Postoperative Vitreous Hemorrhages Remain an Issue in Severe Proliferative Diabetic Retinopathy
POVHs Remain An Issue in Severe Proliferative Diabetic Retinopathy
Adequate intraoperative viewing of the anterior vitreous base can prevent many POVHs.
CLAUDE BOSCHER, MD
In the January 2009 issue of Retinal Physician, Greenwald and coauthors1 reviewed the causes and the various strategies developed to reduce postoperative vitreous hemorrhages (POVHs) in proliferative diabetic retinopathy (PDR). In the September 2012 issue of Retinal Physician, Smith and Steel2 addressed the topic, concluding that the incidence of POVH can be reduced, “although sadly not eliminated.”
The rate of POVH and its spontaneous resolution vary greatly in the literature, perhaps primarily because the severity of the disease is not specified in most clinical series. The Diabetic Retinopathy Vitrectomy Study (DRVS) 3 classification (1988) is actually never used.3
Tolentino4 reported in 1989 a POVH rate of 60%, with 209 episodes of bleeding and 38% reoperations, in a series of 139 eyes (multiple episodes of bleeding in the same eyes). Despite progress in vitrectomy technology and skills, the regular updating of practice patterns, and an increase in adjunctive means compared to the 1980s and the 1990s, notably the use of anti-VEGF intravitreal injections, the rate of POVH this century has remained high. It has ranged from 11.5%,5 20% (from 37.5% to 11.5% and 4.3% based on maneuvers performed as adjuncts to vitrectomy),6 26.2%,7, and 20%8 up to 38.8%.9 Spontaneous resolution of POVH ranges in the literature between 62% and 96%.
Claude R. Boscher, MD, is on the faculty of the American Hospital of Paris. She reports no financial interests in any products mentioned in this article. Dr. Boscher can be reached via e-mail at firstname.lastname@example.org.
Moreover, POVH remains an issue. In 2011, Yeh and coauthors10 collected data on 40 eyes operated on between September 2006 and June 2008 that developed recurrent POVH at between one and 25 months. These cases of POVH occurred despite preoperative anti-VEGF injections and intraoperative trans-scleral cryotherapy of the anterior retina and of the sclerotomy sites. A mean of 8.75 postoperative bevacizumab injections (range one to 19) were necessary in MacCumber’s53 2012 series of 12 eyes with POVH.
I believe that the major issue remaining today in the prevention of POVH after vitrectomy for severe PDR is intraoperative viewing and cleansing of the anterior vitreous base (AVB) during primary vitrectomy. My arguments come from:
● the scientific rationale;
● my experience in endoscopy-assisted vitrectomy (EAV) in PDR; and
● careful study of the literature and subsequent strategies developed to prevent this complication.
In my opinion, these strategies finally aim to palliate the insufficient exposure of the operative field under conventional vitrectomy in the specific indication of severe PDR.
The role of retinal ischemia in angiogenesis in DR has been extensively studied and is well established. Following Davis’ clinical observations,11 Machemer in 1978 hypothesized the role of the vitreous cortex, as a scaffold and “mechanical” tractional factor that further stimulates neovascularization, in addition to retinal ischemia, and the potential of vitrectomy as a cure.12 Histopathological, experimental, and clinical studies have confirmed Machemer’s hypothesis.13-16
Anterior hyaloidal fibrovascular proliferation (AHFVP)17 and entry-site neovascularization with fibrovascular ingrowth (FVI) have been identified as a significant causes of POVH.18-21 Fascinating hypotheses and debates on pathogenesis have noted differences and similarities between these two.22-23
Endoscopy shows that both pathologies develop when the anatomical condition after vitrectomy combines enduring ischemia in the anterior retina, and contraction of residual gel in the anterior and posterior parts of the AVB.
Figure 1. Fibrovascular ingrowth at a previous sclerotomy site: contracted residual “skirt” of anterior vitreous gel with new vessels and anterior peripheral retina without thermal ablation.
EXPERIENCE WITH EAV IN PDR
Smith and Steel alluded to the viewing capacities of endoscopy in their 2012 review.2 I was actually exposed for the first time to endoscopic viewing in a patient with HIV and severe PDR, in 1993. I had already seen a tragic case of AHFVP in 1987, in a 26-year-old patient who was already monocular and who died six months later from complications of kidney failure.
The discovery of the endoscopic anatomy of the AVB and of its specific features in severe PDR led me to investigate the curative and preventive potential of EAV.
EAV Study in Severe PDR:1993-2003
My colleagues and I first reported on our prospective, consecutive, non-randomized, interventional study conducted in patients with severe PDR from 1993 to 2003 at the 1998 Gonin meeting in Edinburgh, then at the 1999 AAO meeting (in a poster),24 at the 2002 combined meeting of the Vitreous and Retina Societies in San Francisco, and finally in a poster at the 2004 AAO meeting.25
In 2004, the cohort — originally 13 eyes of eight patients in 1998 — consisted of 61 eyes of 47 patients (22 female/25 male), ages 23 to 68 years old, with type 1 diabetes (duration 16-39 years). All of the patients had histories of poor metabolic control and systemic complications.
