Citation: Abouelkheir HY, Badawi AE, Abdelkader AM, El-Kanishy A, Saleh S, Abou Samra WA, Kasem MA, Mokbel T. Does the scleral encircling band provide a protective effect against the progression of diabetic retinopathy? Int J Ophthalmol 2019;12(9):1408-1414
DOI:10.18240/ijo.2019.09.06


·
Clinical Research·

Does the scleral encircling band provide a protective effect against the progression of diabetic retinopathy?

Hossam Youssef Abouelkheir, Amani E Badawi, Amr M. Abdelkader, Amr El-Kanishy, Sameh Saleh, Waleed Ali Abou Samra, Manal Ali Kasem, Tharwat Mokbel

Mansoura Ophthalmic Center, Faculty of Medicine, Mansoura University, Mansoura 35516, Egypt

Correspondence to: Amr M. Abdelkade. Department of Ophthalmology, Mansoura Ophthalmic Center, Faculty of Medicine, Mansoura University, Mansoura 35516, Egypt. dramrabdelkader@gmail.com

Received: 2018-11-24        Accepted: 2019-01-14

Abstract

AIM: To evaluate the effect of scleral encircling bands on the development and progression of diabetic retinopathy (DR) in diabetic patients.

METHODS: The medical records of diabetic patients who underwent unilateral retinal detachment (RD) surgery using scleral buckle and encircling band were reviewed retrospectively. Both eyes of patients were included in the study: one eye in each patient had a scleral buckle with encircling band (the operated eye) and the other one is the non-operated eye. The demographic characters, duration of diabetes and period between surgery and the last recall visit were retrieved from each patient. All the cases underwent fundus photo and fluorescein angiography (when indicated) to confirm the DR staging.

RESULTS: Totally 25 patients fulfilled the inclusion and the exclusion criteria were become eligible for the study. A total of 50 eyes of 25 patients were enrolled in this analysis. The mean period of time passed from surgery with encircling band and the last reassessment visit was 12.5±2y. Even though DR could develop in the operated eyes, it was at a less degree of severity compared to the non-operated eyes of same patients (P=0.027).

CONCLUSION: Scleral encircling bands have protective effects against the development and progression of DR.

KEYWORDS: diabetic retinopathy; scleral encircling bands; retinal detachment

DOI:10.18240/ijo.2019.09.06

Citation: Abouelkheir HY, Badawi AE, Abdelkader AM, El-Kanishy A, Saleh S, Abou Samra WA, Kasem MA, Mokbel T. Does the scleral encircling band provide a protective effect against the progression of diabetic retinopathy? Int J Ophthalmol 2019;12(9):1408-1414

INTRODUCTION

Diabetic retinopathy (DR) remains one of the most important causes of blindness among population[1]. Its development and progression are influenced by the duration and type of diabetes besides many other systemic and ocular factors[2].

Aiello[3] reported that eyes with extensive chorio-retinal scars due to inflammatory conditions, trauma, etc showed a decreased prevalence and severity of DR. Depending on this observation, panretinal photocoagulation was used for the treatment of proliferative diabetic retinopathy (PDR). The most widespread explanation is that destruction of the ischemic retina by laser decreases the release of angiogenic factors[4].

Myopia has been reported to have a prophylactic effect against the development of DR[5]. There is an evidence that myopic eyes have reduced blood flow[6] and consequently associated with less damaged micro-circulation in eyes of diabetic patients[7].

From the same point of view, scleral buckling operations and encircling bands were found to decrease the blood flow velocity in the central retinal artery by 35%-50%[8-9], stated that encircling is the factor which is responsible for reducing the ocular blood flow after buckling procedures. 

Although several studies have evaluated the protective and risk factors of DR progression, the impact of the scleral buckling on DR has not been elaborated. To the authors’ knowledge, it is the first report dealing with the association between buckling and the DR progress. The study hypothesis emerged from a striking observation that patients with a history of repaired retinal detachment (RD) with encirculing band, have less DR stages in the operated eye than the fellow eye.

