position for up to 4 weeks [16].

A registry-based analysis by Essex et al. sheds further light on this topic [4]. They analyzed the outcome of 2,367 patients from Australia and New Zealand who underwent primary idiopathic macular hole surgery. Approximately 26% of these patients were not advised to remain in prone position postoperatively, and among those who were advised, most were instructed to remain prone between three and seven days. Essex et al. further compared the outcomes between patients who were not advised a postoperative facedown position to those who were and found that no prone positioning was noninferior for holes of less than 400 [micro]m in diameter, while for larger holes noninferiority could not be concluded [4].

3.3. Primary Anatomical Closure. Most studies used anatomical closure as the primary outcome; their results are summarized in Table 1. Closure rates ranged from 85% to 100%, with most in the 90% to 95% range.

A comparison of S[F.sub.6] and [C.sub.3][F.sub.8] showed similar rates of closure in eight of the nine studies, including the two randomized controlled studies by Casini et al. [3, 5]. One study by Essex et al. using a more stringent noninferiority analysis with a relatively narrow noninferiority margin (5%) also demonstrated noninferiority of S[F.sub.6] compared to [C.sub.3][F.sub.8] [4]. Only one study by Tognetto et al. reported a higher success rate with S[F.sub.6] (93.6% versus 87.2%); however, the authors provide no statistical foundation for this claim [7].

Several studies further analyzed subgroups in an attempt to detect a subset of patients, which might benefit from one agent over the other. Modi et al. examined different hole sizes, stages, and durations; Casini et al. also examined different stages; and Kim et al. compared the agents independently for different stages, durations of symptoms, presence of posterior vitreous detachment, and whether indocyanine green dye was used for ILM peeling [3, 6, 15].

They all found S[F.sub.6] to produce results similar to [C.sub.3][F.sub.8] regardless of the subgroup analyzed (Table 1).

3.4. Visual Acuity. Six studies reported visual acuity outcomes following surgery [3, 5, 6, 14-16]. All showed similar results when comparing S[F.sub.6] to [C.sub.3][F.sub.8] at one to six months of follow-up (Table 1). Improvement following S[F.sub.6] gas ranged from 2.7 to 5.9 Early Treatment Diabetic Retinopathy Study (ETDRS) lines, while following use of [C.sub.3][F.sub.8] ranged between 2.7 and 6.9 ETDRS lines. Five of the six studies report comparative statistics on visual improvement between groups, and all find no significant differences (Table 1). The randomized trial by Casini et al. as well as the prospective cohort study by Xirou et al. showed that visual acuity was initially better in the group treated with S[F.sub.6] but was eventually found to be similar [3, 14].

3.5. Complications. Most studies reported on short-term and long-term complication rates in each group. The randomized controlled trial by Briand et al. showed similar results in terms of cataract development and extraction, a similar time interval between surgery and cataract extraction (p = 0.184) and similar rates of retinal tears (4% vs. 7%), retinal detachment (4% vs. 0%), and ocular hypertension (21% vs. 19%, all p = 1.0) [5]. The retrospective report by Modi et al. on 177 patients revealed a decreased incidence of cataract and ocular hypertension (1.99 vs. 4.02 mmHg) in the group treated with S[F.sub.6], as well as a nonsignificantly lower incidence of glaucoma (9.0% vs 6.1%) [6]. Xirou et al., in a prospective study on 46 patients, revealed similar elevations of intraocular pressure [14]. Kim et al. reported similar rates of cataract development; however, myopic shift rates were greater in the [C.sub.3][F.sub.8] group (SF6: -0.82 diopters vs. [C.sub.3][F.sub.8]: -1.42 diopters for phakic patients, p = 0.016). Finally, in the prospective trial by Mulhern et al., similar rates of posterior subcapsular cataract were seen (55% after [C.sub.3][F.sub.8] vs. 37% after S[F.sub.6]; p = 0.20) and mean intraocular pressure spike maximum was nonsignificantly higher in the S[F.sub.6] group (32.5 mmHg vs. 23.7mmHg; p = 0.131) [16].