Fifty-eight eyes were phakic, and four patients were monocular. All had severe PDR, graded NVC 3 and NVC 4, according to the DRVS 3 classification3. Retinal ischemia on the previous fluorescein angiography studies available covered more than 60% of the retinal surface. Neovascularization was rapidly progressive, and preoperative rubeosis was present in one eye.
Figure 2. Endoscopic panoramic view of anterior ischemic untreated retina after AVB cleansing. Photocoagulation scars appear up to the equator. Residual fibrin strands behind the posterior lens capsule, in the Wieger ligament, and in the anterior hyaloid.
Preoperative thermal ablation was conducted as follows: 49% of eyes received panretinal photocoagulation of ≥4,000 spots; and anterior cryoapplication was performed in two sessions, one and two weeks before surgery in 18% of eyes. Five percent of eyes had no thermal ablation prior surgery.
All eyes had obscuring intravitreal hemorrhages (IVHs). Preoperative B scans demonstrated retinal detachments in 17% of eyes, vitreomacular traction in 19%, interhyaloidoretinal hemorrhages in 15% , and subretinal hemorrhages in 5%.
Endoscopic assistance during three-port pars plana vitrectomy consisted of 360° hyaloidocapsulozonulociliary dissection using a flow-control vitrectomy machine (flow between 1 and 2 cc/min, speed between 100 and 250 cpm, sometimes cut by cut), 360° cleansing of blood clots trapped in the AVB, and high-magnification cleansing of sclerotomies. The lens was avoided by switching sclerotomies and sometimes by opening a fourth sclerotomy. The follow-up ranged from six months to 10.5 years.
Recurrent POVH occurred in the first eye to be operated on, at a time when we had no previous experience, and repeated EAV showed only blood clots left in place in the AVB. Persistent POVH occurred in eight (13%) eyes, due to posterior RDs; rubeosis without neovascular glaucoma (NVG) developed in these eyes.
Iatrogenic retinal tears occurred in 28 of 61 (48%) eyes, anteriorly in 24 eyes, posteriorly in four eyes, and both anteriorly and posteriorly in four eyes.
Iatrogenic lateral lens injuries occurred in seven of 58 (13.7%) eyes. Final visual acuity was ≥20/40 in 28 (45.9%) eyes, ≥20/200 in 38 (62%) eyes, and <20/200 in 23 (37.7%) eyes, including light perception in one eye and no light perception in one eye.
|Instructions for Viewing Videos Online
|To view the videos associated with this article, please view the article online or visit www.youtube.com/user/Retinal Physician1.
Finally, in this homogeneous, prospective, consecutive series of cases of severe PDR, no cases of recurrent POVH were noted after the first eye that was submitted to surgery.
Findings in the AVB of Eyes With POVH in Endoscopic Reoperations
Direct endoscopic viewing shows that incomplete AVB removal in conjunction with incomplete thermal retinal ablation led to FVI at sclerotomies and/or to neovascularization elsewhere in the AVB.
However, direct endoscopic viewing also showed that a significant amount of diabetic POVH may result simply due to the subsequent liberation of blood clots sequestrated into residual gel lamellae of the AVB left in place, a process that can endure for months.
Figure 3. Endoscopic dissection of the Wieger ligament in a phakic eye. A large fresh blood clot and fibrin strands.
Anterior Hyaloidal Fibrovascular Proliferation And Fibrovascular Ingrowth
Our experience reoperating under endoscopy after conventional vitrectomy, for all indications, taught us that even mild amounts of persisting vitreous tissue can generate further traction. FVI is much more rare in proliferative vitreoretinopathy, in which retinal ischemia is a secondary delayed factor, than in PDR, in which it is the triggering factor.
However, FVI does occur in PVR (Video 1). Both clinical conditions are in agreement with the study by Yamashita and coauthors, demonstrating experimentally the potential of tractional forces in accelerating angiogenesis.14
Furthermore, it was actually intraoperative fluorescein angiography, with endoscopic assistance, that demonstrated directly for the first time the role of enduring retinal ischemia anterior to the equator in recurrent POVH.26
In PDR, the contraction of even a small amount of vitreous incarcerated in a sclerotomy can generate FVI if ischemic retinal areas persist in connection to it (Figure 1; Videos 2 and 3). In the presence of retinal ischemia, neovascularization can be triggered anywhere else in the AVB, especially in cases of persisting anteroposterior connections to the Wieger ligament. Even if AFVP, as primarily described, is rare today, as pointed out in most recent publications, it can be encountered in a localized fashion, especially adjacent to a partial RD (Video 4).
During endoscopic primary vitrectomy, enduring anterior ischemia is often disclosed between the equator and the ora serrata, because this area is less accessible for PRP, especially inferiorly, if sessions are conducted in between bleeding episodes. Usually, no associated neovascularization exists (Figure 2). That might be because partial PVD starts and remains long localized posteriorly and at the equator in diabetic eyes, and the accelerating tractional component that stimulates angiogenesis is concentrated at these locations.
