Importance of Recognizing and Preventing Blindness From Juvenile Idiopathic Arthritis Associated Uveitis
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1 Arthritis Care & Research Vol. 64, No. 5, May 2012, pp DOI /acr , American College of Rheumatology REVIEW ARTICLE Importance of Recognizing and Preventing Blindness From Juvenile Idiopathic Arthritis Associated Uveitis STEPHEN D. ANESI AND C. STEPHEN FOSTER The association between rheumatologic and ocular inflammatory disease (OID) is well recognized. Uveitis is one of the leading causes of preventable blindness worldwide (1,2), accounting for 10 15% of causes in the US. One of the most ocularly pernicious forms of uveitis, first described in 1910 (3), is associated with juvenile idiopathic arthritis (JIA), which was previously known as juvenile rheumatoid arthritis or juvenile chronic arthritis. Children younger than 16 years of age represent 5 10% of the population with uveitis (4), and JIA is associated with many of these cases (5,6). Complications from JIA-associated uveitis are well known, especially considering the disease is often occult and not realized by the physician or even the patient until chronic changes and permanent vision loss have occurred. The most recent recommendations for uveitis monitoring in patients with JIA were made in 2006 (7) by the American Academy of Pediatrics in conjunction with a panel of rheumatologists and ophthalmologists. In 2007, the German Uveitis in Childhood Study Group published suggested modifications to these guidelines (8), including a reference to the modified JIA classification by the International League of Associations for Rheumatology (ILAR) in 1995 (9). Screening for uveitis is an underappreciated necessity, as shown by the high percentage of children with complications at initial presentation to a uveitis specialist. One or more complications have been present in 34 67% of children with JIA-associated uveitis (10,11) and have been as prevalent as 86.3% only 3 years after initial presentation. Shockingly, 47% of these patients upon initial presentation were already legally blind (20/ 200 or worse) in at least one eye (10) as a consequence of complications that were likely preventable had the patient been under proper ophthalmologic care. Stephen D. Anesi, MD, C. Stephen Foster, MD, FACS, FACR: Massachusetts Eye Research and Surgery Institution, Cambridge. Address correspondence to C. Stephen Foster, MD, FACS, FACR, 5 Cambridge Center, 8th Floor, Cambridge, MA fosters@uveitis.org. Submitted for publication June 22, 2011; accepted in revised form January 3, Furthermore, complications during long-term followup are profoundly underappreciated, especially by the rheumatologic community. Studies in rheumatologic peerreviewed publications support this, based on observations of patients still under the care of rheumatologists (12,13) but devoid of data from patients who no longer need ongoing rheumatologic care that have progression of eye damage from inadequately treated chronic uveitis. Longterm followup studies of 10 years or less have claimed good outcomes of corrected visual acuity of 20/40 or better ( %) despite high rates of complications ( %) (13,14). A review in the ophthalmologic literature of 43 patients with JIA-associated uveitis with a mean overall duration of uveitis of 12.2 years showed that visual improvement occurred in 70% of patients with therapy, although prognosis was guarded due in part to the large number of patients needing surgery to achieve this (5). Much poorer outcomes are found in studies following patients up to 25 years (15,16). A review of 18 adult patients with JIA-associated uveitis for a mean duration of 20.5 years showed that 100% of eyes had at least one ocular complication (17). There is an obvious need for greater recognition and proper management of JIAassociated uveitis since it too often presents a life-long burden of blindness for children moving into adulthood. JIA has multiple well-documented subsets, including the systemic, polyarticular, and oligoarticular (pauciarticular) forms, with the latter recognized as the most common associated with uveitis (18,19). Established screening guidelines categorize high-risk patients as having oligoarticular, seronegative polyarticular, psoriatic, or other arthritis onset prior to age 7 years with positive antinuclear antibody (ANA) testing and a disease duration under 5 years; it is recommended that these patients be screened at 3-month intervals in the absence of previously diagnosed uveitis (10). A meta-analysis of case series of patients with JIA between 1980 and 2004 (20) found ANAnegative oligoarticular patients have the same risk of developing uveitis as ANA-positive polyarticular patients, and the authors recommend consistency between screening times for these groups (currently 6 months and 3 months, respectively). Rheumatoid factor negativity is typ- 653
