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Show journal of Neuro- Ophthalmology 14( 1): 38- 44, 1994. © 1994 Raven Press, Ltd., New York Incidence of Nonarteritic and Arteritic Anterior Ischemic Optic Neuropathy Population- Based Study in the State of Missouri and Los Angeles County, California Lenworth N. Johnson, M. D., and Anthony C. Arnold, M. D. This population- based study was undertaken to obtain information on age-, sex-, and race- specific incidence of nonarteritic and arteritic anterior ischemic optic neuropathy for the State of Missouri and for Los Angeles County, California. Among subjects who were 50 or older the estimated mean annual incidence rates per 100,000 population were 2.30 for nonarteritic anterior ischemic optic neuropathy and 0.36 for arteritic anterior ischemic optic neuropathy. White individuals appear to be at significantly higher risk of developing nonarteritic anterior ischemic optic neuropathy than black or Hispanic individuals, suggesting possible genetic predisposition. Key Words: Incidence- Ischemic optic neuropathy- Nonarteritic- Population study- Race- Temporal arteritis. From the Neuro- Ophthalmology Division ( L. N. J.), Mason Institute of Ophthalmology, University of Missouri- Columbia, Columbia, Missouri; and UCLA Optic Neuropathy Center ( A. C. A.), Neuro- Ophthalmology Division, Jules Stein Eye Institute, UCLA School of Medicine, Los Angeles, California, U. S. A. This work was aided in part by an unrestricted grant from Research to Prevent Blindness Inc. New York, New York. Address correspondence and reprint requests to Dr. Lenworth N. Johnson, Neuro- Ophthalmology Division, Mason Institute of Ophthalmology, University of Missouri- Columbia, Columbia, MO 65212, U. S. A. Nonarteritic anterior ischemic optic neuropathy-is a common cause of visual loss from optic nerve dysfunction. It is characterized by sudden or rapidly progressive, monocular or binocular visual loss, accompanied initially with segmental or diffuse optic disc edema, and later optic atrophy and retinal arteriolar narrowing ( 1,2). Although nonarteritic anterior ischemic optic neuropathy affects patients of all ages, the median age for nonarteritic anterior ischemic optic neuropathy is approximately 62 years, with fewer than 11% of patients being younger than 45 ( 3- 5). Arteritic anterior ischemic optic neuropathy from temporal arteritis is another important cause of neurogenic visual loss ( 3- 7). In large series, temporal arteritis accounts for approximately 6% to 14% of all cases of anterior ischemic optic neuropathy ( 3- 5). The median age of patients with arteritic anterior ischemic optic neuropathy is approximately 75, and only rarely are patients under 60 years old. Numerous articles have provided excellent clinical perspectives on nonarteritic and arteritic anterior ischemic optic neuropathy, nevertheless, age-, sex-, and race- specific annual incidence of these disorders remains uncertain ( 1- 7). The present population- based study was designed to obtain information on age-, sex-, a nd race- specific incidence of nonarteritic and arteritic anterior ischemic optic neuropathy in the State of Missouri and Los Angeles County, California. SUBJECTS AND METHOD During a 1- year period, between February 1991 and January 1992, a survey card and postage- paid r e t u r n envelope were sent at the end of each month to all ophthalmologists within the State of 38 ISCHEMIC OPTIC NEUROPATHY 39 Missouri. The names and addresses of the ophthalmologists were obtained and updated monthly from the state medical licensing board through the university referral system. A similar survey was performed among ophthalmologists in Los Angeles County, California during a 6- month period from July through December 1991. The ophthalmologists were requested to answer a brief questionnaire on the survey card regarding all patients whom they had evaluated within the past month with new onset of sudden or rapidly progressive loss of vision, accompanied with optic disc edema or optic atrophy. The ophthalmologists were requested to return the cards within 10 days. For the first 5 months of the study, a telephone survey also was conducted in Missouri, by a random sample of 25% of the nonresponders each month, to asses the rate of anterior ischemic optic neuropathy among nonresponding ophthalmologists. A more detailed questionnaire was forwarded to those ophthalmologists who identified patients with optic neuropathy who were 50 or older. The second questionnaire requested additional demographic and clinical information about the patients. One- third of the patients older than 50 were referred for evaluation to the Neuro- Ophthalmology Services of the Mason Institute of Ophthalmology, University of