Abstract
Purpose:
This work evaluates the role of combined phacoemulsification and vitrectomy surgery in the management of cataract associated with noninfectious uveitis.
Methods:
A retrospective chart review was conducted of all patients aged 7 years or older who underwent a combined surgical approach from 2005 to 2018.
Results:
Eighty-five eyes of 67 patients were included in the study; 10.7% of eyes had a best-corrected visual acuity (BCVA) of 20/40 or better at time of surgery. At 1-year follow-up, 63.4% of eyes had a BCVA 20/40 or better and 7.6% had a BCVA of 20/200 or worse. There was an overall decrease in cystoid macular edema after surgery compared with preoperatively (47.6% vs 34.5% presurgery and postsurgery, respectively). Complete inflammatory disease remission off immunomodulatory therapy and systemic steroids was achieved in 21.1% of patients.
Conclusions:
A combined surgical approach is effective in visual rehabilitation in patients with uveitic cataracts and may promote inflammatory disease remission specifically in intermediate uveitis.
Keywords: cataract, phacoemulsification, remission, uveitis, vitrectomy
Introduction
Uveitis is a leading cause of blindness in the developed world, and structural complications related to persistent intraocular inflammation such as cataracts, uveitic glaucoma, cystoid macular edema (CME), and posterior synechiae are common. 1 In children especially, the presence of structural disease at diagnosis is an independent risk factor for the development of further complications. 2 Consequently, prompt diagnosis and a stepwise treatment approach aimed at controlling inflammation are paramount to limit further visual impairment from the inflammatory disease. 3 However, despite aggressive local and systemic approaches to controlling intraocular inflammation, including the use of immunomodulatory therapy (IMT) as steroid-sparing agents, these ocular structural complications persist. 4 The development of cataracts is especially common and frequently requires surgical intervention for visual rehabilitation. 5
Several studies have shown favorable outcomes in uveitis patients who have undergone cataract surgery as long as intraocular inflammation is controlled beforehand. 6 -8 In several other studies, there has been a reported reduction in the incidence of CME and disease activity in patients with intermediate uveitis who have undergone a pars plana vitrectomy (PPV) only. 9 -12 A combined phacoemulsification with PPV has shown efficacy in rapid visual rehabilitation in patients with early or visually significant cataracts and concurrent vitreoretinal pathology and has shown promise in uveitic eyes, while improving visualization during retinal surgery. 13 -15
Although unproven, it has been hypothesized that removal of proinflammatory cytokines and autologous foreign material via vitrectomy may alter the immunologic milieu within the posterior segment. This surgical alteration of the vitreous may promote an immunologically tolerant environment within the eye and facilitate the efficacy of anti-inflammatory therapy. 16 Thus, a surgical intervention that addresses structural complications and rehabilitates vision while potentially allowing better inflammatory control would be highly desirable. However, combined surgery is not without risk. It can be technically difficult because of existing ocular pathology and may carry the risk of exacerbating intraocular inflammation. 17
We hypothesize that combined surgery with phacoemulsification with intraocular lens placement (PCIOL) and a PPV in eyes of patients with cataracts associated with noninfectious anterior-to-intermediate uveitis, intermediate uveitis, or panuveitis would result in improved long-term visual outcomes and facilitate sustained steroid-free remission with or without the need for adjunctive IMT both by addressing the cataract and altering the vitreous inflammatory milieu.
