Changes in choroidal thickness in advanced diabetic retinopathy treated with pan-retinal photocoagulation using a pattern scanning laser versus a conventional laser

DOI: https://doi.org/10.21203/rs.2.9377/v2

Abstract

Background :  To compare the effect of pan-retinal photocoagulation (PRP) using pattern scanning or conventional laser on subfoveal choroidal thickness (SFChT). Methods :  Thirty-eight patients (64 eyes) with advanced diabetic retinopathy (DR) who underwent PRP using pattern scanning or conventional laser were included. Changes in SFChT were compared with baseline values at 1, 3, 6, and 12 months after PRP using swept-source optical coherence tomography. Results : The conventional laser group showed statistically significant decrease in SFChT at 1, 3, 6, and 12 month after PRP ( P <0.001). SFChT was significantly decreased at 3 ( P = 0.025), 6 ( P = 0.004), and 12 months ( P < 0.001) after treatment in the pattern laser group. Conclusion : Eyes with advanced DR showed a significant reduction in SFChT over 12 months regardless of the type of laser used; however, the reduction was sooner after conventional laser than after pattern laser.

Background

Diabetic retinopathy (DR) is a common complication of diabetes and a leading cause of vision loss in working-aged populations in both advanced and developing countries.[1] Pan-retinal photocoagulation (PRP) is considered the gold standard treatment for severe non-proliferative diabetic retinopathy (NPDR) and proliferative retinopathy (PDR) according to the Early Treatment Diabetic Retinopathy Study (ETDRS).[2] Traditionally, PRP has been performed using various wavelengths, including argon green (514 nm) or diode (810 nm) lasers. However, these lasers have recently been replaced by a pattern scanning laser system that uses a frequency-doubled 532-nm wavelength Nd:YAG laser to avoid patient discomfort and fatigue. Furthermore, the reduced pulse duration required when using the pattern scanning laser may be less painful because of decreased thermal diffusion into the choroid.[3]

Several studies have showed that SFChT is affected by treatment, including PRP and intravitreal injections.[4-9] However, there have been no studies comparing the effect of conventional laser and pattern scanning laser systems on choroidal thickness. It has been reported that PRP performed with the pattern scanning laser is less effective than that performed with a traditional laser for regression of retinal neovascularization in eyes with high-risk PDR.[10] The purpose of this study was to compare the effect of PRP on choroidal thickness using the conventional laser and the pattern scanning laser.

Patients and Methods

Subjects

This retrospective interventional comparative study was approved by the institutional review board committee of Chung-Ang University Hospital, Seoul, South Korea, and adhered to the tenets of the Declaration of Helsinki. The medical records of consecutive patients who underwent PRP for severe NPDR or PDR at the Chung-Ang University Hospital between September 1, 2015 and July 31, 2017 and were followed up for at least 12 months were retrospectively reviewed. Signed informed consent was obtained from all patients before each PRP treatment session. The exclusion criteria included prior retinal surgery or photocoagulation, a history of ocular trauma, any history of eye disease, retinal or choroidal disease, refractive error more than ± 3.0 diopters, and systemic disease other than diabetes.

The patients who received anti-VEGF injection before the baseline and during the follow-up periods were excluded. And the patients who underwent cataract surgery within 6 months before the baseline and during follow-up periods were also excluded. 

Eyes with low-quality OCT images (a low image quality index <90) due to or media opacities such as vitreous hemorrhage and cataract were also excluded. However, the eyes with good-quality OCT images and localized vitreous hemorrhage or peripheral cortical lens opacity were not excluded.

Study protocol

All patients underwent a comprehensive ophthalmologic evaluation, including measurement of best-corrected visual acuity (BCVA), intraocular pressure, and refractive error, slit-lamp examination, fundus examination, fluorescein angiography, and swept-source OCT. Fluorescein angiography was performed to determine the severity of DR using an ultra-wide-field confocal scanning laser ophthalmoscope (Panoramic 200MA™, Optos PLC, Dunfermline, UK). The severity of DR was graded according to the ETDRS retinopathy severity scale.[2,11,12] Swept-source OCT (DRI Triton OCT, Topcon, Tokyo, Japan) was also performed. This machine uses a wavelength of 1050 nm and a scan speed of 100,000 A-scans per second, and yields an axial resolution of 8 μm and a depth of 2.4 dB/mm. OCT B-scan imaging was performed with a 6 × 6 mm cube scan and a 9 mm five-line cross-scan.

The central retinal thickness (CRT) was obtained from an automatic thickness map that was created according to the conventional ETDRS grid in 6 × 6 mm cube scan mode after confirmation of the position of the grid.

