Visual Prognosis and Surgical Strategy of Bilateral Pars Plana Vitrectomy for Proliferative Diabetic Retinopathy

doi:10.21203/rs.3.rs-5049388/v1

Purpose

This study aimed to analyze the visual outcome in patients with proliferative diabetic retinopathy (PDR) undergoing bilateral pars plana vitrectomy (PPV) to propose an effective surgical strategy.

Methods

This was a retrospective design of 27 patients (54 eyes) with PDR who underwent bilateral PPV. Univariate and multivariate linear regression analyzed factors affect best-corrected visual acuity (BCVA). Differences between the superior and inferior final BCVA groups were compared using t-tests and chi-squared tests.

Results

The mean BCVA from 1.85 ± 0.94 Log MAR preoperatively improved to 0.76 ± 0.95 Log MAR at the final follow-up (P < 0.001). The final BCVA was significantly better in male patients than female patients (coefficient = -0.546, 95% CI: -1.048 to -0.044, P = .033), better in the first surgery eye than in the second (coefficient = 0.530, 95% CI: 0.030 to 1.030, P = .038), worse with postoperative neovascular glaucoma (NVG) (coefficient = 0.614, 95% CI: 0.045 to 1.184, P = .035). Fibrinogen (FIB) levels were negatively correlated with the final BCVA (coefficient = 0.723, 95% CI: 0.295 to 1.152, P = .001). Shorter surgical time was positively associated with the final BCVA (P = .040).

Conclusion

This study suggests that a formulated surgical strategy, including rational selection of the first surgery eye, shorter surgery time, prevention of NVG, and reduction of FIB levels, can significantly improve visual prognosis for patients with PDR undergoing PPV.

Proliferative Diabetic Retinopathy

Bilateral Pars Plana Vitrectomy

Visual Prognosis

Surgical Strategy

Proliferative diabetic retinopathy (PDR) is a common and severe complication in people with diabetes, and it can result in blindness^[1]. PDR is characterized by the abnormal growth of neovascularization, with or without accompanying fibrous tissue. These pathological changes can lead to vitreous or preretinal hemorrhage and tractional retinal detachment (TRD), significantly impairing visual function.

Although pan-retinal photocoagulation (PRP) and intravitreal injections of anti-vascular endothelial growth factor (VEGF) can effectively control the progression of PDR, for patients with advanced stages of PDR, pars plana vitrectomy (PPV) remains the primary treatment^[2-5].

This study analyzed the clinical outcomes of patients with PDR undergoing bilateral PPV. By investigating the factors influencing postoperative visual outcomes, we aim to provide reasonable surgical strategies to improve surgical outcomes and patient quality of life.

This study was a retrospective analysis that included 27 patients (54 eyes) with PDR who underwent bilateral PPV. These patients were selected from those who received treatment between January 2022 and January 2024. Inclusion criteria included diagnosis with PDR and treatment with bilateral PPV, comprehensive preoperative and postoperative data, and a follow-up duration of at least three months. Exclusion criteria included a history of surgery (excluding cataract surgery) and other diseases that may affect vision, such as ocular trauma, keratitis, uveitis, or endophthalmitis. This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Aier Eye Hospital.

We collected basic clinical demographic information, including sex, age, duration of symptoms, duration of diabetes, body mass index (BMI), and hypertension. All patients underwent preoperative and postoperative follow-up ophthalmic examinations, including best-corrected visual acuity (BCVA), intraocular pressure (IOP), and detailed fundus examinations by slit-lamp biomicroscopy and indirect ophthalmoscopy. The duration of surgery and postoperative complications were recorded. According to the staging of PDR by the Chinese Society of Fundus Disease, stage IV refers to vitreous hemorrhage cases, stage V includes fibrovascular membrane cases, and stage VI includes TRD cases^[2]. In addition, the blood glucose (GLU), glycated hemoglobin (HbA1c), and fibrinogen (FIB) levels were collected.