Missouri- Columbia or the UCLA Optic Neuropathy Center, Jules Stein Eye Institute, University of California at Los Angeles. Based on the information provided in the questionnaire, patients were classified as having nonarteritic anterior ischemic optic neuropathy, arteritic anterior ischemic optic neuropathy from temporal arteritis, or other optic neuropathy. Just over 40% of the patients with nonarteritic and arteritic anterior ischemic optic neuropathy underwent neuro- ophthalmologic examination. The diagnosis of nonarteritic and arteritic anterior ischemic optic neuropathy based on the questionnaire was corroborated for all patients who underwent neuro- ophthalmologic examination. Subjects with nonarteritic anterior ischemic optic neuropathy were 50 or older, had acute visual loss with the presence of segmental or diffuse optic disc edema, normal sedimentation rate, absence of multiple sclerosis, and absence of ocular disease accounting for optic nerve changes such as chronic uveitis. Patients with systemic cancer and nonarteritic anterior ischemic optic neuropathy had a normal computed tomographic scan or magnetic resonance image and normal cerebrospinal fluid analysis. Patients with acute visual loss, optic disc edema, and biopsy- proved temporal arteritis were classified as having arteritic anterior ischemic optic neuropathy. Patients who did not undergo temporal artery biopsy, but who had symptoms suggestive of temporal arteritis and elevated sedimentation rate, also were classified as arteritic anterior ischemic optic neuropathy. All other categories of acute visual loss with optic disc edema were classified as other optic neuropathy. The patient's name and social security number were used to screen for duplication of patient information. Although most ophthalmologists remained in practice throughout the survey period, some previously established ophthalmologists left Los Angeles County or Missouri or discontinued their practices, while new physicians entered both regions. Therefore, the number of survey cards distributed each month throughout the study period varied. Information on population demographics for the State of Missouri and Los Angeles County were obtained from the 1990 United States census ( United States Department of Commerce, Bureau of Census Summary tape File # 1- 1990). The population of Missouri was 5,117,073 and for Los Angeles County was 8,863,164. Estimated mean annual incidence rates, odds ratios, and 95% confidence intervals were computed ( 8,9). Significant differences between nonresponders and respond-ers were tested using Fisher's exact test. RESULTS Missouri Data A total of 2,367 survey cards were sent to ophthalmologists during the 12- month study in Missouri. An average of 198 ophthalmologists ( range: 195- 200) were surveyed each month. Of the 2,367 response cards, 86 ( 3.6%) were returned completed without the physician's name; these were classified as nonresponses. There were 1,293 ( 54.6%) nonresponses of the total 2,367 total possible responses. Of the 1,074 written responses, 107 ( 10.0%) identified a case of acute optic neuropathy. Individuals who were 50 or older comprised 46.7% ( 50 cases) of the 107 cases of acute optic neuropathy. The response rate for the second questionnaire sent to 50 physicians who evaluated patients who were 50 or older with acute optic neuropathy was 72% ( 36 physicians). Of the 107 cases of acute optic neuropathy, there were 30 ( 28.0%) nonarteritic anterior ischemic optic neuropathy, 6 ( 5.6%) arteritic anterior ischemic optic neuropathy, and 71 ( 66.4%) other optic neuropathies. Nonarteritic anterior ischemic optic neuropathy comprised the majority ( 60.0%) of optic neuropathy cases older than age 50 years ( Fig. 1). J Neuro- Ophthalmol, Vol. 14, No. 1, 1994 40 L. N. JOHNSON AND A. C. ARNOLD ALL AGES 50 YEARS OR OLDER N- AION A- AION Other ON OPTIC NEUROPATHY N- AION A- AION Other ON OPTIC NEUROPATHY FIG. 1. The distribution of acute optic neuropathy with optic disc edema in the State of Missouri for all ages and for patients 50 or older. The classification includes nonarteritic ( N- AION) and arteritic ( A- AION) anterior ischemic optic neuropathy, and other optic neuropathies ( ON). The proportion of each form of optic neuropathy is indicated in parentheses. Telephone interviews for 130 ( 22.5%) of the 579 nonresponses were conducted during the first 5 consecutive months of the study in Missouri: 3 ( 2.3%) patients with acute optic neuropathy were identified among the 130 telephone surveys, of which only 1 ( 0.8%) had nonarteritic anterior ischemic optic neuropathy. The proportion of nonarteritic anterior ischemic optic neuropathy among nonresponders from the telephone interview did not differ ( P = .24) from the proportion of