To observe and record the relation between the encircling band and progression of DR and to find out if there a protective effect of an encircling band similar to that seen in myopia, we thought that our aim could be achieved by comparing both eyes of the same diabetic patient: the operated eye with encircling band and the other non-operated eye over a sufficient period of time.


SUBJECTS AND METHODS

Ethical Approval  The aim of the study was explained to the recruited patients and informed consent was obtained from all patients. The study was approved by the Ethics Committee Of Faculty of Medicine, Mansoura University (IRB “R/ 17.10.14), and  followed the tenets of the Declaration of Helsinki.

Study design  A retrospective observational cohort study.

Subjects  The medical records of all patients who underwent surgical repair of unilateral rhegmatogenous retinal detachment (RRD) using scleral buckle and an encircling band technique at the surgical retina unit (Mansoura Ophthalmic Center, Mansoura University, Egypt) were reviewed retrospectively. The review period of extended  for cases operated from January 2001 through December 2008.

In the beginning, we started to collect data of patients who were initially diagnosed with RRD with only one eye and treated by the scleral buckle with the encircling band procedure. All patients should have a known history of diabetes at the time of presentation with no evidence of any changes related to DR by that time.

An exclusion list was put to exclude patients with one or more of the following conditions if found in either eye: glaucoma, myopia with refraction more than -6 D, anisometropia, amblyopia, optic atrophy, history of ocular injury or intraocular surgery and different chorio-retinal atrophic conditions that may affect the retinal blood flow.

Methods

Surgical procedure  Two main surgeons (Abouelkheir HY , El-Kanishy A) and one assistant (Abdelkader AM) performed the surgical procedures of the selected patients according to each RD condition. The scleral buckle (silicone tire 279, Labtician Ophthalmics, Inc., Oakville, Ontario, Canada) was used as a tamponade for all visible retinal break with a silicone circling band (240, Labtician Ophthalmics, Inc., Oakville, Ontario, Canada).

Data collections  A process of recalling the patients with scheduled appointments to come back for a reassessment of their retinal condition was carried out in the period between June 2018 and September 2018. Recalled patients were underwent to a comprehensive ocular and systemic history taking and re-examination with an exclusion of patients developed any ocular disease found in the exclusion list in either eye during the period since the time of the RD repair and the last recall visit in 2018. In addition, we excluded patients who had undergone any kind of treatment related to DR for instance, laser photocoagulation, intra-vitreal steroid, anti-vascular endothelial growth factor (VEGF) or vitrectomy as we cannot comfortably judge on the correlation between the effectiveness of treatment and stage of DR by the time of reassessment. Besides recording the demographic characters, the following data were retrieved from each patient: duration of diabetes, the duration between surgery and the last recall visit. Slit-lamp biomicroscopy examination of both anterior and posterior segments and a detailed fundus examination with the indirect ophthalmoscope and +90 D lens was performed. All the cases clinically diagnosed to have DR underwent fundus photo and fluorescein angiography (when indicated) to confirm the diagnosis and DR staging using Retinal Camera (TopoconTRC-50 DX, Hasunuma-cho, Itabashi-ku, Tokyo, Japan) by an expert medical retina specialist (Badawi AE).

Diabetic retinopathy staging  The documentation of the stage of DR in both eyes was based on International Clinical Diabetic Retinopathy Disease Severity Scale[10]. Table 1 exhibits the definitions and gradings of different DR stages.

Table 1 DR staging (International Clinical Diabetic Retinopathy Disease Severity Scale)[10]

DR stage

Ophthalmoscopic findings

No retinopathy

No apperent abnormalities

Mild NPDR

Only microaneurysms

Moderate NPDR

More than just microaneurysms, but less than severe NPDR.

Severe NPDR

Any of the following without any PDR signs: 1) more than 20 intraretinal haemorrhages in each of 4 quadrants; 2) venous beading in 2 or more quadrants; 3) prominent irma in 1 or more quadrant.