Two vitreoretinal surgeons performed all surgeries. Surgery was performed using standard PPV on a 25-gauge system with intraoperative combined PRP in eyes with severe neovascularization and intravitreal injections of anti-VEGF five days before surgery to reduce intraoperative and postoperative bleeding. In eyes with fibrovascular membranes, the fibrovascular membranes were removed during surgery. In eyes with severe TRD, the retina was reset with SO, which was removed after 3 months. Cataract extraction combined with intraocular lens implantation was performed at the first surgery or SO removal. The order of surgery for both eyes was determined by the severity of PDR and the surgeon's clinical judgment. Postoperatively, patients received topical antibiotics and corticosteroids to prevent infection and reduce the inflammatory response.

SPSS Statistics 24.0 was used for statistical analysis. Continuous variables were presented as mean ± standard deviation (SD), while categorical variables were presented as numbers and percentages. Univariate linear regression analysis was used to identify factors influencing final BCVA. The independent t-test and chi-square test were used to compare the differences between superior and inferior final BCVA outcome groups. A P value < 0.05 was considered statistically significant.

The study included 27 PDR patients, 12 males, and 15 females, all of whom underwent bilateral surgery. A summary of their baseline clinical characteristics is shown in Table 1. The mean age of all patients was 49.35±11.49 years. The mean duration of symptoms was 6.81±5.99 months, while the mean duration of diabetes was 8.61±6.05 years. The mean BMI was 25.88±4.27 kg/m², and 15 patients (55.6%) had hypertension. In terms of diabetic retinopathy staging, 12 patients (22.2%) were stage IV, 14 patients (25.9%) were stage V, and 28 patients (51.9%) were stage VI. Preoperative anti-VEGF therapy was administered to 45 patients (83.3%). The right eye was operated on first in 16 patients (29.63%) and the left eye in 11 patients (20.37%) with a mean operating time of 90.15±34.21 minutes. SO was used during surgery in 24 patients (44.4%). Postoperatively, 7 patients (13.0%) had recurrent VH, which was treated with medical therapy, while 3 patients (5.6%) required additional surgical intervention. Preoperatively, the mean BCVA was 1.85±0.94 Log MAR and the mean IOP was 17.80±2.60 mmHg. Final BCVA improved significantly to 0.76±0.95 Log MAR (p < 0.001), while IOP increased slightly to 17.98±3.17 mmHg.

Table 1. Baseline clinical characteristics of 27 patients (54 eyes) with proliferative diabetic retinopathy who underwent bilateral surgery.

Factors
Male/female, n	12/15
Age, years, meanSD (range)	49.3511.49 (52, 26-74)
Duration of symptoms, months, meanSD (median, range)	6.815.99 (6.00, 0.33-24.00)
Duration of diabetes, years, meanSD (median, range)	8.6116.05 (10.00, 0.08-20.00)
BMI, kg/m², meanSD (median, range)	25.884.27 (24.38, 19.38-37.18)
Hypertension, n (%)	15 (55.6 %)
Staging of DR, n (%)
^†Ⅳ	12 (22.2 %)
^‡Ⅴ	14 (25.9 %)
^*Ⅵ	28 (51.9 %)
Preoperative anti-VEGF therapy, n (%)	45 (83.3 %)
Preoperative BCVA, log MAR, meanSD (median, range)	1.850.94 (1.70, 0.50-3.00)
Preoperative IOP, mmHg, meanSD (median, range)	17.802.60 (18.00, 12.00-24.00)
First surgery eye, n (%)
Right	16 (29.63 %)
Left	11 (20.37 %)
Duration of surgery, minutes, meanSD (median, range)	90.1534.21 (85.00, 35.00-180.00)
Tamponade, n (%)
SO	24 (44.4 %)
Liquid	30 (55.6 %)
Recurrent VH, n (%)
Medication treatment	7 (13.0 %)
Surgical treatment	3 (5.6 %)
Final BCVA, log MAR, meanSD (median, range)	0.760.95 (0.40, 0-5.00)
Final IOP, mmHg, meanSD (median, range)	17.983.17 (18.00, 10.00-30.00)
Final neovascular glaucoma, n (%)	14 (25.9 %)
Final lens status, n (%)
Phakic	17 (31.5 %)
Pseudophakic	37 (68.5 %)
Follow-up, months, meanSD (median, range)	7.46.1

PDR, proliferative diabetic retinopathy; SD, standard deviation; BMI, body mass index; DR, diabetic retinopathy; VEGF, vascular endothelial growth factor; BCVA, best-corrected visual acuity; log MAR, logarithm of minimum angle of resolution; IOP, intraocular pressure; SO, silicone oil; VH, vitreous hemorrhage.

