Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2014  |  Volume : 27  |  Issue : 4  |  Page : 643-649

Evaluation of the progression of diabetic retinopathy after phacoemulsification


Department of Ophthalmology, Faculty of Medicine, Menofia University, Shebin El-Kom, Egypt

Date of Submission13-Feb-2014
Date of Acceptance03-Jun-2014
Date of Web Publication22-Jan-2015

Correspondence Address:
Noha K Gaber
Department of Ophthalmology, Faculty of Medicine, Menofia University, Shebin El-Kom, Menofia
Egypt
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.149631

Rights and Permissions
  Abstract 

Objectives
The aim of the study was to evaluate the progression of diabetic retinopathy (DR) after phacoemulsification in cataractous diabetic patients and determine whether complicated cases of phacoemulsification with opening of the posterior capsule during surgery affect the progression of DR.
Background
Diabetes is the most common risk factor for development of cataract. The visual outcome of cataract surgery in diabetic patients depends on the severity of retinopathy. Cataract may prevent the recognition or treatment of sight-threatening retinopathy before surgery, and, after surgery, vision may be impaired by severe fibrinous uveitis, capsular opacification, anterior segment neovascularization, macular oedema and deterioration of retinopathy, probably due to interruption of the blood-retinal barrier.
Materials and methods
This study includes 40 cataractous diabetic patients, who underwent detailed history taking, full ophthalmic examination, fundus fluorescein angiography and optical coherence tomography before and after phacoemulsification. The patients were divided into two groups. Group A: this group included 20 patients selected from among uncomplicated phacoemulsification surgeries with polymethyl methacrylate or acrylic posterior chamber intraocular lens implantation. Group B: this group included 20 patients selected from among phacoemulsification surgeries with accidental opening of the posterior capsule during surgery and subsequent removal of the anterior vitreous face with or without intraocular lens implantation in the same session.
Results
DR showed a progression rate of 10% in group A compared with 20% in group B. The difference between groups as regards DR progression was highly significant. The statistically significantly higher progression rate in DR observed in complicated cases (group B) may be explained by interruption of the blood-retinal barrier.
Conclusion
Uncomplicated phacoemulsification does not cause acceleration of DR postoperatively. Any progression that is observed postoperatively represents the natural history of the disease. Posterior capsular tear during cataract surgery in diabetic patients leads to statistically significant higher rates of macular oedema, progression of DR and increase in foveal thickness. These events may be related to interruption of the blood-retinal barrier after a posterior capsular tear and the subsequent increased incidence of postoperative inflammation in diabetic patients with diffusion of inflammatory mediators from the anterior segment to the posterior segment. These inflammatory mediators increase the vascular permeability of the retinal capillaries with subsequent macular oedema and increase in foveal thickness.

Keywords: Central macular thickness, diabetic retinopathy, fluorescein angiography, macular oedema, phacoemulsification


How to cite this article:
El-Sobky HM, El-Sebaey AR, El-Hagaa AA, Gaber NK. Evaluation of the progression of diabetic retinopathy after phacoemulsification. Menoufia Med J 2014;27:643-9

How to cite this URL:
El-Sobky HM, El-Sebaey AR, El-Hagaa AA, Gaber NK. Evaluation of the progression of diabetic retinopathy after phacoemulsification. Menoufia Med J [serial online] 2014 [cited 2020 Feb 17];27:643-9. Available from: http://www.mmj.eg.net/text.asp?2014/27/4/643/149631


  Introduction Top


Diabetic retinopathy (DR) is predominantly a microangiopathy in which small blood vessels are particularly vulnerable to damage from hyperglycaemia. However, larger vessels may also be involved. Retinopathy has features of both microvascular occlusion and leakage [1].

Diabetes is the most common risk factor for cataract, with a three- to four-fold excess prevalence in diabetic patients older than 65 years [2].

Cataract is a major problem for diabetic patients because it decreases vision, prevents adequate fundus examination and interferes with the strategy of laser photocoagulation for DR. Diabetic patients have been reported to have a higher prevalence of cataract and develop it at an earlier age compared with nondiabetic individuals [3]. The visual outcome of cataract surgery in diabetic patients depends on the severity of retinopathy. Cataract may prevent the recognition or treatment of sight-threatening retinopathy before surgery, and after surgery vision may be impaired by severe fibrinous uveitis, capsular opacification, anterior segment neovascularization, macular oedema and deterioration of retinopathy [4].