PDR

One or more of the following: 1) neovascularization; 2) vitreous/preretinal haemorrhage.

NPDR: Non-proliferative diabetic retinopathy; PDR: Proliferative diabetic retinopathy; IRMA: Intraretinal microvascular abnormalities.

Statistical Analysis  Both eyes of each patient were enrolled (to exclude any bias from the systemic factors) with a total number of 50 eyes. The eyes with an encircling band (the operated eyes) were one group, and the other eyes (non-operated eyes) were the second group. The collected data were analyzed by IBM SPSS (statistical package for social science) software package version 20.0. Chi-square test was used for categorical analysis between the two groups. The Fisher exact test was selected if the expected count in any cell was five or less. Mann-Whitney and Wilcoxon tests were used to measure the mean rank of DR severity in the two groups. In this study, the study sampling were calculated using a computer program (G power 3.1.9.2) considering proportion p1=0.5, proportion p2=0.6 and β/α=0.80 (one-tailed), the actual power was 0.63 with a total sample size=50 ( 25 in each group). For all tests, a P value of less than 0.05 was considered significant.


RESULTS

The 25 patients (13 males and 12 females) fulfilled the inclusion and the exclusion criteria have become eligible for the study. A total of 50 eyes of 25 patients with diabetes were enrolled in this analysis. At the time of recall assessment, the mean age was 61.8±5.2y. The mean duration of diabetes was 14.9±2.6y and the mean period of time passed from surgery with an encircling band and the last reassessment visit was 12.5±2y. Table 2 demonstrates the demographic and descriptive findings of the study participants.

Table 2 Demographic data, duration of diabetes, period between surgery and reassessment, and stage of DR in the study eyes

Stage of DR in the operated eyes

Stage of DR in the non-operated eyes

Period between surgery and reassessment visit (y)

Duration of

diabetes (y)

Sex

Age at the reassessment visit (y)

Patient’s

 ID

None

Mild NPDR

12

14

Male

66

1

None

None

11

12

Male

61

2

None

Mild NPDR

14

15

Female

56

3

None

None

10

11

Male

49

4

Mild NPDR

Severe NPDR

15

17

Female

65

5

None

Moderate NPDR

14

16

Female

63

6

None

None

11

12

Female

60

7

Mild NPDR

Severe NPDR

13

18

Male

59

8

None

None

10

13

Male

57

9

Severe NPDR

PDR

14

19

Female

67

10

None

None

10

12

Male

56

11

None

None

12

14

Male

68

12

Severe NPDR

PDR

16

21

Female

72

13

PDR

PDR

15

20

Male

69

14

None

None

11

13

Male

64

15

None

Mild NPDR

11

14

Female

63

16

None

Moderate NPDR

14

16

Female

67

17

None

None

10

12

Male

60

18

None

None

10

11

Male

54

19

Moderate NPDR

Moderate NPDR

15

17

Female

62

20

Mild NPDR

PDR

16

19

Female

65

21

None

Mild NPDR

12

14

Female

59

22

None

Mild NPDR

11

15

Male

61

23

None

None

12

13

Female

58

24

None

Mild NPDR

13

15

Male

64

25

NPDR: Non-proliferate diabetic retinopathy; PDR: Proliferative diabetic retinopathy.

There was a statistically significant difference supporting the decreased incidence of development of DR in the operated eyes with encircling band compared with the non-operated eyes (P=0.027, Table 3). Analysis of the 50 eyes showed that DR with different stages was found in 22 (44%) of eyes while 28 eyes (56%) showed no evidence of any diabetic changes.

Table 3 The severity of DR at the time of reassessment among the 2 groups

Group

Mean rank

P

Operated eyes

21.38

0.027

Non-operated eyes

29.62

Mann-Whitney and Wilcoxon tests.

Among those 22 eyes that showed DR changes, only 7 (31.8%) eyes had surgery with an encircling band and 15 (68.2%) eyes were non-operated. Figure 1 demonstrates the distribution of DR stages in the operated and non-operated eyes.