3.6. Pooled Analysis of Primary Closure. Forest plots of proportion of patients who achieved anatomical closure with each compound are presented in Figures 2 and 3. Meta-analytic pooling of the closure rates in the S[F.sub.6] group resulted in 91.73% (95% confidence interval: 88.40 to 94.55, [I.sup.2]: 38.03%, p value for heterogeneity = 0.126). For the patients who received [C.sub.3][F.sub.8], the pooled anatomical closure rate was 88.36% (95% confidence interval: 85.88 to 90.63, [I.sup.2]: 0.0%, p value for heterogeneity = 0.864).

4. Discussion

In this study, a systematic review and meta-analysis of studies comparing S[F.sub.6] and [C.sub.3][F.sub.8] gas tamponades for macular hole surgery was performed. Macular hole closure rates were found to be similar regardless of whether S[F.sub.6] or [C.sub.3][F.sub.8] was used and were typically in the 90-95% range. Visual acuity outcomes were also similar but tended to improve faster with S[F.sub.6]. Rates of complications (including cataract formation, ocular hypertension, and retinal tears) varied among studies and appeared to be inconsistently related to either agent.

Following macular hole repair, contact of the gas bubble with the retina causes the extrusion of subretinal fluid and maintains anatomical position, as well as possibly providing a scaffold for cellular proliferation [14]. It therefore seems reasonable that a larger, longer-acting, bubble would provide further benefit. However, some evidence suggests that hole closure occurs very early in the postoperative period, perhaps as early as the first 24 hours [17]. A recent study by Masuyama et al. showed that repair of the macular hole typically occurs between 4 and 7 days postoperatively and is presumed to be facilitated by ganglion and Muller cells [18].

Long-lasting gasses (such as [C.sub.3][F.sub.8]) may offer more extensive tamponade; however, they also impair vision longer. It is possible that such longer-acting agents are not required, considering the short timescales in which macular hole repair occurs. The outcomes of this review appear to support this notion, as use of S[F.sub.6] produced similar clinical outcomes to [C.sub.3][F.sub.8] in terms of both primary closure and visual outcomes.

This study has several limitations. It included nonrandomized trials in the analysis. However, given the small number of randomized studies performing a direct comparison of S[F.sub.6] and [C.sub.3][F.sub.8] for macular hole surgery, we elected to include relevant retrospective and registry-based studies, in order to increase the power of the meta-analysis. Given the findings of this study, the need for more prospective randomized studies evaluating this comparison may be questionable. In addition, several differences between the studies concerning the surgical technique may have introduced biases to the analyses. However, we discussed and compared variations in surgical technique found across these studies.

5. Conclusions

To the authors' best knowledge, this is the first systematic review and meta-analysis comparing S[F.sub.6] and [C.sub.3][F.sub.8] as a tamponading agent for macular hole surgery. We found that S[F.sub.6] and [C.sub.3][F.sub.8] resulted in both similar visual outcomes as well as similar primary closure rates. Neither agent was clearly associated with increased risk of ocular hypertension, cataract formation, or other adverse events. Visual recovery with S[F.sub.6] tended to occur earlier. It is probable that shorter-acting tamponade agents such as S[F.sub.6] may be sufficient for macular hole surgery; we found no evidence to support [C.sub.3][F.sub.8] as the tamponade gas of choice.

Conflicts of Interest

The authors declare that they have no conflicts of interest.


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[15] S. S. Kim, W. E. Smiddy, W. J. Feuer, and W. Shi, "Outcomes of Sulfur hexafluoride (S[F.sub.6]) versus Perfluoropropane ([C.sub.3][F.sub.8]) gas tamponade for macular hole surgery," Retina, vol. 28, no. 10, pp. 1408-1415, 2008.

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[18] K. Masuyama, K. Yamakiri, N. Arimura, Y. Sonoda, N. Doi, and T. Sakamoto, "Posturing time after macular hole surgery modified by optical coherence tomography images: a pilot study," American Journal of Ophthalmology, vol. 147, no. 3, pp. 481-488, 2009.