Uncomplicated phacoemulsification does not cause acceleration of DR postoperatively and any progression that is observed probably represents the natural history of the disease. Although macular oedema is common after cataract surgery, it may follow a benign course and in many patients the development of clinically significant macular oedema postoperatively probably represents natural progression rather than being a direct effect of surgery [5]. For patients who have active nonproliferative diabetic retinopathy (NPDR), as many as 50-75% of those without preoperative macular oedema will develop it and 30% will develop proliferative diabetic retinopathy (PDR). About 8% will develop neovascularization of the iris. If macular oedema is present before the surgery, it nearly always worsens [6]. If cataract is so dense as to preclude recognition or treatment of sight-threatening retinopathy before surgery, the outcome of surgery may be poor. By contrast, if surgery is undertaken before the cataract reaches the point where diagnosis and treatment of retinopathy are significantly impeded, it may be possible to maintain uninterrupted control of retinopathy, and the outcome of surgery may improve. It is believed that cataract surgery should be performed early in diabetes [7].


  Materials and methods Top


All patients included in this study received a thorough explanation of the study design and aims. Forty cataractous diabetic patients underwent cataract extraction at the ophthalmology department of Menoufia university hospital between April 2012 and June 2013. Seventeen men and 23 women were included, with ages ranging from 54 to 74 years, with a mean of 45.49 ± 12.24 SD.

Preoperative examination

This included history taking (age, sex, duration of diabetes, type of diabetes, visual complaints, presence or absence of hypertension, blood glucose and lipid levels, and previous treatment with laser photocoagulation), full ophthalmic examination including visual acuity measurement using Snellen's chart and detailed slit lamp ocular examination especially the lens status (type and degree of cataract) as well as dilated fundus examination. Fluorescein fundus angiography and optical coherence tomography (OCT) were performed. Patients with PDR, mature senile cataract and previous ocular surgery were excluded from this study.

Surgical procedure

Phacoemulsification was performed using standard techniques (Divide and conquer) under local anaesthesia. The patients are divided into two groups. Group A included 20 patients selected from among uncomplicated phacoemulsification surgeries with 5 mm polymethyl methacrylate (PMMA) (in one case) or acrylic posterior chamber intraocular lens (PC-IOL) implantation (in 19 cases). Group B included 20 patients selected from among phacoemulsification surgeries with accidental opening of the posterior capsule during surgery and subsequent removal of the anterior vitreous face with or without intraocular lens (IOL) implantation. Complicated cases by accidental rupture of the posterior capsule were managed by anterior vitrectomy and 6.5 PMMA PC-IOL implantation in the same session in 14 cases and secondary IOL implantation in six cases. In five cases the IOLs were implanted in the sulcus and in one case the IOL was scleral fixated.

Coloured photography and fluorescein angiography

Coloured photography and fluorescein angiography were performed preoperatively and 3 and 6 months postoperatively. The following features were recorded on each angiography:

  1. The type of macular oedema as defined by the Early Treatment Diabetic Retinopathy Study (ETDRS) on the basis of dye leakage in the macula as detected in late phases of the fluorescein angiogram.
  2. The degree of macular capillary nonperfusion.
  3. The stage of retinopathy and details of retinal changes.


Optical coherence tomography

OCT scanning was performed using the optical coherence tomography scanner OCT 2000 (Humphery-Zeiss instruments) and the HeidelBerg spectral domain OCT. OCT was performed preoperatively and 3 and 6 months postoperatively.

Postoperative follow-up

All patients included in the study were required to have at least 6 months of follow-up with documented fundus examination. Retinopathy progression was defined as (a) the development of any retinopathy where none previously existed, (b) the development of or progression of macular oedema to clinical significance as defined by the ETDRS [8] and (c) the development of proliferative retinopathy from NPDR. Postoperative focal/grid laser therapy was carried out for clinically significant macular oedema as defined by the ETDRS, and panretinal photocoagulation was carried out for retinopathy with high-risk characteristics as defined by the Diabetic Retinopathy Study [8]. All visual acuities were converted to decimal form for statistical analysis (i.e. 6/60 = 0.1).