Hossam Youssef Abouelkheir1

Figure 1 DR stages in both operated and non-operated eyes.

Despite there was a significant decrease in the whole DR  incidence in the operated eyes, there was a significant difference between the operated eyes and the fellow eyes in “no retinopathy and PDR” stages mainly. In the operated eyes with encircling bands: 18 (72%) eyes showed no evidence of DR versus 10 (40%) in the non-operated eyes (P=0.019) while the PDR stage was recorded in 1 (4%) eye in the operated eyes versus 4 (16%) eyes in the non-operated group (P=0.022, Table 4).

Table 4 DR stage distributions among the two groups and its significance    n (%)

Stage

Non-operated eyes

Operated eyes

P

Non

10 (40)

18 (72)

0.019a

Mild NPDR

6 (24)

3 (12)

0.693

Moderate NPDR

3 (12)

1 (4)

0.712

Severe NPDR

2 (8)

2 (8)

1.000

PDR

4 (16)

1 (4)

0.022a

NPDR: Non-proliferate diabetic retinopathy; PDR: Proliferative diabetic retinopathy. Chi-square test (Fisher test), aP˂0.05.

Figures 2 and 3 illustrate that even though DR could develop in the operated eyes, it was definitely at a less degree of severity compared to the non-operated eyes of the same patients.

Hossam Youssef Abouelkheir2

Figure 2 A female patient aged 67y (case No.10) had a scleral encircling band in her right eye since 14y  Right eye color fundus photo (A) and late phase fluorescein angiography image (B) show severe NPDR, while the left eye color fundus photo (C) and late phase fluorescein angiography image (D) show PDR.

Hossam Youssef Abouelkheir3

Figure 3 A female patient aged 65y (case No.21) had a scleral encircling band in her left eye since 16y  Left eye color fundus photo (A) and late phase fluorescein angiography image (B) show mild NPDR, while the right eye color fundus photo (C) and late phase fluorescein angiography image (D) show PDR.

DISCUSSION

In spite, the bothersome drawbacks of the scleral buckling procedure, it is still commonly used as a primary approach for RRD repair[11]. Indentation of the globe with axial length alteration and a refractive shift is one of the frequent side effects of the scleral buckling[12-13].

To study the influence of encircling band on DR, we retrospectively compared both operated and non-operated eyes of the same diabetic patient to adjust all the general and systemic risk independent factors that may affect the development and progression of DR. The current results demonstrated obviously that the scleral buckling procedure affected the DR progression after the surgery. There was a significantly decreased incidence of development of DR in the operated eyes with encircling bands compared to the non-operated eyes. Furthermore, our findings showed that even though DR could develop in eyes with encircling bands, it remained at a less stage of severity compared to the non-operated eyes of the same patients (asymmetric DR), as well as the DR severity was correlated with the date of operation.

Predominantly, DR progresses in a symmetrical manner in both eyes over long periods of time, making it extremely exceptional to occur asymmetrically[5]. Several definitions of asymmetric DR have been described: unilateral non-proliferate diabetic retinopathy (NPDR) or unilateral PDR with no retinopathy in the fellow eye, NPDR in one eye and PDR in the fellow eye, and advanced diabetic retinal changes in one eye and low-risk PDR in the other eye[14].

The protective effect of myopia and elongated axial length against the development of PDR has been shown in many studies[5,7,15]. This could explicate the association between myopia and asymmetrical DR. The authors supposed that, the scleral buckling with longer axial length, as a result, confers the similar protection as in myopia. This effect may be attributed to the low ocular blood flow in myopic eyes[6,16]. Refractive and axial myopic eyes seem to have narrow retinal vessels, increased branching in both venules and arterioles, and less tortuosity in the arterioles[5].

Additionally, myopic eyes suffer more frequently from total posterior vitreous detachment (PVD) (50% vs 12.2% in emmetropic eyes)[17] which reduces the risk of PDR and progression of neovascularization, while the incomplete PVD is reported to be associated with more severe DR. The vitreoretinal traction acts as vitreous scaffold that causes the proliferation of new vessels, thickening, and progression of the fibrous bands[18].