Methods
All participants aged 7 years or older at the time of the study who underwent a PCIOL and PPV for visually significant cataract from 2005 to 2018 were identified by retrospective screening of the electronic medical record. All participants had to have a diagnosis of noninfectious anterior to intermediate, intermediate, or panuveitis based on the Standardization of Uveitis Nomenclature (SUN) criteria and their inflammatory activity (anterior cell, vitreous cell, or vitreous haze) measured. 18 Specific inclusion criteria for a PPV to address structural complications are intermediate uveitis, vitreous hemorrhage, or vitreous opacity precluding a 20/40 view or view of the retina or vitreous haze greater than or equal to 2+; epiretinal membrane (ERM); tractional or rhegmatogenous retinal detachment (RD); refractory CME; and hypotony with cyclitic membranes. As such, a PPV was not used primarily as a therapeutic modality to treat uveitis, but rather was performed in the setting of sight-threatening structural complications that arose in this group of patients. For anterior uveitis and juvenile idiopathic arthritis (JIA)–associated uveitis, the rationale for the combined approach includes removal of anterior hyaloid and vitreous to prevent scaffold for anterior proliferation on the intraocular lens.
We used optical coherence tomography to assess macular edema and multimodal imaging to evaluate for vascular leakage and choroidal lesions. Data were then collected from retrospective chart review and compiled in REDCap (Research Electronic Data Capture, Vanderbilt University) for analysis. 19 A flare was defined as a 2-step increase in level of inflammation (of anterior chamber or vitreous cell or vitreous haze) per the SUN criteria. 18 All eyes were included in this study that met the criteria previously discussed. Patients with infectious uveitis, posterior uveitis, or isolated retinal vasculitis were excluded.
In patients who underwent a PCIOL and PPV, the patient’s intraocular inflammation was controlled for at least 3 months prior to the surgical intervention when possible (RDs were the exception) according to the SUN criteria (less than 0.5+ anterior chamber cell and no vitreous haze). 18 IMT was prescribed if needed and maintained at a stable dose at least 3 months prior to surgery. Most patients received a perioperative systemic steroid taper of 1 mg/kg starting 2 days before surgery and tapered every 5 days thereafter based on inflammation and the clinician’s discretion. For example, in adult patients, oral prednisone was prescribed as follows: 60 mg by mouth every day 2 days prior to surgery and 3 days after, then 40 mg by mouth every day for 5 days, 20 mg by mouth every day for 5 days, then 10 mg by mouth every day for 5 days. Preoperative management also included a topical steroid, in most cases prednisolone acetate 1%, 4 times per day, and a topical nonsteroidal, anti-inflammatory drop 1 week prior to surgery. Topical steroids were tapered 1 drop per week starting 2 weeks after surgery, whereas nonsteroidal frequency was reduced by half 2 weeks after surgery and stopped altogether 4 weeks after surgery. IMT was not stopped until the patient’s disease had been quiet for at least 2 years, and the eventual decision to stop the medication was based on the clinician’s discretion and length of steroid-free disease quiescence.
Cataract surgical procedures were performed using a clear corneal approach. A single-piece, acrylic lens was placed in the capsular bag when possible and a 3-piece acrylic lens was placed in the sulcus in the others. In the pediatric cases, a posterior capsulotomy was performed using a posterior approach. With regard to the pars plana vitreoretinal techniques, a range of 20-, 23-, and 25-gauge instruments was used to perform a core PPV. Elevation of the posterior hyaloid was attempted and performed in all cases except in those of anterior-to-intermediate uveitis or when doing so might increase the risk of iatrogenic retinal damage. Peeling of an ERM, when present, was performed and a fluocinolone acetonide intravitreal implant was placed in a total of 4 eyes. Two to three rows of laser were applied posteriorly to the snowbank, and selective cryotherapy with a single freeze-thaw cycle was applied to the active neovascularization of the snowbank when present. In the 2 cases of RD necessitating surgery, a C3F8 gas tamponade was used.
Disease remission was defined according to our expanded SUN criteria as complete inflammatory quiescence (anterior chamber cellular grade < 0.5+, vitreous haze grade of zero, absence of CME, and/or no new or enlarged chorioretinal lesions or retinal vasculitis) for a minimum of 3 months, without adjunctive local or systemic steroid use. Inflammatory disease remission was further stratified to those eyes on stable doses of IMT and those not on IMT or successfully tapered off.
Statistical analysis was performed using a t test or chi-square test when applicable and a P value of less than .05 was considered statistically significant.