Preoperative data

The study included 40 patients. In group A, 12 patients were female and eight were male; in group B, 11 patients were female and nine patients were male. The ages of the patients in group A ranged from 54 to 72 years, with a mean of 63.4 ± 5.2 years, and in group B it ranged from 54 to 74 years, with a mean of 64 ± 6 years. The ages varied from 54 to 74 years, with a mean of 45.49 ± 12.24 SD. In group A, six patients were insulin dependent and 14 patients were noninsulin dependent, whereas in group B five patients were insulin dependent and 15 patients were noninsulin dependent. There was no statistically significant difference between the two groups with respect to the type of diabetes (P = 0.2) The duration of diabetes ranged from 10 to 20 years, with a mean of 14.4 ± 2.78 years in group A, whereas in group B it ranged from 10 to 20 years, with a mean of 15 ± 3.06 years, with a statistically insignificant difference (P = 0.29) [Table 1]. Lipid level (triglycerides) and blood pressure of all patients included in this study were within normal values. The preoperative best-corrected visual acuity (BCVA) in all patients in both groups ranged from 0.03 to 0.25, whereas the mean preoperative visual acuity was 0.12 ± 0.06 [Table 2].
Table 1: Comparison between the two studied groups with respect to duration of diabetes

Click here to view
Table 2: Statistical analysis of preoperative BCVA in all cases

Click here to view


Visual acuity was documented in the two groups as follows.

Group A

The preoperative BCVA in group A ranged from 0.03 to 0.25, whereas the mean preoperative visual acuity was 0.1 ± 0.06.

Group B

The preoperative BCVA of the eyes included in group B ranged from 0.05 to 0.25, whereas the mean preoperative visual acuity was 0.1 ± 0.07.

The difference between the two groups as regards preoperative visual acuity was statistically not significant.

Preoperatively, all eyes included in this study had NPDR. Grading of DR in group A was as follows: six cases (30%) had mild, 12 cases (60%) had moderate, and two cases (10%) had severe NPDR. In group B, preoperative grading of DR was as follows: nine cases (45%) had mild, eight cases (40%) had moderate, and three cases (15%) had severe NPDR. Statistically, the difference between groups as regards the stage of DR was not significant (P = 0.213).

Macular oedema

Preoperatively, of the total number of patients, 23 (57.5%) had no macular oedema, whereas 17 (42.5%) had focal macular oedema. Statistically, the difference between groups as regards macular oedema was not significant (P = 0.213).

Optical coherence tomography

OCT was performed to evaluate foveal contour and central macular thickness (CMT). The foveal contour was evident by OCT in all eyes enrolled in this study. CMT ranged from 148 to 370 mm, with a mean of 235.7 ± 59.16 mm.

Group A

The preoperative CMT in group A ranged from 150 to 354 mm, with a mean of 245 ± 57.89 mm.

Group B

The preoperative CMT ranged from 148 to 370 mm, with a mean of 226.4 ± 60.43 mm. The mean CMT of patients of group B was preoperatively better than that of group A, but this difference was statistically nonsignificant (P = 0.124).

Intraoperative data

Phacoemulsification was performed using standard techniques (divide and conquer) under local anaesthesia. The patients were divided into two groups. Group A included 20 patients selected from among uncomplicated phacoemulsification surgeries with 5 mm PMMA (in one case) or with acrylic PC-IOL implantation (in 19 cases). Group B included 20 patients selected from among phacoemulsification surgeries with accidental opening of the posterior capsule during surgery and subsequent removal of the anterior vitreous face with or without IOL implantation. Complicated cases by accidental rupture of the posterior capsule were managed by anterior vitrectomy and 6.5 PMMA PC-IOL implantation in the same session in 14 cases and secondary IOL implantation in six cases. In five cases the IOLs were implanted in the sulcus and in one case the IOL was scleral fixated.