Idan Hecht [ID], (1) Michael Mimouni [ID], (2,3) Eytan Z. Blumenthal, (2,3) and Yoreh Barak [ID], (2,3)

(1) Sackler School of Medicine, Tel-Aviv University, Tel Aviv, Israel

(2) Department of Ophthalmology, Rambam Health Care Campus, Haifa, Israel

(3) Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel

Correspondence should be addressed to Yoreh Barak;

Received 1 November 2018; Revised 13 February 2019; Accepted 28 February 2019; Published 12 March 2019

Guest Editor: Steve Charles

Caption: Figure 1: Flow diagram of the inclusion process. Flow diagram of the search and inclusion process based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [11].

Caption: Figure 2: Forest plot of the proportion of patients who achieved anatomical closure following the use of S[F.sub.6] gas. Meta-analytic pooling of the proportion of patients who achieved anatomical closure following surgery in the S[F.sub.6] group. Pooled estimate was 91.73% (95% confidence interval: 88.40% to 94.55%, [I.sup.2]: 38.03%, p value for heterogeneity = 0.126). Size of the squares is proportional to the number of cases in the study. Error bars represent 95% confidence intervals. The diamond shape represents the pooled estimate.

Caption: Figure 3: Forest plot of the proportion of patients who achieved anatomical closure following the use of [C.sub.3][F.sub.8] gas. Meta-analytic pooling of the proportion of patients who achieved anatomical closure following surgery with [C.sub.3][F.sub.8]: pooled estimate was 88.36% (95% confidence interval: 85.88% to 90.63%, [I.sup.2]: 0.0%, p value for heterogeneity = 0.864); size of the squares is proportional to the number of cases in the study. Error bars represent 95% confidence intervals. The diamond shape represents the pooled estimate.
Table 1: Publications reporting on clinical outcomes of macular
hole repair using either S[F.sub.6] or [C.sub.3][F.sub.8] gas

Study [Ref]           Year          Design

Modi et al. [6]       2017      Retrospective
                              comparative study
Casini et al. [3]     2016        Randomized
                               controlled trial
Essex et al. [4]      2016   Registry-based study
Briand et al. [5]     2015        Randomized
                               controlled trial
Kumar et al. [13]     2014    Prospective cohort
Xirou et al. [14]     2012    Prospective cohort
Kim et al. [15]       2008      Retrospective
                              comparative study
Tognetto et al. [7]   2006      Retrospective
                                 cohort study
Mulhern et al. [16]   2000       Prospective
                              comparative study

Study [Ref]             Number of patients

Modi et al. [6]           S[F.sub.6]: 67
                      [C.sub.3][F.sub.8]: 111
                            Total: 177
Casini et al. [3]         S[F.sub.6]: 70
                      [C.sub.3][F.sub.8]: 77
                            Total: 147
Essex et al. [4]         S[F.sub.6]: 1,653
                      [C.sub.3][F.sub.8]: 702
                           Total: 2,456
Briand et al. [5]         S[F.sub.6]: 31
                      [C.sub.3][F.sub.8]: 28
                             Total: 59
Kumar et al. [13]         S[F.sub.6]: 20
                      [C.sub.3][F.sub.8]: 42
                             Total: 62
Xirou et al. [14]         S[F.sub.6]: 23
                      [C.sub.3][F.sub.8]: 23
                             Total: 46
Kim et al. [15]           S[F.sub.6]: 38
                      [C.sub.3][F.sub.8]: 41
                             Total: 79
Tognetto et al. [7]      S[F.sub.6]: 1,004
                      [C.sub.3][F.sub.8]: 337
                           Total: 1,627
Mulhern et al. [16]       S[F.sub.6]: 31
                      [C.sub.3][F.sub.8]: 31
                             Total: 62

Study [Ref]           Postoperative facedown      Gas concentration
                       positioning duration