2 654 Anesi and Foster Significance & Innovations Juvenile idiopathic arthritis (JIA) associated uveitis is an ocularly pernicious inflammatory disease with underappreciated vision outcomes in longterm studies. Complications result from chronic inflammation and long-term corticosteroid therapy. A stepladder approach using steroid-sparing therapy should be employed early to induce remission from inflammation. Increased efforts in screening, research, and education are necessary to help find and treat children with JIA-associated uveitis. Figure 1. Band keratopathy, posterior synechiae, and severe cataract in a quiet eye of a patient with juvenile idiopathic arthritis associated uveitis (photo courtesy of C. Stephen Foster). ical (21) and antihistone antibodies are receiving more attention as possible biomarkers for disease chronicity and severity risk (22). Screening for psoriatic arthritis, recognized as a subset of JIA by ILAR in 1995 (23), must also be considered. The annual incidence of all childhood uveitis is estimated to be per 100,000 in North America and 30 per 100,000 in Europe (24 26). JIA reportedly has been associated with anywhere from % of cases, with most reports ranging between 10% and 35% (6). Arthritis is often diagnosed prior to the development of eye findings, but a population of children exists in whom ocular inflammation is present prior to joint disease. Studies have shown a marked disparity between joint inflammation and ocular inflammation. One study of 35 children with JIA-associated uveitis in 1986 showed that uveitis followed the onset of arthritis in 60% of the cases by 1 6 years (mean SD years); however, 31.4% of the cases had uveitis noted at the onset of arthritis and 8.6% showed evidence of chronic ocular inflammation (i.e., band keratopathy, synechiae, cataracts) at initial arthritis onset (19). Additional support of the disparity between joint inflammation and ocular inflammation is shown by the differential response to various treatments, some of which have been shown to reduce inflammation in only one of the two sites. Etanercept, an anti tumor necrosis factor antibody biologic response-modifying agent (BRM), has been shown to lack therapeutic efficacy for uveitis despite its ability to control arthritis (27,28). Conversely, daclizumab, an anti interleukin-2 receptor (anti-cd25) antibody BRM, was shown to be effective in treating ocular inflammation; however, one patient was removed from the study due to uncontrolled joint and systemic symptoms requiring alternate therapy (29). Clinically, JIA is usually associated with anterior uveitis, or inflammation (cells and flare) mainly localized to the anterior chamber. It is typically a nongranulomatous chronic inflammation, often bilateral, that remains asymptomatic in many patients. JIA may manifest before or after the onset of articular involvement, sometimes leading to chronic inflammatory changes in the eye (30). An important concept to consider in ocular inflammation is the fragility of the eye relative to much of the rest of the human anatomy. There are several structures within the eye that do not retain function after, or do not have the ability to recover from, chronic inflammation, edema, or fibrosis; therefore, any amount of inflammation in the eye is a potential permanent threat to vision. One study at a uveitis tertiary care center over 21 years examined complications at initial presentation to the ophthalmologist, which included band keratopathy (31.5%), posterior synechiae (27.5%), cataracts (22.5%), glaucoma (15.3%), ocular hypotony (9.3%), and macular edema (3.0%) (31) (Figure 1). In the same study, 23.7% of these patients had 20/200 or worse vision in the better-seeing eye. These data are stunning, and it is our strong impression that they are unknown to most rheumatologists. Also problematic is that these data are at times refuted by other studies, as in the aforementioned meta-analysis reporting that adverse visual outcomes (acuity worse than 20/40) were less than previously reported (20). These claims are