Figure 4. Endoscopic cleansing of the anterior part of the AVB. On the video screen is the view in front of the endoscope’s tip (itself invisible). The probe is located anteriorly and superiorly and captures the capsulozonulocliary system.
In endoscopic reoperations of eyes with POVH, FVI and neovascularization elsewhere have never been detected without the association of residual contracted gel with enduring retinal ischemia (Videos 2-5).
Postoperatively, flow control vitrectomy demonstrates the residue has a higher viscosity than primitive gel at this location (Video 3). The accelerating tractional component of the gel skirt left in place at the AVB probably becomes more powerful.
Blood Clots Trapped In the Gel Lamellae of the AVB
This finding explains those cases of multiple consecutive episodes of POVH, followed by consecutive spontaneous resolution episodes long before the era of intravitreal anti-VEGF injections, therefore not involving enduring neovascularization. They can be responsible for a significant number of cases of both persistent and recurrent POVH, with or without FVI and/or neovascularization elsewhere.
High-magnification endoscopy displays the two parts of the AVB, centered on the median white line: the anterior part of the AVB, between the Wieger ligament, the capsulozo-nular system, and the medium white line; and the posterior part of the AVB, between the medium white line and the vitreoretinal juncture.
Indeed, blood can adhere to the Wieger ligament in phakic (Figure 3; Videos 5 and 6), as well as in pseudophakic, eyes (Videos 7-10), to the zonular system (Video 5), and between the ciliary processes (Videos 9 and 10).
Blood clots are often left in place superiorly (Videos 11-13). Actually, enormous quantities of blood can be trapped in the whole AVB. From the first postoperative night to weeks and months later, the blood clots are shed successively over time. They fall in the adjacent residual cortex and then in the empty vitreous cavity, in the inferior AVB, and at the posterior pole, eventually becoming trapped there, along with residual gel adherences.
Blood clots can either be left in place during vitrectomy or become sequestered at the time of recurrent bleeding from any point of origin. Residual active neovascularization may be present.
Early bleeding can originate from the dissection of new and regular vessel walls despite endodiathermy: during awakening after general anesthesia; in the immediate postoperative period; in cases of poorly controlled postoperative blood pressure, even if the quality of hemostasis was checked intraoperatively by lowering the infusion bottle and the infusion pressure and in cases of postoperative hypotony.
Bleeding can arise later from the subsequent mechanical contractions of gel left in place with subsequent completions of posterior hyaloid detachment, without persisting neovascularization, as well as in the presence of incompletely extinguished neovascularization. This can happen in cases of unrecognized vitreoschisis or unrecognized gel adhering due to preoperative PRP or cryotherapy (Video 14).
CAUSES OF POVH IN THE LITERATURE POVH without RD
Beyond FVI and AHFVP, POVH has been also attributed to growing posterior neovascularization after incomplete dissection of the posterior vitreous gel.
Increased awareness of the need to achieve true dissection of the posterior gel and to treat anterior ischemia has been illustrated in publications over the last decade.
However, the specific issue of residual anterior vitreous cortex as a reservoir for blood clots and as an additional autonomous angiogenesis stimulating factor remains underestimated and incompletely addressed.
POVH With RD
If remaining vitreous cortex has been missed, either at the posterior pole or anteriorly, eventually its contraction after surgery, stimulated even more by blood factors, can lead to retinal tears and RD.
Eventually, traction and retinal tears, at the vitreous base during vitrectomy or during crossing by surgical tools at sclerotomies, are unrecognized and lead to RD as well (see the videos accompanying this article). RD itself further generates additional ischemia.
Cases With No Explanation
It is interesting that sometimes no explanation could be found in the literature during reoperations for POVH. This was the case in 65% of cases in Tolentino’s early series4 and in 42% in the extremely carefully studied series of 19 eyes reported by West and Gregor in 2000.5
This lack of explanation could mean that the cause is no longer present at the time of reoperation or that the viewing system used (in West and Gregor’s series, indirect ophthalmoscopy, which provided panoramic viewing, with scleral indentation, plus lensectomy for phakic eyes) was insufficient to determine the cause.
The issues of inadequate visualization of the vitreous gel and its incomplete removal during primary vitrectomy — and the potential of endoscopy to resolve them — were also reported in 2001 by Ciardella and coauthors, who found intraoperative limiting viewing factors in 20% of cases in a retrospective study of charts of PDR.27
TECHNIQUES AND TECHNOLOGIES OF VITRECTOMY IN THE LITERATURE
The description of the technique often amounts to no more than “vitreous and blood clots in the vitreous base were removed as carefully as possible.” The viewing system used is rarely specified. If today there is growing awareness of the importance of the AVB, what was previously referred as the “vitreous base” was often the posterior part of the AVB only.
Wide-angle systems (WAS) allow for, along with external scleral indentation and often lensectomy, the enlargement of visual access to the AVB and the performing of a greater number of dissections and thermal ablations in an increasing number of eyes.