Statistical analysis of the data

Visual acuities were converted into decimal form for statistical analysis. Qualitative data such as macular oedema and DR grade were converted to quantitative data for statistical analysis. The macular oedema was assigned one of the following grades: 0 = no macular oedema; 1 = focal macular oedema; 2 = diffuse macular oedema; and 3 = cystoid macular oedema; and 4 = clinically significant macular oedema. The grade of DR was assigned one of the following: 1 = mild NPDR; 2 = moderate NPDR; 3 = severe NPDR; and 4 = very severe NPDR.

Postoperative results

As regards visual acuity in group A, 18 cases (90%) showed improvement by two or more lines at the end of the follow-up period, whereas two cases (10%) showed no change in their preoperative visual acuity. In group B, 17 patients (85%) showed improvement by two or more lines at the end of the follow-up period, whereas three patients (15%) showed no change in their preoperative visual acuity. The postoperative BCVA in group A ranged from 0.1 to 0.5, whereas the mean preoperative visual acuity was 0.29 ± 0.139. The postoperative BCVA of the eyes included in group B ranged from 0.1 to 0.5, whereas the mean postoperative visual acuity was 0.26 ± 0.115.

The difference between the two groups as regards postoperative visual acuity was statistically not significant (P = 0.322) [Table 3].
Table 3: Statistical analysis of final BCVA in all cases

Click here to view


As regard fundus examination, in group A preoperatively six cases (30%) had mild, 12 cases (60%) had moderate, and two cases (10%) had severe NPDR. After a postoperative period of 6 months (final follow-up visit) DR progressed to mild in four cases (20%), moderate in 14 cases (70%), and severe in two cases(10%). In group B, nine cases (45%) had mild, eight cases (40%) had moderate, and three cases (15%) had severe NPDR. Six months postoperatively (final follow-up visit) DR progressed to mild in five cases (25%), moderate in 10 cases (50%), and severe in five cases (25%).

Difference between both groups

It was found that progression of DR occurred in 10% of patients in group A compared with 20% in group B. The difference between groups as regards DR progression was highly significant (P = 0.001).

Optical coherence tomography

OCT was performed for all eyes enrolled in our study preoperatively and at 3 and 6 months postoperatively. CMT was compared at different intervals and statistically significant improvement was observed in each group separately at the sixth month.

The CMT was evaluated in each group as follows [Table 4]: in group A, at the first follow-up, the CMT ranged from 210 to 470 mm, with a mean foveal thickness of 300.35 ± 76.28 mm, whereas at last follow-up it ranged from 158 to 360 mm, with a mean CMT of 250.54 ± 82.41 mm. In group B, at the first follow-up visit at 3 months it ranged from 200 to 490 mm, with a mean foveal thickness of 333.35 ± 75.42 mm, whereas at the last follow-up it ranged from 180 to 430 mm, with a mean CMT of 285.8 ± 67.86 mm.
Table 4: Comparison between changes in the central macular thickness in both groups

Click here to view


Difference between the two groups

The preoperative mean CMT was better in group B than in group A with a statistically nonsignificant difference (P = 0.158) [Table 4].

After 3 months the mean CMT in group A was better than that in group B, with a statistically significant difference (P = 0.048).

After 6 months the mean CMT in group A was better than that in group B, with a statistically significant difference (P = 0.032).

Fluorescein angiography

Preoperatively 12 patients (60%) in group A had no macular oedema, whereas eight patients (40%) showed focal macular oedema. In contrast, 11 patients (55%) in group B showed no macular oedema (no leakage by fluorescein angiography), whereas nine patients (45%) showed focal macular oedema (focal leakage at the macular area). Statistically, the difference between groups as regards preoperative macular oedema was not significant (P = 0.213) [Table 5].
Table 5: Results of fluorescein angiogram in the two groups

Click here to view


Group A

In group A, after 3 months of follow-up 11 eyes (55%) showed no evidence of dye leakage in late phases of the angiogram, eight eyes (40%) showed focal leakage, and one eye (5%) showed persistent diffuse leakage. At the final follow-up, 10 eyes (50%) showed no evidence of dye leakage in late phases of the angiogram, eight eyes (40%) showed focal dye leakage, and two eyes (10%) showed persistent diffuse leakage [Figure 1],[Figure 2],[Figure 3] and [Figure 4].
Figure 1: Preoperative fundus fluorescein angiography of the retina of a patient 4 in group A, showing focal dye leakage in the late angiograms with encroachment on the FAZ.