misleading, however, since this study did not account for visual acuity between the patients individual eyes, which is important considering the tremendous advantage of proper stereoscopic vision, which requires good acuity in both eyes; several of the reviewed series were reported by nonophthalmologists. These studies also underrepresent the population with uveitis, again considering patients with JIA-associated uveitis who have little or no rheumatologic followup due to quiescence of joint inflammation but have active ocular disease. Complications are often found in patients with JIAassociated uveitis, especially in those not receiving timely and effective treatment. Proper management of all ocular inflammation is critical to good long-term prognosis, and should include swift referral to a specialist who is comfortable dealing with OID. Another important concept is avoidance of long-term corticosteroid therapy, whether topical, systemic, or locally injected, which invariably leads to complications. Many patients require long-term systemic therapy with nonsteroidal antiinflammatory drugs (NSAIDs) or immunomodulatory therapy (IMT) to control stubborn vision-threatening inflammation refrac-
3 Preventing Blindness From Uveitis in JIA 655 tory to conservative measures. One study from a tertiary care center examining 89 children with JIA-associated uveitis over 18 years showed that 73% of these children were receiving IMT and 40% were treated with IMT and NSAIDs (6). A stepladder approach can be used when deciding upon systemic medication for ocular inflammation, requiring regular examinations and monitoring for drug toxicity (32). Many obstacles are encountered by ophthalmologists managing JIA-associated uveitis in children. They are often forced to manage the large amount of complications these patients have prior to initial presentation. As stated earlier, ocular inflammation occasionally presents with or prior to joint involvement, typically without any warning signs or symptoms noticeable to the child. Many children are too young or naive to notice or mention problems with their vision, or they fear the social stigma of possibly needing glasses. These children are poor advocates for themselves in an incredibly serious matter that they, depending on their age or maturity, often cannot be expected to comprehend. Examining these children may also be difficult, and subtle inflammation may be missed by an untrained or unsuspecting examiner. Sadly, specialists must also shoulder the burden of complications arising because of all the providers who were both inexperienced in properly managing OID and too stubborn to reach out to and comanage with those more knowledgeable; after all, the degree of inflammation may not seem that bad and topical corticosteroid therapy should certainly be able to take care of that. While corticosteroids are sometimes necessary for acute inflammation, long-term treatment must absolutely not be relied on since corticosteroids often are not enough to control the disease and inevitably lead to cataract formation and possibly glaucoma. Parents often advocate for referral themselves after their child has been subjected to repeated problems. Childhood uveitis is an aggressive disease that must be treated aggressively. Proper management includes knowledge of what therapy to use and when to use it, while moving along to something else if one therapy proves to be ineffective. When NSAIDs are ineffective in preventing relapse of uveitis after the child is completely off all corticosteroid therapy, or when inflammation is overtly severe, antimetabolites (i.e., methotrexate, azathioprine, mycophenolate mofetil), calcineurin inhibitors (modified cyclosporin) in conjunction with antimetabolites, and BRMs (i.e., infliximab, adalimumab, rituximab, abatacept) have been used off label to great effect in treating chronic inflammation from JIA-associated uveitis (33 40). Over the past 2 decades, BRMs have garnered greater attention in both the rheumatologic and ophthalmologic communities, given how successful these medications have become in treating some inflammation refractive to other known therapies. Alkylating agents are generally avoided but may be appropriately used in extreme cases. Similar to recent rheumatologic standards, the mission must be remission, treating to a target of no active inflammation with complete stoppage of corticosteroid treatment. Different patients respond to different therapies differently, and we have