However, it is noticeable that PDR is the only indication for which, even recently, surgeons reported resorting to indirect ophthalmoscopy.5,7,8,28 One study attempted to compare conventional corneal lenses with WAS for PDR and could not demonstrate any statistically significant difference regarding POVH: respectively, 55% vs 42% of persistent and 15% vs 17% of recurrent POVHs, in a series of 180 eyes.29
In fact, the scleral depression that must be performed during WAS compresses the vitreous lamellae and actually masks, along with panoramic viewing, the real depth of the AVB.
Finally, viewing through WAS depends on the transparency of the anterior segment, including the corneal condition, pupil dilation, and lens transparency, which are often compromised in severe DR prior to surgery but which can be even compromised intraoperatively, especially under (sometimes heavy) scleral depression.
Removal of even a clear lens is the last concept elaborated on for improving intraoperative viewing of the AVB during vitrectomy. As pointed out by Suk et al.30 in the May 2012 issue of Retinal Physician, current technology and increased skills improve the safety of the combined procedure.
Figure 5. Intraoperative giant anterior tear due to traction during instrument motions by the incarcerated gel into the sclerotomy on the anterior untreated ischemic retina.
However, PDR still carries a specific risk of postoperative inflammatory complications, especially if heavy intraoperative thermal ablation must be performed. Regarding the prevention of POVH, even a careful study of the literature makes evaluation of the real benefit after combined vitrectomy and lensectomy difficult. POVH was reported in only one eye of 34 in one publication, but there were no data on the severity of the retinopathy.31
Suzuki et al.32 reported in 2000 a reoperation rate of 20% after combined procedures in a series of 155 diabetic eyes, including 13.5% for POVH and 3.5% for NVG. Lahey33 reported in 2003 a reoperation rate of 11% for POVH among 223 eyes. A well-documented series regarding comparable risk factors and preoperative conditions reported no significant difference in POVH between vitrectomy alone and combined procedures. Reoperation disclosed AHFVP or FVI, indicating that the problem of anterior visualization had not been completely solved by lensectomy.34
Dusting the Gel With Triamcinolone Acetonide
The use of chandeliers for endoillumination allows for bimanual dissection. However, identification of subsequent layers of membrane in cases of posterior vitreoschisis is not always reliable.
SURGICAL STRATEGIES DURING VITRECTOMY TO PREVENT POVH
Cryotherapy to Achieve Anterior Thermal Ablation
Anterior cryotherapy was first reported in 1985 for recurrent IVH despite PRP.35 Notably, despite long-known adverse effects, including rupture of the blood-retinal barrier and exacerbation of contraction of the vitreous gel, cryotherapy, an “old” technology compared to the ones provided by the escalation of sophisticated means, has remained36-38 and is currently advocated for6,8,10,39 in the specific case of PDR.
Figure 6. Intraoperative retinal flap inside the untreated anterior ischemic retina (hemorrhage) at the juncture with old laser scars located more posteriorly.
Indeed, applied to the peripheral retina, cryotherapy eliminates persisting anterior retinal ischemia, preventing further angiogenesis, both of the retina and the iris. Applied to the sclerotomies, it suppresses the ciliary epithelial metabolic proinflammatory activity involved in FVI.40
But why would cryotherapy be preferred to endolaser? Yeh and coauthors10 acknowledged “intraoperative PRP [has] limited access to the anterior retina.” They comment further that they “chose cryotherapy over other methods because of its simplicity and safety.”
Yeh and coauthors further acknowledged, “under a wide viewing system, the place and color change of treated areas were clearly visible.” The issue of anterior visualization for adequate PRP during conventional vitrectomy is raised.
Also, one should bear in mind that another recent study found that cryotherapy of the sclerotomy sites actually increased the risk of POVH.41 Finally, anterior retinal ablation with cryotherapy may be insufficient to prevent POVH if residual vitreous has been left in place (Videos 8-10, 13, and 14).
In our 2004 series, we resorted to cryotherapy prior to surgery and intraoperatively, in cases with rubeosis or without thermal ablation at presentation. In two of our cases, for which vitrectomy was delayed after cryo because of interfering illness, the patients actually developed tractional RDs between two and three weeks. However, this was before the anti-VEGF era. Today, we prefer to inject preoperative anti-VEGF and perform PRP up to the ora during EAV.
Perioperative Use of Intravitreal Anti-VEGF Injections and Internal Tamponade
Regarding preoperative anti-VEGF injection, a recent (2011) review of six studies found the incidence of recurrent POVH was “almost significantly less” in eyes pretreated with bevacizumab.42 Another study — not included in the 2011 review — reported in 2009 that 13% of POVHs in 137 eyes were actually not influenced by preoperative injections of bevacizumab.43
Furthermore, 59 additional postoperative injections were necessary over 25 months in Yeh and coauthors’ recent series of 20 eyes, despite complete intraoperative anterior thermal ablation.10
Since November 2005, we have been using intravitreal anti-VEGF injections five to eight days before EAV for PDR. We have found that these injections greatly facilitated intraoperative posterior dissections, and we believe they would have reduced the rate of posterior tears and postoperative RDs, and as a result persistent POVH, in our 2004 series, which were of posterior origin.
We believe that gas tamponade 7,45 can minimize the bleeding from cutting the edge of new vessels, shedding of thrombi, and wound healing at sclerotomy sites, which are caused more often in cases of persistent hemorrhage, present from day 1 postoperatively.