Click here to view
Figure 2: Final fundus fluorescein angiography of the retina of a patient 4 in group A, showing focal dye leakage in the late angiograms with encroachment on the FAZ.

Click here to view
Figre 3: Preoperative fundus fluorescein angiography of the retina of a patient 3 in group B, showing diffuse dye leakage in the late angiograms with encroachment on the FAZ.

Click here to view
Figure 4: Final fundus fluorescein angiography of the retina of a patient 3 in group B, showing more diffuse dye leakage in the late angiograms with encroachment on the FAZ.

Click here to view


Group B

After 3 months of follow-up, eight eyes (40%) showed no evidence of dye leakage in late phases of the angiogram, eight eyes (40%) showed focal dye leakage, and four eyes (20%) showed persistent diffuse leakage. At the final follow-up, eight eyes (40%) showed no evidence of dye leakage in late phases of the angiogram, six eyes (30%) showed focal dye leakage, and six eyes (30%) showed persistent diffuse leakage. The difference between the two groups was statistically significant with respect to changes in the fluorescein angiogram at 3 months (P = 0.046) and 6 months (P = 0.025) [Table 5].


  Discussion Top


This study has demonstrated that the degree of diabetic macular oedema generally worsened after cataract surgery, but thereafter decreased gradually. Our results agree with previous studies by Dowler et al. [7] and Funatsu et al. [9], who showed that diabetic macular oedema progressed in ~20-40% of eyes that underwent cataract surgery, but in a considerable percentage of these eyes the macular oedema resolved spontaneously.

Similar to the results of the present study, Hayashi et al. [10] postulated that the degree of diabetic macular oedema generally worsens after cataract surgery. However, macular oedema that occurs after cataract surgery resolves spontaneously in some patients for up to a year.

In the present study it was reported that two cases (10%) of uncomplicated phacoemulsification (group A) showed progression of mild DR to moderate DR, whereas in group B, which had an accidentally opened posterior capsule during surgery, four cases (20%) showed progression of mild DR to moderate DR and two cases (10%) showed progression of moderate DR to severe NPDR. The percentage of cases that showed progression was higher in group B (20%) and the difference was statistically significant (P = 0.001).

The rates of progression in the uncomplicated group were lower than those reported by Zaczek et al. [11], who studied progression of DR after phacoemulsification in diabetic patients at different stages of DR and in controls. The present rates were also lower than those reported by Borrillo et al. [12], who studied the rate of progression of DR following phacoemulsification surgery in the same year and reported 25% progression over 6-10 months of follow-up. Romero-Aroca et al. [13] conducted a prospective study to determine the incidence of DR progression after phacoemulsification in patients with type II diabetes. DR in the operated eye progressed in 23.48% of operated eyes and in 21.21% of fellow eyes. They suggested that uneventful phacoemulsification cataract surgery may not cause DR progression.

In this study, 90% of patients in group A and 85% in group B showed improvement by two or more lines in their visual acuity, whereas the remaining patients showed no change in visual acuity. The mean postoperative visual acuity at the final follow-up visit was 0.27 ± 0.127. In accordance with the present study, Mittra et al. [14] conducted a retrospective study on diabetic patients who underwent phacoemulsification surgery to determine the rate of progression of DR after surgery. They reported that 78% of cases showed improvement by two or more lines in visual acuity.


  Conclusion Top


According to the results of this study we believe that uncomplicated phacoemulsification does not cause acceleration of DR postoperatively. Moreover, macular oedema, which is common after cataract surgery, may follow a benign course and any progression that is observed postoperatively probably represents natural progression rather than being a direct effect of surgery.

It is concluded that posterior capsular tear during cataract surgery in diabetic patients leads to statistically significant higher rates of macular oedema, progression of DR and increase in foveal thickness, which may be explained by interruption of the blood-retinal barrier following posterior capsular tear and subsequent increase in the incidence of postoperative inflammation in diabetic patients with diffusion of inflammatory mediators from the anterior segment to the posterior segment. These inflammatory mediators increase the vascular permeability of the retinal capillaries with increase in foveal thickness and macular oedema.