Results
The study population characteristics are shown in Table 1. Eighty-five eyes of 67 patients met the inclusion criteria of undergoing a PCIOL and PPV for visually significant cataract associated with noninfectious anterior-to-intermediate uveitis, intermediate uveitis, or panuveitis. The mean age at time of surgery was 32.8 years, 57% were female, and the right eye was the operative eye in 55.3% of cases. Mean length of time from diagnosis to surgery was 539 days (range, 8-2920 days). Eighteen patients included in the study underwent bilateral surgery on separate occasions. Intermediate uveitis compromised 55.3% of diagnoses, followed by anterior-to-intermediate uveitis and panuveitis at 25.9% and 18.8%, respectively. The majority of cases were undifferentiated; however, sarcoidosis was the most commonly associated systemic disease. Methotrexate and adalimumab were the most commonly used immunomodulatory agents. A total of 71.6% of patients received at least 1 IMT agent and more than 50% of the population received at least 2 drugs. Only 4.8% of patients received long-term systemic steroids and the mean dose was 5 mg per day. Disease quiescence, as defined by our expanded SUN criteria, was achieved in 97.6% of patients for at least 3 months prior to surgery.
Table 1.
The Study Population.
| Demographics | Mean, % | Range |
|---|---|---|
| Age, y | 32.8 | 4–69 |
| Sex, % | ||
| Male | 43 | |
| Female | 57 | |
| Eye, % | ||
| Right | 55.3 | |
| Left | 44.7 | |
| Bilateral surgery, % | 13.4 | |
| Diagnosis, % | ||
| Anterior-to-intermediate uveitis | 25.9 | |
| Intermediate uveitis | 55.3 | |
| Panuveitis | 18.8 | |
| Underlying disease, % | ||
| None | 64.7 | |
| JIA | 5.9 | |
| MS associated | 4.7 | |
| HLA-B27 associated | 7.1 | |
| VKH | 2.4 | |
| Fuch’s iridocyclitis | 1.2 | |
| TINU | 1.2 | |
| Sarcoidosis | 10.6 | |
| Psoriatic | 1.2 | |
| IMT, % | ||
| Methotrexate | 72.1 | |
| Mycophenolate | 32.8 | |
| Adalimumab | 39.3 | |
| Cyclosporine | 6.6 | |
| Tacrolimus | 1.6 | |
| Remicade | 11.5 | |
| Oral NSAID | 8.2 | |
| Long-term oral steroid (< 7.5 mg) | 4.8 | |
| 1 IMT agent, % | 19.8 | |
| 2 IMT agents, % | 48.1 | |
| 3 IMT agents, % | 3.7 | |
| Quiescence > 3 mo, % | 97.6 | |
| Intraoperative complications | 4.7 | |
| CME prior to surgery | 47.6 | |
| CME following surgery | 34.5 | |
| Onset of disease prior to surgery, d | 539 | 8–2920 |
| Follow-up, d, mean (SEM) | 1780 (1693) | 27–6187 |
| Eyes followed at time point, % | ||
| 6 mo | 96 | |
| 1 y | 80 | |
| 2 y | 58 | |
| 3 y | 51 | |
| 4 y | 44 | |
| 5 y | 33 |
Abbreviations: CME, cystoid macular edema; IMT, immunomodulatory therapy; HLA, human leukocyte antigen; JIA, juvenile idiopathic arthritis–associated uveitis; MS, multiple sclerosis; NSAID, nonsteroidal anti-inflammatory drug; TINU, tubulointerstitial nephritis and uveitis; VKH, Vogt-Koyanagi-Harada syndrome.
The most common indication for surgery was a visually significant cataract (Figure 1A). An intraocular lens was placed in all but one case, and in one other case had to be removed because of persistent inflammation following surgery (data not shown). Posterior synechialysis was performed in 25% of cases, whereas an ERM required removal in 27% of cases (Figure 1B). Patient follow-up mean was 1780 days after surgery.