SFChT was measured using a built-in caliper tool as the distance between the Bruch membrane and the choroid-sclera interface at the fovea.  Two independent observers (NP, JTK), who were masked to the clinical data for each patient, measured the choroidal thickness and the averaged values were used for the statistical analysis.

Pan-retinal Photocoagulation

PRP was performed by a single retinal specialist (JTK) under topical anesthesia with a 532-nm solid-state green diode laser (OcuLight GLx laser, Iridex Corp. Mountain View, CA, USA) or a 532-nm frequency-doubled neodymium-doped yttrium aluminum garnet (Nd-YAG) solid-state pattern scan laser (Valon pattern laser, Dual Laser Ltd. Oy, Finland) using a TransEquator contact lens (VolkOptical Inc., Mentor, OH, USA). The patients were classified into a conventional laser group or a pattern laser group as appropriate. The patients received PRP using conventional diode laser before January 2017, and PRP using pattern laser was performed from January 2017 (due to acquisition of the laser). PRP was placed from the vascular arcades to the peripheral retina. PRP was performed in all eyes in both groups in two sessions one week apart.

For conventional laser, the laser power was adjusted from 200 mW until a gray-white opacity was achieved. The pulse duration was 200 ms and the spot size was 200 µm. For pattern laser, a 5 × 5- multispot array with a 200-µm spot size, a 20-ms pulse duration, and a 1.5-width spot spacing was used. The laser power was titrated from 200 mW until a gray-white opacity was achieved.

Statistical Analysis

The data are presented as the mean ± standard deviation. The CRT, SFChT, reduction in SFChT (ΔSFChT), and rate of reduction in SFChT (%ΔSFChT) were analyzed during follow-up. The statistical analyses were performed using SPSS version 23.0 software (IBM Corp., Armonk, NY, USA) with the independent t-test, paired t-test, and chi-square test as appropriate. A P-value <0.05 was considered statistically significant.

Results

Baseline Characteristics

Sixty-four eyes (38 patients) with severe NPDR (n=27) or PDR (n=37) were included in this study. There were 37 eyes in the conventional laser group and 27 eyes in the pattern laser group. The mean patient age was 55.2 ± 11.7 (range 34–71) years, the mean duration of diabetes was 13.2 ± 5.8 (range 7–22) years, the mean HbA1c value was 8.0% ± 1.8%, the mean BCVA was 0.24 ± 0.25 logMAR, the mean intraocular pressure was 15.2 ± 3.3 mmHg, and the mean spherical equivalent was -0.73 ± 1.8. There was no significant difference in age, sex, refractive error, HbA1c, BCVA, or mean duration of diabetes between the two study groups (Table 1).

PRP was performed using a mean power of 318.5 ± 285.7 (range 210–500) mW in the conventional laser group and a mean power of 355.9 ± 111.5 (range 240–540) mW in the pattern laser group (P = 0.061). The total number of photocoagulation burns was 1512.8 ± 246.8 in conventional laser group and 3216.8 ± 287.3 in the pattern laser group (P < 0.001).

There was no correlation between the mean baseline SFChT and age (P = 0.138), HbA1c (P = 0.237), BCVA (P = 0.747), or spherical equivalent (P = 0.795). The inter-observer reproducibility of the SFChT measurement ranged from 0.986 to 0.990. The baseline CRT was similar in both groups and there was no statistically significant difference in the changes in CRT following PRP between the study groups.

Mean subfoveal choroidal thickness in the conventional and pattern laser groups

The mean SFChT in the conventional laser group was 318.4 ± 58.3 μm at baseline and decreased significantly (P < 0.001 vs baseline) at 1, 3, 6 and 12 months, respectively (Fig 1A).

The mean SFChT in the pattern laser group was 313.3 ± 91.9 μm at baseline. There were no significant changes in the mean SFChT between baseline and 1 month (309.5 ± 93.4 μm, P = 0.404 vs baseline) after PRP. The mean SFChT were significantly decreased to 309.5 ± 93.4 μm at 3 months (P = 0.404 vs baseline), 301.2 ± 89.6 μm at 6 months (P = 0.004 vs baseline), and 285.1 ± 87.6 μm at 12 months (P

< 0.000 vs baseline; Fig 1A).