^†With retinal neovascularization or optic disc neovascularization.

^‡With fibrovascular membrane.

^*With tractional retinal detachment.

Univariate linear regression was used to analyze the factors influencing the final BCVA. The analysis identified several variables that were significantly associated with postoperative BCVA. Sex emerged as a significant predictor, with male patients having better visual outcomes compared to females (coefficient = -0.546, 95% CI: -1.048 to -0.044, P = .033). Additionally, patients who underwent surgery on the second eye had worse BCVA (coefficient = 0.530, 95% CI: 0.030 to 1.030, P = .038). Neovascular glaucoma (NVG) was a significant indicator of worse visual outcomes (coefficient = 0.614, 95% CI: 0.045 to 1.184, P = .035). FIB levels significantly negatively correlated with BCVA (coefficient = 0.723, 95% CI: 0.295 to 1.152, P = .001). Other variables, including age, symptoms duration, diabetes duration, hypertension, BMI, DR staging, preoperative anti-VEGF therapy, surgery duration, SO tamponade, recurrent VH, final IOP, GLU, and HbA1c levels, did not show a statistically significant association with postoperative BCVA, (P > 0.05). Multivariate linear regression analysis showed that male (coefficient=-0.506, 95% CI: -0.944 to -0.067, P = .025), second surgery eye (coefficient=0.459, 95% CI: 0.030 to 0.888, P = .037) and FIB (coefficient=0.665, 95% CI: 0.273 to 1.058, P = .001) were significantly associated with final BCVA (Table 2).

Table 2. Univariate linear regression and multiple linear regression analysis of the final BCVA in 27 PDR patients who underwent bilateral surgery.

	Univariate linear regression analysis		multiple linear regression analysis
	Coefficient (95%) CI	P	Coefficient (95%) CI	P
Male	-0.546 (-1.048- -0.044)	.033	-0.506 (-0.944- -0.067)	.025
Age (years)	0.010 (-0.012-0.033)	.361
Duration of symptoms (months)	0.011 (-0.033-0.054)	.628
duration of diabetes (years)	-0.013 (-0.056-0.031)	.564
Hypertension	0.122 (-0.401-0.646)	.641
BMI (kg/m²)	0.047 (-0.013-0.108)	.120
DR staging	0.087 (-0.235-0.408)	.590
Preoperative anti-VEGF therapy	0.140 (-0.558-0.838)	.689
Second surgery eye	0.530 (0.030-1.030)	.038	0.459 (0.030-0.888)	.037
Duration of surgery (minutes)	0.006 (-0.001-0.014)	.102
SO tamponade	0.140 (-0.383-0.663)	.593
Recurrent VH	0.396 (-0.072-0.863)	.096
Final IOP (mmHg)	0.066 (-0.015-0.147)	.107
Final neovascular glaucoma	0.614 (0.045-1.184)	.035	0.416 (-0.084-0.916)	.101
FIB (g/L)	0.723 (0.295-1.152)	.001	0.665 (0.273-1.058)	.001
GLU (mmol/L)	0.085 (-0.039-0.209)	.175
HbA1c (%)	-0.010 (-0.155-0.134)	.885

BCVA, best-corrected visual acuity; PDR, proliferative diabetic retinopathy; BMI, body mass index; DR, diabetic retinopathy; VEGF, vascular endothelial growth factor, SO, silicone oil; VH, vitreous hemorrhage; IOP, intraocular pressure; FIB, fibrinogen; GLU, Glucose ; HbA1c, Hemoglobin A1c.

Several significant differences were observed when comparing the clinical characteristics of the superior and inferior final BCVA groups (Table 3). The superior final BCVA group had a significantly better BCVA outcome with a mean final BCVA of 0.36 ± 0.26 log MAR compared to the inferior BCVA group with a mean final BCVA of 1.15 ± 1.19 log MAR (P = .002). Additionally, there was a significant difference in which eye was operated on first; 19 patients in the superior BCVA group underwent surgery first, while only 8 patients in the inferior BCVA group (P = .003). The mean duration of surgery was also significantly different between the groups, with the superior BCVA group undergoing surgery for a mean of 80.67±26.61 minutes compared to 99.63±38.60 minutes in the inferior (P = .040). There were no significant differences in age, duration of symptoms, BMI, DR staging, preoperative anti-VEGF therapy, preoperative BCVA, preoperative IOP, tamponade, recurrent VH, final IOP, FIB, GLU, and HbA1c levels (P > 0.05).