However, a large study did not disclose the association between myopia and with the incidence of DR, but it considered myopia as a protective factor against the progression to PDR in younger-onset diabetes patients only[19]. The pathological microvascular alterations in early stages of DR are mainly perivascular and intravascular such as microaneurysm formulation and thickening in the capillary basement membrane, while in advanced stages, the pathology is foremost extravascular like proliferation and exudation[20]. In myopic eyes, reduced blood flow could decrease the extravasation of blood elements that act as a promoter for macrophages to potentiate the proliferation consequences. This explains the protective role of myopia in delaying the vision-threating stages rather than its impact on the disease incidence[5,21]. The authors assumed the same theory that the myopic shift and AL alterations occurring after the scleral buckling provides such protection against DR progression.

Reduced ocular blood flow with scleral buckle was observed in many studies[22-24]. Regillo et al[8] used color Doppler imaging to study blood flow changes after scleral buckling with encircling bands and their results showed a decrease of average blood flow velocity in the central retinal artery by 35% on the first operative day and by 50% one week postoperatively. In two different studies[9,25], the central retinal artery peak systolic and end diastolic velocities were (6.64 and 2.01 cm/s respectively) in high myopic eyes[25] and in eyes after scleral buckling procedures were (5.96 and 2.32 cm/s respectively)[9]. Comparing the values reveals that applying an encircling band to the eye will affect retinal blood flow nearly to the extent as in high myopic eyes. This also may explain our notice, that eyes of diabetic patients with previous scleral buckling procedure almost show less incidence of development and progression of DR. The protective effect of encircling band on DR could be understood if we study the ocular blood flow in diabetic patients. Several conflicting reports have been published,  some studies reported an initial decrease of retinal blood flow in DR[26-27] and others declared a subsequent increase of blood flow prior to the vaso-proliferative stage[28-29], as a probable response to hypoxia and hyperglycemia[30]. Regrettably, it was not viable to measure the ocular blood flow and its impacts in the operated eyes including in the study.

Retinal hypoxia has been known as the main contributor of the induction of VEGF and PDR development[31]. Reduction in oxygen demand and consumption in eyes with longer axial length was established that might mitigate the consequence of hypoxia in diabetic patients[32]. Several studies have speculated a lower concentration of VEGF  in the aqueous of elongated eyes[33-35], thus clarifies the inverse relationship between PDR prevalence and longer axial length. Our current findings supported their findings, where there was a significant decrease the PDR incidence in the operated eyes. Further, scleral buckling reduces the probability of PVD occurrence as well as a progression of previous one via vitreous base support and shorting the distance between the vitreous base and the retina. Likewise, the buckling decreases vitreous traction and epiretinal membranes[36] and thus promotes an extra protection against the proliferation. In addition, panretinal photocoagulation was found to decrease ocular blood flow[37-38]. These studies reveal the major role of ocular blood flow in DR. Encircling, through reduction of the retinal blood flow, appears to interfere with the main hemodynamic change associated with development and progression of DR.

This study showed decreased DR severity in eyes with formerly successful scleral buckling with encircling bands. Scleral buckling at the equator during diabetic vitrectomy may improve the results and help regression of the proliferative retinopathy. However, the limitation of this study includes absence of another control group of patients who did not undergo surgery at all due to the retrograde nature of the study and insuffcient use of carotid doppler to role out ocular ischemia syndrome. Studies with larger sample size including independent control groups are needed for summation of more outcomes including computation of ocular blood flow and considering the interindividual variance.

In conclusion, encircling bands have protective effects against the development and progression of DR. Depending on this observation we think that applying an encircling element at the equator during diabetic vitrectomy may improve the results and help regression of the proliferative retinopathy. However, in order to confirm this practical application, a separate study should be done with large numbers of eyes and long term follow up to get more information about this procedure.  