Figure 1.
Surgical information and visual acuity outcomes. (A) The cause for surgery is plotted as the percentage of the total. (B) The percentage of surgical procedures in addition to pars plana vitrectomy and phacoemulsification. (C) Best-corrected VAs (BCVAs) were divided into 20/40 or better, 20/50 to 20/150, and 20/200 or worse subgroups and recorded before surgery, at 1, 3, 6, and 12 months after surgery, and then at final recorded follow-up and plotted as the percentage of the total population. (D) Preoperative and final BCVAs were compared and percentage of the total population was recorded. BCVAs that improved were compared by chi-square analysis with those that remained unchanged or were worse. **P < .01. Pre indicates before surgery; RD, retinal detachment.
Approximately 42% of patients had a best-corrected visual acuity (BCVA) in the affected eye of 20/200 or less prior to surgery (Figure 1C). By 1 month postoperatively, less than 10% of patients had a BCVA of 20/200 or worse (see Figure 1C). Sixty-three percent of patients had a BCVA of 20/40 or better by 1 year; 7.6% had a BCVA of 20/200 or worse at this time (see Figure 1C). Visual improvement remained relatively stable throughout the patients’ long-term follow-up (mean 1780 days), with 62.4% of patients having a final BCVA 20/40 or better (see Figure 1C). Only 3 eyes were lost to follow-up prior to 90 days after surgery and 80% were still being followed at 1 year (see Table 1). In total, this resulted in a statistically significant improvement in BCVA in 84.7% of eyes from preoperative to final examination when compared with those that were unchanged (7.1%) or became worse (8.1%) since before surgery (Figure 1D).
An intraoperative complication was reported in 4.7% of cases, and in all cases was associated with capsular violations (see Table 1). The most common postoperative complication and cause of vision loss was the development of a posterior capsule opacification in 38.1% and 38.8%, respectively (Figure 2). A total of 41.2% of cases had no postoperative complication noted (see Figure 2A). Approximately 5% of patients would require long-term medical management of ocular hypertension with 88.6% of these patients requiring at least 2 ocular antihypertensives (see Figure 2A). The most significant complication was poorly controlled, elevated intraocular pressure requiring surgery in 14.3%, of which 87.5% of eyes would eventually require tube shunts if not the initial intervention (see Figure 2A). Despite these measures, significant glaucoma progression was noted in 8.2% of the study population (see Figure 2B). CME was another common cause of postoperative vision decline within the patient population; however, there was a 27.5% reduction in eyes with CME postoperatively compared with before surgery (34.5% vs 47.6%, respectively) (Figure 2B, Table 1).
Figure 2.
Postoperative complications and causes for vision decline. (A) Postoperative complications and (B) postoperative causes of vision decline are plotted as a percentage of the total study population. CME indicates cystoid macular edema; ERM, epiretinal membrane; IOL, intraocular lens; OHT, ocular hypertension; PCO, posterior capsule opacification.
The total number of inflammatory flares was counted for each eye during follow-up. Fifty-five percent of eyes did not have an inflammatory flare per our expanded SUN criteria and/or CME requiring treatment after surgery, and more than 90% of eyes had 3 or fewer such flares postoperatively (Figure 3A). Further evaluation revealed that 49.1% of patients on IMT would have no flares following surgery and would remain quiescent on IMT throughout follow-up without additional systemic steroids (Figure 3B).
Figure 3.
Disease recurrence following surgery. (A) The total number of inflammatory exacerbations were counted for each patient, grouped, and plotted as a percentage of the total population. (B) For patients on immunomodulatory therapy (IMT), rates of remission on medication is shown. (C) The total number of flares was compared in 4 patients in whom the fellow eye did not undergo a concomitant vitrectomy. Plotted as the mean number of flares ± SEM.