Conversely in such cases, intraoperative anti-VEGF is irrelevant and might even be deleterious (due to the interaction of anti-VEGF and platelet function), as mentioned by Yang et al.44
We have seen that blood clots trapped in the residual AVB alone can cause both types of POVH, persistent and recurrent. Neither gas tamponade nor anti-VEGF injection at the end of vitrectomy will prevent POVH in such cases.
Intraoperative preventive anti-VEGF injections are also not necessary if all neovascular tufts, as well as the conditions for subsequent development of FVI or neovascularization elsewhere, have been thoroughly addressed.
If the conditions remain for FVI and neovascularization to develop elsewhere, intraoperative anti VEGF injections may prevent them indirectly. They can extinguish the activity of the neovascularization, thus inhibiting new bleeding, and as a result the sequestration of additional new blood clots. However, because this action is temporary (four weeks), it may be insufficient in some cases (Video 3), and repetitive POVH will occur.
In summary, as illustrated in the accompanying videos of reoperations for POVH, there are a wide variety of postoperative conditions, and they may coexist. They cannot be clarified, except by a direct, complete AVB evaluation. Only such an evaluation can treat, and most of all prevent, these hemorrhages adequately on a case-by-case basis.
The absence of such evaluations explains the wide variation in POVH rates among various clinical series that seem comparable preoperatively, as well as why there have been varying numbers of postoperative anti-VEGF injections required to cure these hemorrhages.
ADVANTAGES OF EAV
The principles of practice patterns are well established today, but the issue of POVH remains because it is a problem of intraoperative visualization. Endoscopy allows for undistorted 360° viewing and access to the anterior “zonular” vitreous base, without the need for lensectomy or for scleral depression (which masks the real depth of the AVB), independent of the pre- and intraoperative conditions of transparency of the anterior segment.
High magnification allows for visualization of the anterior gel and of the posterior vitreoretinal juncture, which cannot be detected by panoramic control without resorting to dusting or dyeing (Video 15).
Early in our experience, one case that developed postoperative fibrinoid syndrome was of great teaching value because it demonstrated residual gel stuck to the retinal and ciliary surfaces and left in place, both posteriorly and anteriorly, by “insufficiently aggressive” EAV (Video 16).
During primary vitrectomy, high-magnification hyaloidocapsulozonulociliary dissection, in the phakic as well as in the pseudophakic eye, allow for the removal of all clots and for suppression of the canvas for potential future sequestration, from the posterior capsule to the ciliary processes, to the medium white line, and between the medium white line and the ora serrata, as well as between the ora serrata and the anterior limit of many vitrectomies (Video 17).45
The cleansing of sclerotomies (Video 18), followed by PRP until the ora serrata (Videos 2, 6, and 25), allows for the prevention of FVI. The combined use of a flow-control vitrectomy pump allows for indirect control that the posterior hyaloid, as a whole structure, has been removed (Video 19). Blood clots trapped in the AVB can be thoroughly removed, including in the anterior part of the AVB and superiorly (Figure 4; Videos 17 and 20).
At the end of the procedure, all ischemic retinal areas have been treated, and no or minimal gel canvas is left for either FVI or neovascularization elsewhere or for sequestration of blood clots.
Furthermore, endoscopic hyaloidocapsulozonulociliary dissection creates the postoperative anatomical condition called the “state of pseudophakia” by McLeod,46 which accelerates blood clearance though the anterior segment.
Finally, in “everyday real life,” anatomical conditions that lead to surgical indications in PDR are widely variable between extremes, such as RD with NVC4 according to DVRS 3 vs cases of obscuring IVHs by simple traction on vessel walls (new or regular), despite well-conducted PRP. Endoscopy allows for a case-by-case, personalized evaluation of the operative field and of the nature and the number of surgical maneuvers to perform.
SPECIFIC RISKS WITH EAV
The more the surgeon trims the vitreous and the AVB, the greater the risk is of iatrogenic retinal tears on an ischemic fragile friable retina. Indeed, if our own rate of postoperative RD (13% of 61 eyes) is not superior to the rates in contemporary studies (18.5% of 38 eyes)47 and was actually related to posterior, and not to anterior, tears, we acknowledge that an increased risk of anterior iatrogenic retinal tears is the price to pay to achieve complete AVB dissection.
In the September 2012 issue of Retinal Physician, Chao and coauthors48 raised the possibility that the late outbreak of giant retinal tears in PDR might come from “excessive vitreous base shaving.”
Actually, “shaving” the gel under panoramic control, even under scleral depression, does leave a circular “skirt” of tissue with persistent connections between the anterior and the posterior part of the AVB, especially to the Wieger ligament. Further contraction can produce an anterior giant tear inside an ischemic fragile retina, between the ora serrata and the anterior limit of previous PRP, if thermal ablation is not completed until the ora serrata.
Chao and coauthors noted that “pars plana vitrectomy for PDR is not usually considered to be a risk factor for giant retinal tears.” Actually, Aaberg mentioned giant retinal tears in PDR.53 The same pathophysiology applies intraoperatively as well (Figure 5; Video 21).