ACKNOWLEDGEMENTS

Conflicts of Inerest: Abouelkheir HY, None; Badawi AE, None; Abdelkader AM, None; El-Kanishy A, None; Saleh S, None; Abou Samra WA, None; Kasem MA, None; Mokbel T, None.


REFERENCES

1 Flaxman SR, Bourne RRA, Resnikoff S, Ackland P, Braithwaite T, Cicinelli MV, Das A, Jonas JB, Keeffe J, Kempen JH, Leasher J, Limburg H, Naidoo K, Pesudovs K, Silvester A, Stevens GA, Tahhan N, Wong TY, Taylor HR, Vision Loss Expert Group of the Global Burden of Disease Study. Global causes of blindness and distance vision impairment 1990-2020: a systematic review and meta-analysis. Lancet Glob Health 2017;5(12):e1221-e1234.

 

2 Lee R, Wong TY, Sabanayagam C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis (Lond) 2015;2:17.
https://doi.org/10.1186/s40662-015-0026-2
PMid:26605370 PMCid:PMC4657234

 

3 Aiello LM. Perspectives on diabetic retinopathy. Am J Ophthalmol 2003;136(1):122-135.
https://doi.org/10.1016/S0002-9394(03)00219-8

 

4 Wang W, Lo A. Diabetic retinopathy: pathophysiology and treatments. Int J Mol Sci 2018;19(6):1816.
https://doi.org/10.3390/ijms19061816
PMid:29925789 PMCid:PMC6032159

 

5 Kim DY, Song JH, Kim YJ, Lee JY, Kim JG, Yoon YH, Joe SG. Asymmetric diabetic retinopathy progression in patients with axial anisometropia. Retina 2018;38(9):1809-1815.
https://doi.org/10.1097/IAE.0000000000002109
PMid:29547453

 

6 Samra WA, Pournaras C, Riva C, Emarah M. Choroidal hemodynamic in myopic patients with and without primary open-angle glaucoma. Acta Ophthalmol 2013;91(4):371-375.
https://doi.org/10.1111/j.1755-3768.2012.02386.x
PMid:22458651

 

7 Fu Y, Geng DF, Liu H, Che HX. Myopia and/or longer axial length are protective against diabetic retinopathy: a meta-analysis. Acta Ophthalmol 2016;94(4):346-352.
https://doi.org/10.1111/aos.12908
PMid:26547796

 

8 Regillo CD, Sergott RC, Brown GC. Successful scleral buckling procedures decrease central retinal artery blood flow velocity. Ophthalmology 1993;100(7):1044-1049.
https://doi.org/10.1016/S0161-6420(93)31541-1

 

9 Hanioglu-Kargi S, Yazar Z, Ziraman I, Gursel E. Effects of scleral buckling on the retrobulbar haemodynamic changes. Eye (Lond) 2000;14(Pt 2):165-171.
https://doi.org/10.1038/eye.2000.47
PMid:10845010

 

10 Wilkinson CP, Ferris FL 3rd, Klein RE, Lee PP, Agardh CD, Davis M, Dills D, Kampik A, Pararajasegaram R, Verdaguer JT, Global Diabetic Retinopathy Project Group. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 2003;110(9):1677-1682.
https://doi.org/10.1016/S0161-6420(03)00475-5

 

11 Sallam AB, Donachie PHJ, Yorston D, Steel DHW, Williamson TH, Jackson TL, Sparrow JM, Johnston RL. Royal college of ophthalmologists' national database study of vitreoretinal surgery: report 7, intersurgeon variations in primary rhegmatogenous retinal detachment failure. Retina 2018;38(2):334-342.
https://doi.org/10.1097/IAE.0000000000001538
PMid:28221255

 

12 Lee DH, Han JW, Kim SS, Byeon SH, Koh HJ, Lee SC, Kim M. Long-term effect of scleral encircling on axial elongation. Am J Ophthalmol 2018;189:139-145.
https://doi.org/10.1016/j.ajo.2018.03.001
PMid:29526704

 