ΔSFChT was significantly greater in the conventional laser group than in the pattern laser group at 1 month (14.7 ± 17.3 μm vs 3.8 ± 21.9 μm, P = 0.03), 3 months (20.8 ± 18.6 μm vs 9.4 ± 19.1 μm, P = 0.027), and 6 months (25.3 ± 21.2 μm vs 12.1 ± 18.5 μm, P = 0.018) after PRP. There was no statistically significant difference at 12 months (38.3 ± 19.2 μm vs 28.1 ± 22.8 μm, P = 0.075) after PRP (Fig 1B, Table 2).

The %ΔSFChT was also greater in the conventional laser group than in the pattern laser group at 1 month (4.5% ± 5.1% vs 1.1% ± 7.2%, P = 0.52), 3 months (6.3% ± 5.5% vs 2.7% ± 6.4%, P = 0.03), 6 months (7.8% ± 6.7% vs 3.7% ± 6.4%, P = 0.02), and 12 months (11.9% ± 5.9% vs 8.9% ± 7.2%, P = 0.087;Table 2).

Changes in subfoveal choroidal thickness between the severe NPDR and PDR groups

Thirty-seven of the 64 eyes (38 patients) had PDR and 27 had severe NPDR. The mean SFChT in the PDR group was 319.4 ± 73.5 μm at baseline and decreased significantly through the follow-up period after PRP. The mean SFChT in the severe NPDR group was 309.1 ± 74.3 μm at baseline and also decreased significantly at every time point after PRP (Fig. 2A). 

The ΔSFChT values in the PDR and severe NPDR groups were 9.9 ± 22.3 μm and 11.7 ± 15.5 μm, respectively, at 1 month, 16.7 ± 20.9 μm and 13.7 ± 16.8 at 3 months, and 24.6 ± 22.5 and 20.9 ± 16.2 at 6 months. There was no statistically significant difference in the amount of reduction in ΔSFChT between the two groups. However, the ΔSFChT was significantly greater in the PDR group than in the severe NPDR group at 12 months after PRP (38.6 ± 22.9 μm vs 24.8 ± 13.7, P = 0.006; Fig. 2B, Table 2).

The %ΔSFChT values in the PDR and severe NPDR groups were 2.7% ± 6.9% and 3.6% ± 4.8%, respectively, at 1 month, 4.9% ± 6.5% and 4.4% ± 5.2% at 3 months, and 7.6% ± 7.3% and 7.3% ± 5.6% at 6 months. There was no statistically significant difference in the amount of change in %ΔSFChT between the two groups. However, the %ΔSFChT was significantly greater in the PDR group than in the severe NPDR group at 12 months after PRP (12.1% ± 7.3% vs 8.1% ± 4.2%, P = 0.01;  Table 2 ).

Discussion

In this study, we compared the changes in SFChT in eyes with advanced DR after PRP between a conventional laser group and a pattern laser group. There was a significant decrease in SFChT after PRP compared with baseline in both groups of eyes during the follow-up period. The reduction in SFChT was more prominent in the conventional laser group than in the pattern laser group at an early stage following PRP.

Blumenkranz et al. have developed a pattern scanning laser with a shorter pulse duration of 10–20 ms that uses a Nd:YAG laser with a 532-nm wavelength.[3] They reduced the pulse duration of the laser to decrease patient discomfort and to reduce the amount of time taken to perform PRP. The shorter pulse duration requires less pulse energy. The laser scars produced by the shorter pulses are smaller than those produced by longer pulses.[13] Nagpal et al. reported that the average scar size created by the conventional laser was significantly greater than that created by the pattern scanning laser (430 µm vs 310 µm) at 3 months after PRP with the same 200 µm spot size.[14] Photocoagulation scars created using a conventional laser with a pulse duration of 100–200 ms tend to enlarge progressively because of heat diffusion.[13] Therefore, it seems that the difference in the changes in SFChT between the two groups after PRP in this study was related to differences in the expansion of the laser burn scar. Moreover, the laser fluence created by the pattern scanning laser was significantly less than that created by the conventional laser (40.33 J/cm2 vs 191 J/cm2).[14]

Several studies have shown that the SFChT decreases after PRP and that PRP-treated eyes have a smaller SFChT than naïve eyes.[4,8,9,15-17] Zhang et al. found that the SFChT decreased significantly 3 months after PRP,[8] as did Okamoto et al,[9] while Ohara et al found that SFChT decreased significantly 6 months after PRP[17] and Kang et al reported a significant reduction in the SFChT in the 12 months after PRP.[15] Present study also showed that the SFChT was significantly reduced over 12 months after PRP. This study is consistent with the previous study in aspect of long lasting PRP effect.[15] Previously, Maeshima et al. described progressive enlargement of laser scar over the several years.[18] Moreover, they reported that the mean annual expansion rates of laser scar were 7–12.7%. We thought that the long lasting effect on SFChT over 12 months is associated with scar expansion of laser burn.