In addition, vitreous viscosity is higher in PDR,49 perhaps intrinsically or because of repetitive blood invasions. Further, PRP induces vitreoretinal adhesions. Therefore, the disease itself carries a specific additional risk of iatrogenic tears by traction at distance during core vitrectomy (Video 22), during introduction and removal of surgical tools (Videos 21 and 23), and during attempts to dissect vitreous cortex stuck to the retina by laser or cryo (Figure 6; Video 24).
We usually perform complementary anterior thermal ablation, disclosed by endoscopic primary evaluation of the operative field, at the beginning of the procedure and before even central vitrectomy, in an hypothetical attempt to reinforce the retino-retinal adhesions (Video 25). However, pharmacological assistance is certainly a promising approach.50
Independent of the type of tear — giant or not — endoscopy discloses the tear intraoperatively. Complete dissection of the surrounding gel, until there is no connection left, is performed under high magnification, followed by endolaser and internal tamponade. This process suppresses the risk of subsequent RD, as demonstrated in our series, in which the dissections that generated tears and postoperative RDs were at the posterior pole and not at the AVB.
Lessons from the endoscopic anatomy of the AVB and from reoperations with endoscopy for POVH after conventional vitrectomy have led us to develop an approach in severe cases of PDR that may seem “radical” — endoscopy-assisted 360° high-magnification removal of the vitreous cortex, including the anterior part of the AVB.
Actually, EAV allows for the application of the teachings of early — and perhaps forgotten — publications.11-16 It does fulfill the recommendations Aaberg and Abrams delivered in 198751 and Aaberg in 1997, when he gave the W. H. Helmerich III award lecture cited above.
Aaberg concluded, “these obstacles [to successful vitrectomy] should be best managed by prevention rather than subsequent treatment … appropriate management at initial vitrectomy will reduce the incidence of these complications.”
Such control capacity of the specific challenges and complications of vitrectomy in PDR might also encourage early surgical timing. Early vitrectomy had been advocated for severe cases with a potential for high and fast-growing severity, at various times.54-56
At that stage, and even more today with the current use of preoperative anti-VEGF injections, vitreoretinal adhesions at posterior neovascular tufts are still moderate; segmentation can be achieved with vitrectomy and endodiathermy probes alone, and with minimal instrument motions through sclerotomies. Earlier surgery combined with endoscopic visualization of the AVB and pharmacological assistance might prevent complications and improve functional results and cost-effectiveness in this complex, severe disease. RP
1. Greenwald Y, Pollack A, Kleinmann G. Post-vitrectomy diabetic vitreous hemorrhage: etiology, clinical management, and prevention. Retin Physician. 2009;6:46-49.
2. Smith JM, Steel DHW. Rebleeding after diabetic vitrectomy. Retin Physician. 2012;9:56-61.
3. Early vitrectomy for severe proliferative diabetic retinopathy in eyes with useful vision. Results of a randomized trial--Diabetic Retinopathy Vitrectomy Study Report 3. The Diabetic Retinopathy Vitrectomy Study Research Group. Ophthalmology. 1988;95:1307-1320.
4. Tolentino FI, Cajita VN, Gancayco T. Vitreous hemorrhages after closed vitrectomy for proliferative diabetic retinopathy. Ophthalmology. 1989;96:1495-1500.
5. West JF, Gregor ZJ. Fibrovascular ingrowth and recurrent haemorrhage following diabetic vitrectomy. Br J Ophthalmol. 2000; 84:822-825.
6. Yeh PT, Yang CM, Yang CH, et al. Cryotherapy of the anterior retina and sclerotomy sites in diabetic vitrectomy to prevent recurrent vitreous hemorrhage: an ultrasound biomicroscopy study. Ophthalmology. 2005;112:2095-2102.
7. Yang CM, Yeh PT, Yang CH. Intravitreal long-acting gas in the prevention of early postoperative vitreous hemorrhage in diabetic vitrectomy. Ophthalmology. 2007;114:710-715.
8. Steel DH, Habib MS, Park S, et al. Entry site neovascularization and vitreous cavity hemorrhage after diabetic vitrectomy. The predictive value of inner sclerostomy site ultrasonography. Ophthalmology. 2008;115:525-532.
9. Yeoh J, Williams C, Allen P, et al. Avastin as an adjunct to vitrectomy in the management of severe proliferative diabetic retinopathy: a prospective case series. Clin Exp Ophthalmol. 2008;36:449-454.
10. Yeh PT, Yang CH, Yang CM. Intravitreal bevacizumab injection for recurrent vitreous haemorrhage after diabetic vitrectomy. Acta Ophthalmol. 2011;89:634-640.
11. Davis MD. Vitreous contraction in proliferative diabetic retinopathy. Arch Ophthalmol. 1965;74:741-751.
12. Machemer R. Pathogenesis of proliferative neovascular retinopathies and the role of vitrectomy. A hypothesis. Int Ophthalmol. 1978;11-13.