In 4 cases, the patient underwent a combined PPV and cataract surgery in the first eye and either did not need surgery during the follow-up period or underwent only cataract surgery in the second eye. In 3 of 4 cases, there was at least a 50% reduction in the total number of flares and/or episodes of recurrent CME following the combined surgery compared with the other eye. This approached a statistically significant reduction in number of flares when comparing the 2 eyes (P = .06, see Figure 3C). In the fourth case, neither eye has flared since surgery.
Drug-free disease remission as defined by our expanded SUN criteria (at least 3 months of no inflammatory recurrences during follow-up with cessation of all IMT and off all topical and systemic steroids) was achieved in 15 of 57 eyes (26.3%) (Figure 4A). This was not attempted prior to 2 years of steroid-free therapy except in 1 case, in which the patient stopped treatment prematurely. Three of the 15 patients would eventually require reinitiation of IMT because of recurrent inflammation and/or CME during long-term follow-up (see Figure 4A). The mean time for recurrence was 3 years (range, 1.5-5 years). Subgroup analysis showed the highest rates of recurrence were among patients with anterior-to-intermediate uveitis (50.0%) followed by panuveitis at 20.0% (Figure 4B). No case of intermediate uveitis recurred following cessation of all IMT and steroids (Figure 4B).
Figure 4.
Remission rates following immunomodulatory therapy (IMT) cessation. (A) The percentage of patients who continued, stopped, and restarted on IMT of all patients receiving IMT included in the study. (B) Recurrence was then evaluated by anatomic location of uveitis and displayed in a Kaplan-Meier curve by percentage of the subgroup.
Conclusions
The management of chronic noninfectious uveitis often requires complex clinical decision making to balance the use of early and aggressive local and systemic therapies in an effort to limit structural damage and preserve vision while minimizing the ocular and systemic risks associated with treatment. When surgery is necessary in these uveitic eyes, the stakes are high because of the propensity to exacerbate inflammation and the risk of postoperative complications including hypotony, macular edema, and ocular hypertension. 7,20 In this study we found that with aggressive perioperative inflammatory control, significant VA gains, disease remission with or without IMT, a reduction in inflammatory recurrences, and an overall decrease in CME were possible with a combined surgical approach despite the aforementioned risks.
We found that complications occur following combined PCIOL/PPV surgery despite inflammatory quiescence greater than 3 months preoperatively, and additional surgery is sometimes required, most commonly glaucoma procedures. The number of eyes requiring antihypertensive therapy and/or surgery in our study may seem high at first glance, but is in fact similar to other studies that have found rates of glaucoma approaching 20% in chronic uveitis. 20 Others have found that even with preoperative quiescence, visual outcomes are typically worse following cataract surgery in posterior uveitides compared with anterior uveitis presumably because of vision-limiting retinal pathology in the former. 7,21,22 However, the Multicenter Uveitis Steroid Treatment trial showed cataract surgery in patients with intermediate uveitis, posterior uveitis, or panuveitis resulted in visual outcomes of 20/40 or better in 62% of patients at 9 months. 5 These results were similar to our findings of cases with a combined PCIOL/PPV (62% vs 62.4% at 9 months and final follow-up, respectively) and those with vitrectomy only. 5,12
Overall, nearly 85% of the patients in our study had an improvement in BCVA at their last follow-up compared with preoperative BCVA despite ocular comorbidities. Thus, a combined approach resulted in favorable outcomes despite the longer, more complicated surgery while also increasing the chance of disease remission.