Despite the consistent finding of a decrease in the SFChT during long-term observation, reports on the more short-term studies have been conflicting but suggest a significant increase in SFChT at 1–12 weeks after PRP.[19-21] It is thought that the inconsistent early changes in SFChT after PRP might be caused by release of inflammatory cytokines in response to laser photocoagulation. Four eyes in our pattern laser group and two eyes in our conventional laser group showed thickening of the SFChT by more than 5%ΔSFChT. It seems that eyes with increased vascular permeability, especially in patients with poor glycemic control, might be more likely to have increased SFChT in the early phase after PRP than eyes in patients with good glycemic control.

We also compared the changes in SFChT after PRP between the PDR and severe NPDR groups. The two groups showed a similar tendency for a decrease in SFChT during the study period. However, the reduction in SFChT was more prominent in the PDR group than in the severe NPDR group at 12 months following PRP. The reduction in SFChT after PRP may be caused by a decrease in the level of vascular endothelial growth factor (VEGF) secreted from the non-perfusion area in response to ablation of an ischemic retina and choriocapillaris. There have been reports of a significant reduction in SFChT in eyes treated with intravitreal injections of anti-VEGF or triamcinolone acetonide as well as PRP.[22-24] These findings also suggest that the choroid tissue is sensitive to the amount of VEGF or cytokines released from the retinal tissue.

Basically, we have tried to analyze the correlation between the change of DR stage and SFChT after PRP. Before PRP treatment, FAG was usually performed to evaluate the DR stage. However, FAG was not regularly performed to analyze the regression of new vessels in eyes with proliferative DR and rarely performed in eyes with severe NPDR after PRP. Thus, prospective study will be needed to analyze the correlation between the regression of diabetic retinopathy stage and the changes of SFChT after PRP.

This study has several limitations. First is its small sample size. The second is its retrospective rather than controlled prospective design. Third, recurrence or persistence of new vessels in eyes with PDR after PRP was not considered. Fourth, diurnal variation was not considered. Fifth, the effect of intravitreal anti-VEGF injection was not considered in eyes with DME. However, despite these limitations, this is the first study to compare the effect of pattern scanning laser with that of conventional laser on SFChT after PRP. Further investigations with a prospective design are needed to confirm the findings of the present study.

Conclusions

SFChT is reduced significantly after PRP. However, the effect of conventional laser on the SFChT is greater than that of pattern scanning laser, especially in the early stages after PRP.

Abbreviations

BCVA: best-corrected visual acuity 

CRT: central retinal thickness 

DR: diabetic retinopathy 

ETDRS: Early Treatment Diabetic Retinopathy Study

Nd-YAG: neodymium-doped yttrium aluminum garnet 

NPDR: non-proliferative diabetic retinopathy 

PDR: proliferative retinopathy  

PRP: pan-retinal photocoagulation 

SFChT: subfoveal choroidal thickness 

ΔSFChT: reduction in SFChT                     

%ΔSFChT: rate of reduction in SFChT

Declarations

Ethics approval and consent to participate: The study protocol has been approved by the institutional review board committee of Chung-Ang University Hospital, Seoul, South Korea on human research (IRB no. 1701-003-16029), and the study was conducted in accordance with the tenets of the Declaration of Helsinki. Signed informed consent was obtained from all patients before each PRP treatment session.

Consent for publication: Not applicable

Availability of data and materials: The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests: The authors have no conflicts of interest to declare.

Funding: This work was supported by the National Research Foundation of Korea (NRF-2015R1C1A1A01054285, NRF-2019R1H1A1035593) by the Ministry of Science, Information & Communication Technology (ICT), and Future Planning. These funding sources had no role in the study design; collection, analysis, or interpretation of the data; or in the writing of the report.

Authors' contributions: Involved in the design of the study (JTK); conduct of the study (JTK); collection, management, analysis of the data (NP, JTK); preparation of the manuscript (NP, JTK); and critical revision of the manuscript (JTK). All authors read and approved the final manuscript.

Acknowledgements: Not Applicable.

References

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2        Early photocoagulation for diabetic retinopathy. ETDRS report number 9. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology 1991;98:766-785.

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Tables

Table 1. Demographic and clinical characteristics of patients included in the study.

 

Total
 (64 eyes)

Conventional laser
group
(37 eyes)

Pattern laser
group
(27 eyes)

P-value

Age (years)

55.2 ± 11.7

55.3 ± 11.3

55.1 ± 12.7

0.936*

Sex M/F (no.)