13. Faulborn J, Bowald S. Microproliferations in proliferative diabetic retinopathy and their relation to the vitreous. Corresponding light and electron microscopic studies. Graefes Arch Clin Exp Opthalmolol. 1985;223:130-138.
14. Yamashita H, Hori S. A new model of neovascularization caused by tractional force. Invest Ophthalmol Vis Sci. 1988;29:ARVO E-Abstract 177.
15. Federman JL, Boyer D, Lanning, et al. An objective analysis of proliferative diabetic retinopathy before and after vitrectomy. Am J Ophthalmol. 1979;86:276-283.
16. Akiba J, Arzabe CW, Trempe CL. Posterior vitreous detachment and neovascularization in diabetic retinopathy. Ophthalmology. 1990;97:889-891.
17. Lewis H, Abrams GW, Foos RY. Clinicopathologic Findings in anterior hyaloidal fibrovascular proliferation after diabetic vitrectomy. Am J Ophthalmol. 198;104:614-618.
18. Böker T, Spitznas M. Ultrasound biomicroscopy for examination of the sclerotomy site after pars plana vitrectomy. Am J Ophthalmol. 1994;118:813-815.
19. Bhende M, Agraharam SG, Gopal L, et al. Ultrasound biomicroscopy of sclerotomy sites after pars plana vitrectomy for diabetic vitreous hemorrhage. Ophthalmology. 2000;107:1729-1736.
20. McLeod D. Entry site neovascularisation after diabetic vitrectomy. Br J Ophthalmol. 2000;84:810-811.
21. Hershberger VS, Augsburger JJ, Hutchins RK, et al. Fibrovascular ingrowth at sclerotomy sites in vitrectomized diabetic eyes with recurrent vitreous hemorrhage. Ophthalmology. 2004;105:1215-1221.
22. Krieger AE. Sclerotomy complications following pars plana vitrectomy. Br J Ophthalmol. 2001;8:121-122.
23. Krieger AE (2001). Ultrasound biomicroscopy of sclerotomy sites. Ophthalmology. 2001;108:1175-1176.
24. Boscher C, Cathelineau B, Cathelineau G, et al. Endoscopy-assisted vitrectomy in diabetic retinopathy for prevention of fibrovascular anterior proliferation. Poster presented at: Annual meeting of the American Academy of Ophthalmology; New Orleans, LA; Oct. 29-Nov. 2, 1989.
25. Boscher C, Cathelineau B, Amar R, et al. Recurrent intravitreal hemorrhage after endoscopy assisted vitrectomy (EAV) for severe proliferative diabetic retinopathy (PDR). Poster presented at: Annual meeting of the American Academy of Ophthalmology; New Orleans, LA; Oct. 23-26, 2004.
26. Terasaki H, Miyake Y, Awaya S. Endoscopic fluorescein angiography of peripheral retinal pars plana during vitrectomy or proliferative diabetic retinopathy. Am J Ophthalmol. 1997;12:370-376.
27. Ciardella AP, Fisher YL, Carvalho C et al. Endoscopic vitreoretinal surgery for complicated proliferative diabetic retinopathy. Retina. 2001;21:20-27.
28. Steel H, Habib M, Owen R. Preventing recurrent vitreous hemorrhage. Ophthalmology. 2006;113:2373-2374.
29. Virata SR, Kylstra JA. Postoperative complications following vitrectomy for proliferative diabetic retinopathy with sew-on and noncontact wide-angle viewing lenses. Ophthalmic Surg Lasers. 2001;32:193-197.
30. Suk KK, Murray TG. Combined cataract surgery with pars plana vitrectomy. Retinal Physician. 2012;9:42-46.
31. Jun Z, Pavlovic S, Jacobi KW. Results of combined vitreoretinal surgery and phacoemulsification with intraocular lens implantation. Clin Exp Ophthalmol. 2001;9:307-311.
32. Suzuki Y, Sakuraba T, Mizutani H, et al. Postoperative refractive error after simultaneous vitrectomy and cataract surgery. Ophthalmic Surg Lasers. 2000;31:271-275.
33. Lahey JM, Francis RR, Kearney JJ. Combining phacoemulsification with pars plana vitrectomy in patients with proliferative diabetic retinopathy: A series of 223 cases. Ophthalmology. 2003;110:1335-1339.
34. Kadonosono K, Matsumoto S, Uchio E, et al. Iris neovascularization after vitrectomy combined with phacoemulsification and intraocular lens implantation for proliferative diabetic retinopathy. Ophthalmic Surg Lasers. 2001;32:19-24.
35. Mosier MA, Del Piero E, Gheewala SM. Anterior retinal cryotherapy in diabetic vitreous hemorrhage. Am J Ophthalmol. 1985;100:440-444.
36. Blumenkranz M, Gardner T, Blankenship G. Fluid-gas exchange and photocoagulation after vitrectomy. Indications, technique, and results. Arch Ophthalmol. 1986;104:291-296.
37. Neely KA, Scroggs MW, McCuen BW II. Peripheral retinal cryotherapy for postvitrectomy diabetic vitreous hemorrhage in phakic eyes. Am J Ophthalmol. 1998;126:82-90.