Table 3. Comparison of clinical characteristics between the superior final BCVA group and inferior final BCVA group

Clinical characteristics	Superior final BCVA	Inferior final BCVA	P
Age (years)	49.30±11.57	49.41±11.63	.972
Duration of symptoms (months)	6.54±6.75	7.08±5.22	.745
BMI (kg/m²)	25.83±4.39	25.92±4.24	.939
DR staging			.788
^†Ⅳ	7	5
^‡Ⅴ	7	7
^*Ⅵ	13	15
Preoperative anti-VEGF therapy	23	22	.715
First surgery eye	19	8	.003
Preoperative BCVA (log MAR)	1.74±0.89	1.96±0.98	.388
Preoperative IOP (mmHg)	17.52±2.90	18.07±2.29	.438
Duration of surgery (minutes)	80.67±26.61	99.63±38.60	.040
Tamponade			.273
SO	10	14
Liquid	17	13
Recurrent VH			.788
Medication treatment	3	4
Surgical treatment	2	1
Final BCVA (log MAR)	0.36±0.26	1.15±1.19	.002
Final IOP (mmHg)	17.81±2.35	18.15±3.85	.703
Final neovascular glaucoma	6	8	.535
FIB (g/L)	2.83±0.46	2.88±0.64	.766
GLU (mmol/L)	6.56±2.03	7.10±2.15	.344
HbA1c (%)	8.18±1.89	7.98±1.76	.690

BCVA, best-corrected visual acuity; BMI, body mass index; DR, diabetic retinopathy; VEGF, vascular endothelial growth factor; log MAR, logarithm of minimum angle of resolution; IOP, intraocular pressure; SO, silicone oil; VH, vitreous hemorrhage; FIB, fibrinogen; GLU, Glucose ; HbA1c, Hemoglobin A1c.

^†With retinal neovascularization or optic disc neovascularization.

^‡With fibrovascular membrane.

^*With tractional retinal detachment.

PPV is a critical treatment for PDR, as it effectively removes VH and fibrovascular proliferative membranes, restores vision, and postpones progress in PDR^{[6, 7]}. Our study results showed a significant improvement in BCVA after PPV in patients with bilateral PDR, with the preoperative mean BCVA improving from 1.85 ± 0.94 Log MAR preoperatively to 0.76 ± 0.95 Log MAR at final follow-up (P < 0.001). These results are consistent with those reported by Patel^[8] et al., who reported a significant improvement in mean Snellen BCVA from 20/774 preoperatively to 20/53 at the final follow-up (P < 0.001). This concordance between studies reinforces PPV's efficacy in treating PDR and highlights its role in visual recovery. In addition, our analysis identified several key factors influencing postoperative BCVA, providing important insights for optimizing surgical strategies.

When examining the influence of gender on visual outcomes, our results indicate that male patients had significantly better postoperative BCVA compared to female patients (P = .033). This difference may be due to physiological differences, such as differences in ocular anatomy and hormone levels, all of which may influence visual recovery. Previous research has documented a higher prevalence of PDR in women with type 2 diabetes, identifying female gender as an independent risk factor for the development of PDR^[9]. Second, diabetic patients with less education are less compliant with eye examinations, and education is negatively associated with vision loss^{[10, 11]}. Historically, women in China have had relatively fewer educational opportunities and heavier family responsibilities, and compliance with regular eye examinations is often lower. The lower compliance significantly accelerated the progression of PDR. It affected the visual recovery of PDR patients after PPV, and patients who had regular eye examinations had significantly better HbA1c levels and postoperative BCVA than those who did not^{[12, 13]}. These findings suggest that gender-specific strategies may be necessary to optimize visual prognosis in PDR patients.