37/27

22/15

15/12

0.755

HbA1c (%)

8.0 ±1.8

8.3 ±2.2

7.8 ± 1.5

0.33*

Duration of DM (years)

13.2 ± 5.8

13.1 ± 4.8

13.3 ± 6.7

0.56*

BCVA (logMAR)

0.24 ± 0.25

0.27 ± 0.29

0.21 ± 0.2

0.486*

IOP (mmHg)

15.2 ± 3.3

14.2 ± 3.6

16.2 ± 2.6

0.068*

SE (diopter)

-0.73 ± 1.8

-0.63 ± 1.8

-0.75 ± 1.8

0.944*

PDR/Severe NPDR (no.)

37/27

22/15

15/12

0.477

Baseline CRT (μm)

266.2 ± 87.4

284.1 ± 104.7

250.3 ± 67.4

0.166*

BCVA, best-corrected visual acuity; CRT, central retinal thickness; DM, diabetes mellitus; HbA1c, glycated hemoglobin; IOP, intraocular pressure; NPDR, non-proliferative retinopathy; PDR, proliferative retinopathy; SE, spherical equivalent. *Independent t-test; chi-square test



Table 2 Comparison of mean subfoveal choroidal thickness between the two study groups during follow-up after panretinal photocoagulation.

 

 

 

Changes in mean SFChT
according to laser used

 

Changes in mean SFChT
according to severity of DR

 

Total
 (n=64)

 

Pattern laser
group
(n=27)

Conventional laser
group
(n=37)

*P- value

 

Severe NPDR group
(n=27)

PDR group
(n=37)

*P-value

SFChT Baseline

315.8 ± 73.3

 

313.3 ± 91.9

318.4 ± 58.3

0.798

 

309.1 ± 74.3

319.4 ± 73.5

0.617

SFChT 1 M

305.6 ± 71.6

 

309.5 ± 93.4

302.9 ± 52.7

0.742

 

297.4 ± 72.5

310.1 ± 71.8

0.527

SFChT 3 M

299.7 ± 69.6

 

303.9 ± 89.6

298.0 ± 52.3

0.758

 

295.4 ± 72.7

302.1 ± 68.8

0.73

SFChT 6 M

296.1 ± 72.6

 

301.2 ± 89.6

294.6 ± 57.9

0.74

 

290.2 ± 74.4

296.0 ± 72.6

0.993

SFChT 12 M

281.8 ± 69.4

 

285.1 ± 87.6

280.7 ± 53.9

0.819

 

284.2 ± 71.6

280.4 ± 69.1

0.847

Δ SFChT 1 M

10.1 ± 20.1

 

3.8 ± 21.9

14.7 ± 17.3

0.03

 

11.7 ± 15.5

9.3 ± 22.3

0.666

Δ SFChT 3 M

16.1 ± 19.5

 

9.4 ± 19.1

20.8 ± 18.6

0.027

 

13.7 ± 16.9

17.3 ± 20.9

0.519

Δ SFChT 6 M

19.7 ± 21.0

 

12.1 ± 18.5

25.3 ± 21.2

0.018

 

12.9 ± 16.2

23.4 ± 22.5

0.072

Δ SFChT 12 M

34.0 ± 21.2

 

28.1 ± 22.8

38.3 ± 19.2

0.075

 

24.8 ± 13.7

38.9 ± 22.9

0.006

%Δ SFChT 1 M

2.9 ± 6.2

 

1.1 ± 7.2

4.5 ± 5.1

0.52

 

3.7 ± 4.8

2.6 ± 6.9

0.525

%Δ SFChT 3 M

4.8 ± 6.1

 

2.7 ± 6.4

6.3 ± 5.5

0.03

 

4.4 ± 5.3

5.0 ± 6.6

0.701

%Δ SFChT 6 M

6.2 ± 6.8

 

 3.7 ± 6.4

7.8 ± 6.7

0.02

 

4.2 ± 5.6

7.2 ± 7.3

0.121

%Δ SFChT 12 M

10.7 ± 6.6

 

8.9 ± 7.2

11.9 ± 5.9

0.087

 

8.1 ± 4.2

12.2 ± 7.3

0.01

*Independent t-test. NPDR, non-proliferative retinopathy; PDR, proliferative retinopathy; SFChT, subfoveal choroidal thickness; ΔSFChT, reduction of SFChT = SFChT at baseline – SFChT at time point); %ΔSFChT, percentage of reduction in SFChT = 100 × (SFChT at baseline – SFChT at time point)/SFChT at baseline