no way to predict which children will be among the 70% who respond to methotrexate monotherapy and which may require intravenous immunoglobulin in combination with rituximab. When administered under close supervision, medications should provide an escape from the life-long rescue with topical and systemic corticosteroid therapy, and many times in the experience of these authors, the medications can be stopped indefinitely after approximately 2 years of immunomodulation without recurrence of further disease activity. The notion that these medications are too risky is profoundly inaccurate, shown by the abundance of reports and retrospective series in peer-reviewed publications supporting the use of IMT in treating JIA-associated uveitis; prospective trials are, few as they may be, difficult to justify and carry out in this population. What else can be done to lessen the amount of poor outcomes seen so frequently in this disease? Since relying on presentation of arthritis is not always effective in catching the early development of ocular inflammation, we advocate that more assertive action be taken. This can only be possible through wider and earlier screening in preschools and day care programs, and may help lower both the percentage of complications seen at initial presentation to specialists and the number of poor visual outcomes of these children in general. Additionally, children with JIA-associated uveitis need proper management of their disease, which includes avoiding long-term corticosteroid monotherapy and moving to IMT when necessary. Providers who feel uncomfortable managing these patients should advocate for the help of others, preferably fellowship-trained uveitis specialists. This would also include providers who are unable to bear the burden of costly off-label medications and the strenuous process of obtaining prior authorization coverage. Herein yet another problem arises, that too few eye specialists exist who are comfortable treating these patients either medically or surgically. The number of such trained ophthalmologists is quite insufficient for the needs of the population affected. Therefore, many ophthalmologists need to partner with a rheumatologist or hematologist in a comanagement strategy that will allow the child to receive such needed care, rather than simply reverting to the expedient of continuing therapy with corticosteroids. An additional problem is that we repeatedly see instances in which such collaboration is not collegial, but rather antagonistic, with the rheumatologist or hematologist uncomfortable taking the responsibility of prescribing medications that possess risk while being dependent upon the ophthalmologist to determine and report that inflammation is sufficient enough to warrant such therapy or more therapy. Some doctors seem comfortable taking the ophthalmologist s word, while others clearly do not seem comfortable, and hence the antagonism, with the patient ultimately experiencing the consequences. Also, active communication between all providers involved is essential in the proper management of IMT, including when it is appropriate to increase or taper therapy. There is a need for increased education for everyone involved in the care of children with JIA-associated uveitis. An emphasis on the importance of recognizing and properly treating JIA-associated uveitis must be made dur-
4 656 Anesi and Foster ing the early phases of physician education. Dedicated lectures and training during medical school, residency, and fellowship programs by faculty who are either uveitis specialists or familiar with the current standard of care regarding management of JIA-associated uveitis are sorely needed; there is a gross deficiency of uveitis faculty throughout the ophthalmology training programs in the US. Rheumatology and pediatric programs alike must educate their residents and fellows in these matters to maximize the support available to these children and their families. An increase in the amount of discussion and research in professional forums is also needed to help heighten the awareness of the debilitating nature and proper management of this disease. In August 2010, an expert panel of ophthalmologists and rheumatologists in the management of JIA-associated uveitis met in Boston to help form a consensus of opinions on the treatment of all forms of uveitis in children, with special emphasis on JIAassociated uveitis. The results of this roundtable meeting and a consensus of the opinions