13 Ophir SS, Friehmann A, Rubowitz A. Circumferential silicone sponge scleral buckling induced axial length changes: case series and comparison to literature. Int J Retina Vitreous 2017;3:10.
https://doi.org/10.1186/s40942-017-0063-1
PMid:28357135 PMCid:PMC5367001

 

14 Early Treatment Diabetic Retinopathy Study design and baseline patient characteristics. ETDRS report number 7. Ophthalmology 1991;98:741-756.
https://doi.org/10.1016/S0161-6420(13)38009-9

 

15 Man RE, Sasongko MB, Sanmugasundram S, Nicolaou T, Jing X, Wang JJ, Wong TY, Lamoureux EL. Longer axial length is protective of diabetic retinopathy and macular edema. Ophthalmology 2012;119(9):1754-1759.
https://doi.org/10.1016/j.ophtha.2012.03.021
PMid:22627119

 

16 Abou Samra W, Samera WA, Shahin M, El-Awady H, El-Rahman AA, El-Toukhy N. Assessment of ocular hemodynamics after laser in situ keratomileusis using color Doppler imaging. Int Ophthalmol 2014;34(2):269-275.
https://doi.org/10.1007/s10792-013-9804-9
PMid:23743872

 

17 Wang X, Tang LS, Gao L, Yang YJ, Cao D, Li YP. Myopia and diabetic retinopathy: a systematic review and meta-analysis. Diabetes Res Clin Pract 2016;111:1-9.
https://doi.org/10.1016/j.diabres.2015.10.020
PMid:26531140

 

18 Sebag J, Nguyen-Cuu J. The effects of vitreous on proliferative diabetic retinopathy and the response to pan retinal photocoagulation. Graefes Arch Clin Exp Ophthalmol 2017;255(2):421-422.
https://doi.org/10.1007/s00417-016-3527-3
PMid:27771777

 

19 Moss SE, Klein R, Klein BE. Ocular factors in the incidence and progression of diabetic retinopathy. Ophthalmology 1994;101(1):77-83.
https://doi.org/10.1016/S0161-6420(94)31353-4

 

20 Shin ES, Sorenson CM, Sheibani N. Diabetes and retinal vascular dysfunction. J Ophthalmic Vis Res 2014;9(3):362-373.

 

21 Rangasamy S, McGuire PG, Franco Nitta C, Monickaraj F, Oruganti SR, Das A. Chemokine mediated monocyte trafficking into the retina: role of inflammation in alteration of the blood-retinal barrier in diabetic retinopathy. PLoS One 2014;9(10):e108508.
https://doi.org/10.1371/journal.pone.0108508
PMid:25329075 PMCid:PMC4203688

 

22 Yoshida A, Hirokawa H, Ishiko S, Ogasawara H. Ocular circulatory changes following scleral buckling procedures. Br J Ophthalmol 1992;76(9):529-531.
https://doi.org/10.1136/bjo.76.9.529
PMid:1420055 PMCid:PMC504341

 

23 Nagahara M, Tamaki Y, Araie M, Eguchi S. Effects of scleral buckling and encircling procedures on human optic nerve head and retinochoroidal circulation. Br J Ophthalmol 2000;84(1):31-36.
https://doi.org/10.1136/bjo.84.1.31
PMid:10611096 PMCid:PMC1723226

 

24 Kubicka-Trzaska A, Górniak-Bednarz A. Macular microcirculation blood flow changes after conventional surgery for rhegmatogenous retinal detachment. Klin Oczna 2007;109(4-6):179-182.

 

25 Akyol N, Kükner AS, Ozdemir T, Esmerligil S. Choroidal and retinal blood flow changes in degenerative myopia. Can J Ophthalmol 1996;31(3):113-119.