NVG is a secondary glaucoma that carries a high risk of blindness and is difficult to treat effectively. PDR is one of the primary etiologic factors leading to NVG^{[14, 15]}. Another significant finding of our study is the high incidence of NVG after PPV, which was observed in 25.9% of cases. This rate is significantly higher than the 6% incidence reported in a systematic review and meta-analysis^[16]. This may be due to the inclusion of pre-existing NVG cases in our study and the relatively small sample size. Diabetes-induced retinal hypoxia promotes neovascularization. Persistent retinal hypoxia, even after vitreous removal and PRP, may continue to drive neovascularization, especially in patients with poorly controlled diabetes. The postoperative inflammatory response in PDR patients may further exacerbate this condition by disrupting the blood-retinal barrier, increasing vascular permeability, and promoting the release of inflammatory cytokines and VEGF, which contribute to abnormal neovascularization^[17-19]. Neovascularization can lead to angle closure and significant elevation of IOP, resulting in irreversible optic nerve damage and vision loss. We found that patients who developed NVG had a worse visual prognosis at final follow-up (P = .035), which reminds us of the importance of postoperative IOP control and prevention of NVG.

In addition, our study found a significant correlation between FIB levels and final BCVA (P = 0.001), suggesting that elevated FIB levels may be a marker of poor visual prognosis. Fibrinogen, as an acute response protein, is often elevated in response to inflammation and coagulation disorders and is closely associated with microvascular complications in diabetic patients^{[20, 21]}. FIB levels are significantly elevated in patients with PDR^[22]. In PDR patients, high FIB levels typically indicate chronic inflammation or metabolic imbalance^{[23, 24]}. Postoperative inflammation, exacerbated by elevated FIB levels, may increase exudation and fibrous tissue formation, negatively impacting visual recovery. In addition, as a critical component of the coagulation system, elevated FIB may increase blood viscosity, impairing retinal blood flow and exacerbating hypoxia, leading to decreased vision. A study by Huang^[25] et al. showed that reducing FIB levels in diabetic patients with retinopathy could improve blood viscosity, potentially improving retinal perfusion. Our results suggest that management of FIB levels may be critical in predicting and improving visual outcomes after PPV.

The order of surgery also plays a critical role in visual recovery. Our data showed that the first surgery eye had significantly more visual improvement than the second, consistent with previous studies^[26]. Several factors may contribute to the significant improvement in the first surgery eye. Typically, both eyes are not operated on simultaneously but at different times, allowing for a time lag. During this time, the disease may progress and worsen in the second eye^[27]. Persistent hyperglycemia can cause chronic damage to the retinal microvasculature, exacerbating retinal hypoxia, which drives further disease progression, often accompanied by neovascularization and fibrovascular proliferation, both of which can negatively impact postoperative visual recovery. In addition, patients are generally in a better psychological and physiological state at the time of first surgery, contributing to better outcomes. If the recovery from the first surgery is favorable, patients may have higher expectations for the second surgery. However, the early postoperative use of both eyes may influence the visual recovery of the second eye. Careful selection of the eye for the first surgery could optimize visual recovery in bilateral PPV patients.

Finally, we found that shorter surgical times were associated with better postoperative BCVA (P = .04), consistent with Someya et al.^[28]. Longer surgery times may reflect more severe PDR in patients, presenting technical challenges or complications during surgery, resulting in more significant mechanical damage to the ocular tissues and, consequently, more postoperative inflammation. These complex situations may prolong recovery and increase the risk of adverse outcomes. In addition, the duration of surgery may be closely related to the experience and skill of the surgical team. The result suggests that shorter surgical time is a critical factor in improving the visual prognosis of PDR patients.

However, this study has some limitations. Primarily, retrospective design may lead to selection bias. Furthermore, the short follow-up and small sample size limit the generalizability of the findings. Although we identified several predictive factors for visual prognosis, these findings require further validation in larger, prospectively designed studies. Future research should investigate the specific role of systemic factors, surgical techniques, and postoperative management in determining the prognosis of patients with PDR undergoing PPV.

In conclusion, this study shows significant visual outcomes of PPV in treating bilateral PDR and analyzes the key factors affecting visual prognosis. Strategically planning surgical procedures, such as appropriately prioritizing the order of eye surgery, minimizing surgical time, and effectively managing FIB levels and NVG may significantly improve postoperative visual outcomes.

Author Contribution information

Zhi-gang Wang: Writing – review & editing, Writing – original draft, Investigation, Conceptualization.