Modi et al. [6]       S[F.sub.6]: 45 minutes        20% S[F.sub.6]
                      of every hour (duration   13% [C.sub.3][F.sub.8]
                      NR) [C.sub.3][F.sub.8]:
                        45 minutes of every
                        hour (duration NR)
Casini et al. [3]       S[F.sub.6]: 2 days          20% S[F.sub.6]
                       [C.sub.3][F.sub.8]: 2    14% [C.sub.3][F.sub.8]
Essex et al. [4]       S[F.sub.6]: 0-14 days              NR
                             0-14 days
Briand et al. [5]       S[F.sub.6]: 7 days        20-25% S[F.sub.6]
                        [C.sub.3][F.sub.8]:     15% [C.sub.3][F.sub.8]
                              14 days
Kumar et al. [13]      S[F.sub.6]: 18 hours         25% S[F.sub.6]
                         daily for 3 days       18% [C.sub.3][F.sub.8]
                      [C.sub.3][F.sub.8]: 18
                      hours daily for 3 days
Xirou et al. [14]       S[F.sub.6]: 2 days          20% S[F.sub.6]
                       [C.sub.3][F.sub.8]: 2    14% [C.sub.3][F.sub.8]
Kim et al. [15]         S[F.sub.6]: 7 days          20% S[F.sub.6]
                       [C.sub.3][F.sub.8]: 7    16% [C.sub.3][F.sub.8]
Tognetto et al. [7]       S[F.sub.6]: NR                  NR
                      [C.sub.3][F.sub.8]: NR
Mulhern et al. [16]   S[F.sub.6]: 14-30 days        23% S[F.sub.6]
                       [C.sub.3][F.sub.8]: 6    16% [C.sub.3][F.sub.8]

Study [Ref]            ILM peeling        Anatomical closure

Modi et al. [6]         All cases          S[F.sub.6]: 86.4%
                                       [C.sub.3][F.sub.8]: 86.5%
Casini et al. [3]       All cases           S[F.sub.6]: 90%
                                        [C.sub.3][F.sub.8]: 91%
Essex et al. [4]      97.7% of cases      Mean of both 95.0%
                                           (individually NR)
Briand et al. [5]       All cases          S[F.sub.6]: 93.3%
                                       [C.sub.3][F.sub.8]: 92.9%
Kumar et al. [13]       All cases           S[F.sub.6]: 85%
                                       [C.sub.3][F.sub.8]: 90.5%
Xirou et al. [14]       All cases          S[F.sub.6]: 100%
                                        [C.sub.3][F.sub.8]: 96%
Kim et al. [15]         All cases           S[F.sub.6]: 90%
                                        [C.sub.3][F.sub.8]: 91%
Tognetto et al. [7]   67.7% of cases       S[F.sub.6]: 93.6%
                                       [C.sub.3][F.sub.8]: 87.2%
Mulhern et al. [16]   Not routinely        S[F.sub.6]: 96.7%
                        performed      [C.sub.3][F.sub.8]: 93.5%

Study [Ref]           Results: primary closure

Modi et al. [6]         Similar (p = 0.982),
                        irrespective of hole
                      size, stage, or duration
Casini et al. [3]       Similar, independent
                              of stage
Essex et al. [4]      S[F.sub.6] noninferior,
                       regardless of macular
                             hole size
Briand et al. [5]       Similar (p = 0.943)
Kumar et al. [13]        Similar (p = 0.67)
Xirou et al. [14]             Similar
Kim et al. [15]         Similar (p = 0.91),
                        regardless of stage,
                       duration of symptoms,
                        presence of PVD, and
                       use of ICG dye for ILM
Tognetto et al. [7]     Higher success rates
                          with S[F.sub.6]
Mulhern et al. [16]      Similar (p = 1.0)

Study [Ref]                Results: visual
                            improvement *