38. Cekic O, Batman C. Peripheral retinal cryotherapy for postvitrectomy diabetic vitreous hemorrhage in phakic patients. Am J Ophthalmol. 1999;127:740-741.
39. Steel DH, Connor A, Habib MS. Entry site treatment to prevent late recurrent postoperative vitreous cavity haemorrhage after vitrectomy for proliferative diabetic retinopathy. Br J Ophthalmol. 2010;94:1219-1225.
40. Koch FH, Kreiger AE, Spitznas M, Glasgow B, et al. Parsplana incisions of four patients: histopathology and electron microscopy. Br J Ophthalmol. 1995;79:486-493.
41. Entezari SM, Ramezani A, Hamadieh H. Cryotherapy of sclerotomy sites for prevention of late post-vitrectomy hemorrhage. Graefes Arch Clin Exp Ophthalmol. 2010;248:13-19.
42. Zaho LQ, Zhu H, Zhao PQ, et al. A systematic review and meta-analysis of clinical outcomes of vitrectomy with or without intravitreal bevacizumab pretreatment for severe diabetic retinopathy. Br J Ophthalmol. 2011;95:1216-1222.
43. Lo WR, Kim SI, Aaberg TM, et al. Visual outcomes and incidence of recurrent vitreous hemorrhage after vitrectomy in diabetic eyes pretreated with bevacizumab (Avastin). Retina. 2009;29:926-931.
44. Yang CM, Yeh PT, Yang CH, et al. Bevacizumab pretreatment and long-acting gas infusion on vitreous clear-up after diabetic vitrectomy. Am J Ophthalmol. 2008;146:211-217.
45. Torii H, Takahashi K, MD, Yoshitomi F, et al. Mechanical detachment of the anterior hyaloid membrane from the posterior lens capsule. Ophthalmology. 2001;108:2182 - 2185.
46. McLeod D. Microsurgical management of neovascularisation secondary to posterior segment ischaemia. Eye. 1991;5:252-259.
47 . Cooper B, Shah GK, Grand MG, et al. Visual outcomes and complications after multiple vitrectomies for diabetic vitreous hemorrhage. Retina. 2004;24:19-22.
48. Chao DL, Gonzales M, Flynn HW. Giant retinal tears after pars plana vitrectomy for diabetic vitreous hemorrhage. Retin Physician. 2012;9(7):40-41.
49. Reed DC, Sharif-Kashani P, Pirouz Kavehpour P, et al. The rheological properties of chopped vitreous from various patient ages and disease states. Invest Ophthalmol Vis Sci. 2012;53:ARVO E-Abstract 3757.
50. Hirata A, Takano A , Inomata Y. Plasmin-assisted vitrectomy for management of proliferative membrane in proliferative diabetic retinopathy: a pilot study. Retina. 2007;27:1074-1078.
51. Aaberg TM, Abrams GW. Changing indications and techniques for vitrectomy in management of complications of diabetic retinopathy. Ophthalmology. 1987;94:775-779.
52. MacCumber M. Intravitreal bevacizumab for recurrent vitreous hemorrhage after vitrectomy for diabetic retinopathy. Paper presented at: Annual meeting of the Retina Society; Washington, DC; October 5, 2012.
53. Aaberg TM Sr. W.H. Helmerich, III, memorial lecture. Presented at: Annual meeting of the American Society of Retinal Specialists; New Orleans, LA; September 1997.
54. O’Hanley GP, Canny CLB. Diabetic dense premacular hemorrhage. A possible indication for prompt vitrectomy. Ophthalmology. 1985;92:507-511.
55. Ramsay RC, Knobloch WH, Cantrill HL. Timing of vitrectomy for active proliferative diabetic retinopathy. Ophthalmology. 1986;93:283-289.
56. Favard C, Guyot-Argenton C, Assouline M, et al. Full panretinal photocoagulation and early vitrectomy improve prognosis of florid diabetic retinopathy. Ophthalmology. 1996;103:561-574.
THE AUTHOR WOULD LIKE TO ACKNOWLEDGE: BERYL CATHELINEAU, MD, AND THE LATE PROFESSOR GERARD CATHELINEAU, CHAIR OF THE DIABETOLOGY DEPARTMENT, HOPITAL SAINT LOUIS, PARIS, WHO UNDERSTOOD VERY EARLY THE POTENTIAL OF EAV AND WHO REFERRED MANY OF THE PATIENTS INCLUDED IN THIS SERIES; MARGUERITE VALLAT, MD, AND STEVEN SINCLAIR, MD, FOR MANY FRUITFUL EXCHANGES ABOUT DIABETIC RETINOPATHY OVER WITH YEARS AND FOR THEIR KIND ADVICE IN THE WRITING OF THIS ARTICLE; AND PROF. THOMAS AABERG, WHOSE LECTURE AT THE 1997 ASRS MEETING INSPIRED OUR APPROACH OF SEVERE PDR WITH EAV AND WHO WAS KIND ENOUGH TO CORRESPOND VIA - MAIL ABOUT IATROGENIC RETINAL TEARS IN PDR.
Retinal Physician, Volume: 10 , Issue: April 2013, page(s): 40 - 49