Ping Li: Writing – review & editing, Writing – original draft, Conceptualization.

Xiu-min Yang: Writing – review & editing, Writing – original draft, Conceptualization.

Zi-qi Wang: Writing – review & editing, Writing – original draft, Methodology, Investigation, Conceptualization.

Chu Zhang: Writing – review & editing, Writing – original draft, Conceptualization.

Competing Interest information: The authors have no conflicts of interest to declare that are relevant to the content of this article.

Causes of blindness and vision impairment in 2020 and trends over 30 years, and prevalence of avoidable blindness in relation to VISION 2020: the Right to Sight: an analysis for the Global Burden of Disease Study [J]. Lancet Glob Health, 2021, 9(2): e144-e160.
Fundus Disease Group OSOCM, Association. Guidelines for clinical diagnosis and treatment of diabetic retinopathy [J]. Chin J Ophthalmol, 2014, 50(11): 851-865.
Uludag G, Hassan M, Matsumiya W, Pham BH, Chea S, Trong Tuong Than N, et al. Efficacy and safety of intravitreal anti-VEGF therapy in diabetic retinopathy: what we have learned and what should we learn further? [J]. Expert Opin Biol Ther, 2022, 22(10): 1275-1291.
Arrigo A, Aragona E, Bandello F. VEGF-targeting drugs for the treatment of retinal neovascularization in diabetic retinopathy [J]. Ann Med, 2022, 54(1): 1089-1111.
Kaźmierczak K, Żuchowski P, Stafiej J, Malukiewicz G. Functional and structural outcomes and complications after pars plana vitrectomy for severe features of proliferative diabetic retinopathy in type 1 and type 2 diabetes mellitus [J]. PLoS One, 2023, 18(7): e0288805.
Lin J, Chang JS, Yannuzzi NA, Smiddy WE. Cost Evaluation of Early Vitrectomy versus Panretinal Photocoagulation and Intravitreal Ranibizumab for Proliferative Diabetic Retinopathy [J]. Ophthalmology, 2018, 125(9): 1393-1400.
Lin TZ, Kong Y, Shi C, Eric Pazo E, Dai GZ, Wu XW, et al. Prognosis value of Chinese Ocular Fundus Diseases Society classification for proliferative diabetic retinopathy on postoperative visual acuity after pars plana vitrectomy in type 2 diabetes [J]. Int J Ophthalmol, 2022, 15(10): 1627-1633.
Patel V, Rohowetz LJ, Pakravan P, Kalavar M, Yannuzzi NA, Sridhar J. Outcomes of Pars Plana Vitrectomy with Panretinal Photocoagulation for Treatment of Proliferative Diabetic Retinopathy Without Retinal Detachment: A Seven-Year Retrospective Study [J]. Clin Ophthalmol, 2023, 17: 471-478.
Kajiwara A, Miyagawa H, Saruwatari J, Kita A, Sakata M, Kawata Y, et al. Gender differences in the incidence and progression of diabetic retinopathy among Japanese patients with type 2 diabetes mellitus: a clinic-based retrospective longitudinal study [J]. Diabetes Res Clin Pract, 2014, 103(3): e7-10.
Klein R, Klein BE, Jensen SC, Moss SE. The relation of socioeconomic factors to the incidence of proliferative diabetic retinopathy and loss of vision [J]. Ophthalmology, 1994, 101(1): 68-76.
Paz SH, Varma R, Klein R, Wu J, Azen SP. Noncompliance with vision care guidelines in Latinos with type 2 diabetes mellitus: the Los Angeles Latino Eye Study [J]. Ophthalmology, 2006, 113(8): 1372-1377.
Itoh-Tanimura M, Hirakata A, Itoh Y, Sano ME, Inoue M, Ishida H. Relationship between compliance with ophthalmic examinations preoperatively and visual outcome after vitrectomy for proliferative diabetic retinopathy [J]. Jpn J Ophthalmol, 2012, 56(5): 481-487.
Micevych PS, Taha AM, Poddar A, Stewart JM. Individual and Systems-Based Risk Factors for Diabetic Vitrectomy in an Urban Safety-Net Hospital [J]. Ophthalmol Retina, 2023, 7(12): 1027-1034.