Modi et al. [6]         S[F.sub.6]: 2.7 lines
                        (0.900 [+ or -] 0.383
                       to 0.629 [+ or -] 0.375
                        logMAR) at 3-6 months
                              4.2 lines
                       (1.03 [+ or -] 0.39 to
                         0.61 [+ or -] 0.40
                        logMAR) at 3-6 months
                           No significant
                       difference (p = 0.066)
Casini et al. [3]       S[F.sub.6]: 5.9 lines
                       (0.894 to 0.301 logMAR)
                             at 1 month
                       [C.sub.3][F.sub.8]: 6.9
                        lines (0.965 to 0.272
                         logMAR) at 1 month
Essex et al. [4]                 NR
Briand et al. [5]       S[F.sub.6]: 3.5 lines
                            at 12 months
                       [C.sub.3][F.sub.8]: 3.4
                         lines at 12 months
                           No significant
                       difference (p = 0.787)
Kumar et al. [13]                NR
Xirou et al. [14]       S[F.sub.6]: 3.8 lines
                       (0.67 [+ or -] 0.20 to
                         0.29 [+ or -] 0.12
                         logMAR) at 6 months
                      2.8 lines (0.90 [+ or -]
                        0.10 to 0.62 [+ or -]
                      0.23 logMAR) at 6 months
                           No significant
                        difference (p = 0.06)
Kim et al. [15]         S[F.sub.6]: 4.9 lines
                         (0.86 [+ or -] 0.41
                        to 0.37 [+ or -] 0.43
                        logMAR) at 12 months
                           5.4 lines (0.99
                        [+ or -] 0.43 to 0.45
                      [+ or -] 0.35 logMAR) at
                              12 months
                           No significant
                        difference (p > 0.30)
Tognetto et al. [7]              NR
Mulhern et al. [16]     S[F.sub.6]: 2.8 lines
                       (0.86 [+ or -] 0.18 to
                         0.575 [+ or -] 0.31
                         logMAR) at 3 months
                       [C.sub.3][F.sub.8]: 2.7
                        lines (0.88 [+ or -]
                        0.21 to 0.61 [+ or -]
                      0.37 logMAR) at 3 months
                      No significant difference
                             (p = 0.719)

Study [Ref]           Results: complications

Modi et al. [6]       S[F.sub.6] exhibited a
                      decreased incidence of
                        cataract and ocular
                      hypertension (1.99 vs.
                       4.02 mmHg) as well
                       as a nonsignificantly
                        lower incidence of
                        glaucoma (9.0% vs.
Casini et al. [3]      Patients treated with
                      S[F.sub.6] experienced
                        greater improvement
                        of visual acuity at
                      1 week postoperatively
                       (p < 0.01) but not at
                              1 month
Essex et al. [4]                NR
Briand et al. [5]       Similar in terms of
                       cataract development
                        and extraction and
                          adverse events
Kumar et al. [13]               NR
Xirou et al. [14]      Patients treated with
                      S[F.sub.6] experienced
                      greater improvement of
                      visual acuity initially
                      but was similar in the
                        following 6 months.
                       Similar elevations of
                       intraocular pressure
Kim et al. [15]        Cataract development
                        was similar. Myopic
                       shift was greater in
                      the [C.sub.3][F.sub.8]
                         group (p = 0.016)
Tognetto et al. [7]             NR
Mulhern et al. [16]   Incidence of posterior
                       subcapsular cataract
                       was similar. Mean IOP
                         spike maximum was
                      nonsignificantly higher
                      in the S[F.sub.6] group

NR, not reported; [C.sub.3][F.sub.8], perfluoropropane;
S[F.sub.6], sulfur hexafluoride; ILM, internal limiting
membrane; PVD, posterior vitreous detachment; ICG,
indocyanine green; IOP, intraocular pressure.
* Expressed in Early Treatment Diabetic Retinopathy
Study (ETDRS) chart lines.
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Article Details
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Author:Hecht, Idan; Mimouni, Michael; Blumenthal, Eytan Z.; Barak, Yoreh
Publication:Journal of Ophthalmology
Article Type:Clinical report
Date:Mar 31, 2019
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