 

26 Srinivas S, Tan O, Nittala MG, Wu JL, Fawzi AA, Huang D, Sadda SR. Assessment of retinal blood flow in diabetic retinopathy using Doppler Fourier-domain optical coherence tomography. Retina 2017;37(11):2001-2007.
https://doi.org/10.1097/IAE.0000000000001479
PMid:28098726 PMCid:PMC6581777

 

27 Nagaoka T, Sato E, Takahashi A, Yokota H, Sogawa K, Yoshida A. Impaired retinal circulation in patients with type 2 diabetes mellitus: retinal laser Doppler velocimetry study. Invest Ophthalmol Vis Sci 2010;51(12):6729-6734.
https://doi.org/10.1167/iovs.10-5364
PMid:20631236

 

28 Burgansky-Eliash Z, Barak A, Barash H, Nelson DA, Pupko O, Lowenstein A, Grinvald A, Rubinstein A. Increased retinal blood flow velocity in patients with early diabetes mellitus. Retina 2012;32(1):112-119.
https://doi.org/10.1097/IAE.0b013e31821ba2c4
PMid:21878846

 

29 Dimitrova G, Kato S, Yamashita H, Tamaki Y, Nagahara M, Fukushima H, Kitano S. Relation between retrobulbar circulation and progression of diabetic retinopathy. Br J Ophthalmol 2003;87(5):622-625.
https://doi.org/10.1136/bjo.87.5.622
PMid:12714407 PMCid:PMC1771632

 

30 Man RE, Sasongko MB, Xie J, Best WJ, Noonan JE, Lo TC, Wang JJ, Luu CD, Lamoureux EL. Decreased retinal capillary flow is not a mediator of the protective myopia-diabetic retinopathy relationship. Invest Ophthalmol Vis Sci 2014;55(10):6901-6907.
https://doi.org/10.1167/iovs.14-15137
PMid:25270188

 

31 Campochiaro PA, Aiello LP, Rosenfeld PJ. Anti-vascular endothelial growth factor agents in the treatment of retinal disease: from bench to bedside. Ophthalmology 2016;123(10S):S78-S88.
https://doi.org/10.1016/j.ophtha.2016.04.056
PMid:27664289

 

32 Bazzazi N, Akbarzadeh S, Yavarikia M, Poorolajal J, Fouladi DF. High myopia and diabetic retinopathy: a contralateral eye study in diabetic patients with high myopic anisometropia. Retina 2017;37(7): 1270-1276.
https://doi.org/10.1097/IAE.0000000000001335
PMid:27749693

 

33 Hu QJ, Liu GH, Deng Q, Wu QJ, Tao Y, Jonas JB. Intravitreal vascular endothelial growth factor concentration and axial length. Retina 2015;35(3):435-439.
https://doi.org/10.1097/IAE.0000000000000329
PMid:25158940

 

34 Sawada O, Miyake T, Kakinoki M, Sawada T, Kawamura H, Ohji M. Negative correlation between aqueous vascular endothelial growth factor levels and axial length. Jpn J Ophthalmol 2011;55(4):401-404.
https://doi.org/10.1007/s10384-011-0027-1
PMid:21607685

 

35 Sawada O, Kawamura H, Kakinoki M, Sawada T, Ohji M. Vascular endothelial growth factor in the aqueous humour in eyes with myopic choroidal neovascularization. Acta Ophthalmol 2011;89(5):459-462.
https://doi.org/10.1111/j.1755-3768.2009.01717.x
PMid:20102348

 

36 Mehdizadeh M, Afarid M, Haghighi MS. Retinal redetachment after cataract surgery in eyes with previous scleral buckling. J Ophthalmic Vis Res 2011;6(1):73-75.

 

37 Okamoto M, Matsuura T, Ogata N. Effects of panretinal photocoagulation on choroidal thickness and choroidal blood flow in patients with severe nonproliferative diabetic retinopathy. Retina 2016;36(4):805-811.
https://doi.org/10.1097/IAE.0000000000000800
PMid:26447396

 

38 Iwase T, Kobayashi M, Yamamoto K, Ra E, Terasaki H. Effects of photocoagulation on ocular blood flow in patients with severe non-proliferative diabetic retinopathy. PLoS One 2017;12(3):e0174427.
https://doi.org/10.1371/journal.pone.0174427
PMid:28355247 PMCid:PMC5371365