Dumbrăveanu L, Cușnir V, Bobescu D. A review of neovascular glaucoma. Etiopathogenesis and treatment [J]. Rom J Ophthalmol, 2021, 65(4): 315-329.
Tang Y, Shi Y, Fan Z. The mechanism and therapeutic strategies for neovascular glaucoma secondary to diabetic retinopathy [J]. Front Endocrinol (Lausanne), 2023, 14: 1102361.
Sun D, Lin Y, Zeng R, Yang Z, Deng X, Lan Y. The incidence and risk factors of neovascular glaucoma secondary to proliferative diabetic retinopathy after vitrectomy [J]. Eur J Ophthalmol, 2021, 31(6): 3057-3067.
Azzolini C, Brancato R, Camesasca FI, Codenotti M. Influence of silicone oil on iris microangiopathy in diabetic vitrectomized eyes [J]. Ophthalmology, 1993, 100(8): 1152-1158; discussion 1158-1159.
Gershoni A, Barayev E, Jbara D, Hadayer A, Axer-Siegel R, Dotan A, et al. Postoperative complications of combined phacoemulsification and pars plana vitrectomy in diabetic retinopathy patients [J]. Front Med (Lausanne), 2022, 9: 978346.
Yoshida S, Kobayashi Y, Nakao S, Sassa Y, Hisatomi T, Ikeda Y, et al. Differential association of elevated inflammatory cytokines with postoperative fibrous proliferation and neovascularization after unsuccessful vitrectomy in eyes with proliferative diabetic retinopathy [J]. Clin Ophthalmol, 2017, 11: 1697-1705.
Streja D, Cressey P, Rabkin SW. Associations between inflammatory markers, traditional risk factors, and complications in patients with type 2 diabetes mellitus [J]. J Diabetes Complications, 2003, 17(3): 120-127.
Weisel JW. Fibrinogen and fibrin [J]. Adv Protein Chem, 2005, 70: 247-299.
Zhao H, Zhang LD, Liu LF, Li CQ, Song WL, Pang YY, et al. Blood Levels of Glycated Hemoglobin, D-Dimer, and Fibrinogen in Diabetic Retinopathy [J]. Diabetes Metab Syndr Obes, 2021, 14: 2483-2488.
Sen S, Udaya P, Jeya Maheshwari J, Kohli P, Parida H, Kannan NB, et al. Comparative proteomics of proliferative diabetic retinopathy in people with Type 2 diabetes highlights the role of inflammation, visual transduction, and extracellular matrix pathways [J]. Indian J Ophthalmol, 2023, 71(8): 3069-3079.
Luyendyk JP, Schoenecker JG, Flick MJ. The multifaceted role of fibrinogen in tissue injury and inflammation [J]. Blood, 2019, 133(6): 511-520.
Huang SY, Jeng C, Kao SC, Yu JJ, Liu DZ. Improved haemorrheological properties by Ginkgo biloba extract (Egb 761) in type 2 diabetes mellitus complicated with retinopathy [J]. Clin Nutr, 2004, 23(4): 615-621.
Jiang JH, Wu RH, Ren MX, Lin K, Lin W, Hu XT, et al. Surgical strategy and outcome in patients with bilateral proliferative diabetic retinopathy [J]. Int Ophthalmol, 2023, 43(12): 4921-4931.
Klein R, Knudtson MD, Lee KE, Gangnon R, Klein BE. The Wisconsin Epidemiologic Study of Diabetic Retinopathy XXIII: the twenty-five-year incidence of macular edema in persons with type 1 diabetes [J]. Ophthalmology, 2009, 116(3): 497-503.
Someya H, Muraoka T, Kanda T, Takeuchi M. [Results and Prognostic Factors for Visual Outcome Following Micro Incision Vitrectomy Surgery in Proliferative Diabetic Retinopathy] [J]. Nippon Ganka Gakkai Zasshi, 2016, 120(10): 682-688.

No competing interests reported.

Visual Prognosis and Surgical Strategy of Bilateral Pars Plana Vitrectomy for Proliferative Diabetic Retinopathy

Status:

Version 1

Abstract

Purpose

Methods

Results

Conclusion

Introduction

Methods

Results

Discussion

Declarations

References

Additional Declarations

Status:

Version 1