of these experts were published as a childhood uveitis monograph (41). Efforts by organizations such as the Ocular Immunology and Uveitis Foundation (OIUF) and the Childhood Arthritis & Rheumatology Research Alliance (CARRA) to advance research in pediatric uveitis and rheumatologic disease and to provide training for individuals to apply the knowledge gained from such research have made great strides toward increasing awareness and improving outcomes of JIA and JIA-associated uveitis. Last, the families of children with JIA need to be made aware of the dangers of chronic uveitis if left untreated and the need for frequent monitoring. These families must realize that they are their child s best advocate in the fight to prevent blindness from this disease, and that they must be actively involved in their child s disease management and future. Further education of the general public to increase awareness of this disease is the ultimate goal so that children who unknowingly have ocular inflammation can possibly avoid potentially preventable life-long visual impairment. AUTHOR CONTRIBUTIONS Both authors were involved in drafting the article or revising it critically for important intellectual content, and both authors approved the final version to be published. REFERENCES 1. Vadot E, Barth E, Billet P. Epidemiology of uveitis: preliminary results of a prospective study in Savoy. In: Sarri KM, editor. Uveitis update. Amsterdam: Elsevier; p Rothova A, Suttorp-van Schulten MS, Frits Treffers W, Kijlstra A. Causes and frequency of blindness in patients with intraocular inflammatory disease. Br J Ophthalmol 1996;80: Ohm J. 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5 Preventing Blindness From Uveitis in JIA Foster CS, Tufail F, Waheed NK, Chu D, Miserocchi E, Baltatzis S, et al. Efficacy of etanercept in preventing relapse of uveitis controlled by methotrexate. Arch Ophthalmol 2003; 121: Smith JA, Thompson DJ, Whitcup SM, Suhler E, Clarke G, Smith S, et al. A randomized, placebo-controlled, doublemasked clinical trial of etanercept for the treatment of uveitis associated with juvenile idiopathic arthritis. Arthritis Rheum 2005;53: Sen HN, Levy-Clarke G, Faia LJ, Li Z, Yeh S, Barron KS, et al. High-dose daclizumab for the treatment of juvenile idiopathic arthritis-associated active anterior uveitis. Am J Ophthalmol 2009;148: Sainz de la Maza M. Seronegative spondyloarthropathies. In: Foster CS, Vitale AT, editors. Diagnosis and treatment of uveitis. Philadelphia: WB Saunders; p Thorne JE, Woreta F, Kedhar SR, Dunn JP, Jabs DA. Juvenile idiopathic arthritis-associated uveitis: incidence of ocular complications and visual acuity loss. Am J Ophthalmol 2007; 143: Lee FF, Foster CS. Pharmacotherapy of uveitis. Expert Opin Pharmacother 2010;11: Weiss AH, Wallace CA, Sherry DD. Methotrexate for resistant chronic uveitis in children with juvenile rheumatoid arthritis. J Pediatr 1998;133: Samson CM, Waheed N, Baltatzis S, Foster CS. Methotrexate therapy for chronic noninfectious uveitis: analysis of a case series of 160 patients. Ophthalmology 2001;108: Goebel JC, Roesel M, Heinz C, Michels H, Ganser G, Heiligenhaus A. Azathioprine as a treatment option for uveitis in patients with juvenile idiopathic arthritis. Br J Ophthalmol 2011;95: Sobrin L, Christen W, Foster CS. Mycophenolate mofetil after methotrexate failure or intolerance in the treatment of scleritis and uveitis. Ophthalmology 2008;115: Tappeiner C, Roesel M, Heinz C, Michels H, Ganser G, Heiligenhaus A. Limited value of cyclosporine A for the treatment of patients with uveitis associated with juvenile idiopathic arthritis. Eye (Lond) 2009;23: Fledelius HC, Nielsen SM, Nissen KR, Pedersen FK, Zak MS. Anti-TNF treatment of juvenile uveitis. Ugeskr Laeger 2007; 169: In Danish. 38. Vazquez-Cobian LB, Flynn T, Lehman TJ. Adalimumab therapy for childhood uveitis. J Pediatr 2006;149: Heiligenhaus A, Miserocchi E, Heinz C, Gerloni V, Kotaniemi K. Treatment of severe uveitis associated with juvenile idiopathic arthritis with anti-cd20 monoclonal antibody (rituximab). Rheumatology (Oxford) 2011;50: Zulian F, Balzarin M, Falcini F, Martini G, Alessio M, Cimaz R, et al. Abatacept for severe anti tumor necrosis factor refractory juvenile idiopathic arthritis related uveitis. Arthritis Care Res (Hoboken) 2010;62: Foster CS, Gonzalez-Gonzalez LA, Anesi SD, Palafox SK, editors. Childhood uveitis. Manchester Center (VT): Shires Press; 2011.
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