  Acknowledgements Top


Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Kanski JJ. Retinal vascular disorders. In: Kanski JJ, ed. Clinical ophthalmology: systemic approach, chapter 10. 2nd ed. London, Boston, Singpore, Toronto: Butterworth Heineman Company 1989; 299-367.  Back to cited text no. 1
    
2.
Dowler JG, Hykin PG, Hamilton AM. Phacoemulsification versus extracapsular cataract extraction in patients with diabetes. Ophthalmology 2000; 107 :457-462.  Back to cited text no. 2
    
3.
Shahidi M, Ogura Y, Blair NP, Rusin MM, Zeimer R. Retinal thickness analysis for quantitative assessment of diabetic macular edema. Arch Ophthalmol 1991; 109 :1115-1119.  Back to cited text no. 3
    
4.
Jaffe GJ, Burton TC, Kuhn E, Prescott A, Hartz A Progression of nonproliferative diabetic retinopathy and visual outcome after extracapsular cataract extraction and intraocular lens implantation. Am J Ophthalmol 1992; 114 :448-456.  Back to cited text no. 4
    
5.
Squirrell D, Bhola R, Bush J, Winder S, Talbot JF. A prospective, case controlled study of the natural history of diabetic retinopathy and maculopathy after uncomplicated phacoemulsification cataract surgery in patients with type 2 diabetes. Br J Ophthalmol 2002; 86 :565-571.  Back to cited text no. 5
    
6.
Benson WE, Brown GC, Tasman W. Diabetes and its ocular complications. Philadelphia: Mosby International Ltd 1988; 30-38.  Back to cited text no. 6
    
7.
Dowler JG, Sehmi KS, Hykin PG, Hamilton AM. The natural history of macular edema after cataract surgery in diabetes. Ophthalmology 1999; 106 :663-668.  Back to cited text no. 7
    
8.
[No authors listed]. Treatment techniques and clinical guidelines for photocoagulation of diabetic macular edema. Early Treatment Diabetic Retinopathy Study Report Number 2. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology 1987; 94 :761-774.  Back to cited text no. 8
    
9.
Funatsu H, Yamashita H, Noma H, Shimizu E, Mimura T, Hori S. Prediction of macular edema exacerbation after phacoemulsification in patients with nonproliferative diabetic retinopathy. J Cataract Refract Surg 2002; 28 :1355.  Back to cited text no. 9
    
10.
Hayashi K, Igarashi C, Hirata A, Hayashi H. Changes in diabetic macular oedema after phacoemulsification surgery. Eye (Lond), 2009; 23 :389-396,   Back to cited text no. 10
    
11.
Zaczek A, Olivestedt G, Zetterström C. Visual outcome after phacoemulsification and IOL implantation in diabetic patients, Br J Ophthalmol 1999; 83 :1036-1041.  Back to cited text no. 11
    
12.
Borrillo JL, Mittra RA, Dev S, Mieler WF, Pescinski S, Prasad A, et al. Retinopathy progression and visual outcomes after phacoemulsification in patients with diabetes mellitus. Trans Am Ophthalmol Soc 1999; 97 : 435-445; discussion 445-449.  Back to cited text no. 12
    
13.
Romero-Aroca P, Fernandez-Ballart J, Almena-Garcia M, et al. Non-proliferative diabetic retinopathy and macular oedema progression after phacoemulsification. J Cataract Refract Surg 2006; 32 :1438-1444.  Back to cited text no. 13
    
14.
Mittra RA, Borrillo JL, Dev S, Mieler WF, Koenig SB. Retinopathy progression and visual outcomes after phacoemulsification in patients with diabetes mellitus. Arch Ophthalmol 2000; 118 :912-917.  Back to cited text no. 14
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

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



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and me...
Discussion
Conclusion
Acknowledgements
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed1247    
    Printed16    
    Emailed1    
    PDF Downloaded148    
    Comments [Add]    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]