We hypothesize that the combined surgical approach more frequently fails to induce long-term, drug-free remission in anterior-to-intermediate uveitis because of the primary locus of the inflammation. In anterior uveitis, most inflammation is confined to the anterior chamber, iris, and ciliary body and would not be readily affected by removing the vitreous. In this study anterior-to-intermediate uveitis remission rates were not readily affected by the combined approach. In intermediate uveitis and panuveitis, however, there is a significant elevation in pro-inflammatory mediators within the vitreous compared with anterior uveitis. 23,24 An abrupt reduction in the antigenic load from a PPV would presumably result in an improvement in overall disease activity in these subtypes of uveitis by altering the inflammatory environment, as seen in our study with higher rates of drug-free remission. 24,25
The patients in our study with intermediate uveitis also did not need to be restarted on IMT like that seen in the anterior-to-intermediate uveitis group. Others have proposed that a unicameral eye promotes an immunologically tolerant environment by allowing diffusion of anti-inflammatory compounds from the anterior chamber into the vitreous cavity, and this change in diffusion is responsible for the reduction in inflammation following surgery. 26 Although the exact mechanism has yet to be elucidated, the rapid and profound surgical reduction in inflammation promoted a statistically significant improvement in drug-free remission rates in our study, specifically in intermediate uveitis, and previously by others. 16,27 Treatment of the pars plana snowbank likely helped remission rates because it alone has shown efficacy in inducing remission of pars planitis. 28 Unfortunately, none of these hypotheses have been proven because of the paucity of prospective, comparative studies and the difficulty mirroring human disease in animal models. 12,16,25
In the one failed case of complete disease remission (drug-free) in panuveitis, the patient stopped treatment prematurely (7 months of total therapy); however, because the disease remained inactive initially, the treating physician elected to withhold restarting therapy unless the disease flared. Two years later, this patient required reinitiation of IMT because of intraocular inflammation and persistent CME. This case highlights the need for prolonged IMT even with surgery and is supported by the finding that early withdrawal of IMT (less than 9 months) in JIA-associated uveitis resulted in inflammatory relapse in 69% of patients. 29 This is in contrast to the arthritic component of JIA, in which a longer duration of remission on medication does not appear to reduce the chance of disease relapse. 30
A combined surgical approach has several practical advantages in the management of uveitic cataract beyond a reduction in inflammatory recurrences and disease remission. Media opacification and posterior segment pathology both may be addressed in a single operative session, thereby reducing cost, adding convenience for the patient, and hastening visual recovery. However, there are a few potential disadvantages including exacerbation of underlying inflammation, unpredictable postoperative pressure, logistical considerations, surgical complications, and issues surrounding the lens to be implanted.
There are several specific strengths to this report. They include the long-term follow-up (mean 1780 days), a study population that is fairly representative of a large, academic uveitis practice, the large number of patients included within the study, and the use of standardized measurement for reporting inflammation (SUN criteria). There are some deficiencies of this study, including the lack of randomization and a control group (ie, patients managed with IMT and/or surgery alone), the small group sizes in complete remission for more extensive comparison, heterogeneity of the study population, selection bias, and its retrospective nature. We also did not investigate the role of intravitreal corticosteroids in these patients, but intravitreal dexamethasone implants have shown good efficacy. 31 We hope these results will highlight the need for a large, randomized controlled trial to evaluate the efficacy of a combined surgical approach. Our experience suggests that a combined surgical approach is effective in visual rehabilitation in patients with cataracts associated with uveitis and may promote inflammatory disease remission, particularly in patients with noninfectious intermediate uveitis.
Acknowledgment
The authors would like to thank Dr. Vincent Hau for his work on this project.
Footnotes
Ethical Approval: This study was approved by the institutional review board at the University of Utah (Protocol 00112830) and the research adhered to the tenets of the Declaration of Helsinki.
Statement of Informed Consent: Informed consent was not sought for the present study because it was deemed by the institutional review board to be a potential risk of a HIPAA (Health Insurance Portability and Accountability Act) breach to contact prior patients and thus was not required.
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The Research to Prevent Blindness, Inc, New York, New York, provided an unrestricted grant to the Department of Ophthalmology & Visual Sciences at the University of Utah. The Centers for Disease Control and Prevention was supported in part by the Heed Ophthalmic Foundation and REDCap was supported by National Center for Advancing Translational Sciences/National Institutes of Health grant 8UL1TR000105. The sponsors had no role in the design of this study.
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