nonarteritic anterior ischemic optic neuropathy among responders. Los Angeles County Data A total of 2,014 survey cards were sent during the 6- month study in Los Angeles County. An average of 336 ophthalmologists ( range: 334- 338) participated in the study each month. Of the 2,014 response cards, 8 ( 0.4%) were returned completed without the physician's name; these were classified as nonresponses. There were 1,274 ( 63.3%) nonresponses of the 2,014 total possible responses. Of the 740 written responses, 82 ( 11.0%) identified a case of optic neuropathy. Individuals who were 50 or older comprised 53.7% ( 44 cases) of the 82 cases of acute optic neuropathy. The response rate for the second questionnaire sent to 44 physicians who evaluated patients who were 50 or older with acute optic neuropathy was 66% ( 29 physicians). Of the 82 cases of optic neuropathy, there were 23 ( 28.1%) nonarteritic anterior ischemic optic neuropathy, 6 ( 7.3%) arteritic anterior ischemic optic neuropathy, and 53 ( 64.6%) other optic neuropathies. Nonarteritic anterior ischemic optic neuropathy comprised the majority ( 52.3%) of optic neuropathy cases older than 50 ( Fig. 2). Combined Data Of the 53 patients with nonarteritic anterior ischemic optic neuropathy, 16 ( 30.2%) had no history of medical disease prior to the development of nonarteritic anterior ischemic optic neuropathy; 15 patients ( 28.3%) had hypertension; 4 patients ( 7.5%) had prior angina or myocardial infarction; 5 patients ( 9.4%) had previous stroke; and 1 patient ( 1.9%) had diabetes mellitus. Of 21 patients with nonarteritic anterior ischemic optic neuropathy, 16 ( 76.2%), who were able to identify the time of onset when visual loss first was noted, indicated that the loss of vision occurred between 6 a. m. and noon, with most patients being asleep within the 30 minutes interval prior to the onset of visual loss. Based on the Missouri data, there was no seasonal variation for the development of nonarteritic anterior ischemic optic neuropathy, with essentially an even distribution of cases for each month ( Fig. 3). Table 1 provides a summary of the estimated mean annual incidence rates and 95% confidence intervals for nonarteritic and arteritic anterior ischemic optic neuropathy. All incidence rates are based on 100,000 population, and 95% confidence intervals are given in parentheses. The estimated mean annual incidence rates for nonarteritic anterior ischemic optic neuropathy were 0.54 ( 0.42, 0.67) for all ages, 2.30 ( 1.78, 2.82) for subjects who were 50 or older, and 3.25 ( 2.48, 4.02) for subjects older than 60. There was only 1 ( 3.3%) black individual among / Neuro- Ophthalmol, Vol. 14, No. 1, 1994 ISCHEMIC OPTIC NEUROPATHY 41 ALL AGES 50 YEARS OR OLDER C eo N- AION A- AION Other ON OPTIC NEUROPATHY 80 C 60 6- MONTH DATA ( 52.3%) ( 34.1%) N- AION A- AION Other ON OPTIC NEUROPATHY FIG. 2. The distribution of acute optic neuropathy with optic disc edema in Los Angeles County, California for all ages and for patients 50 or older. The classification includes nonarteritic ( N- AION) and arteritic ( A- AION) anterior ischemic optic neuropathy, and other optic neuropathies ( ON). The proportion of each form of optic neuropathy is indicated in parentheses. the 30 nonarteritic anterior ischemic optic neuropathy cases seen in Missouri. Similarly, there was only 1 ( 4.4%) American Indian and 1 ( 4.4%) Hispanic individual among the 23 nonarteritic anterior ischemic optic neuropathy cases seen in Los Angeles County. All other cases of nonarteritic anterior ischemic optic neuropathy occurred among white subjects. The estimated mean annual incidence rates of nonarteritic anterior ischemic optic neuropathy for individuals who were 50 or older were 13.1 ( 0.0, 38.8) for American Indians, 2.77 ( 2.13, 3.41) for whites, 0.32 ( 0.0, 0.96) for blacks, and 0.27 ( 0.0, 0.79) for Hispanics. The estimated mean annual incidence rates of nonarteritic anterior ischemic optic neuropathy for individuals who were 60 or older was 25.8 ( 0.0, 76.4) for American Indians, 3.77 ( 2.86, 4.68) for whites, 0.55 ( 0.0, 1.62) for blacks, and 0.50 ( 0.0, 1.48) for Hispanics. The incidence of nonarteritic anterior ischemic optic neuropathy appears to be significantly higher both for whites as compared with blacks, with odds ratio of 8.5 ( 95% confidence interval: 1.7, 44.1), and similarly for whites as compared with Hispanics, with odds ratio of 10.4 ( 95% confidence interval: 2.1, 50.7). The incidence of nonarteritic anterior ischemic optic neuropathy for whites does not appear to be different from American Indians, with odds ratio of 0.2 ( 95% confidence interval: 0.0, 1.3). The estimated mean annual incidence rates for arteritic anterior ischemic optic neuropathy were 0.09 ( 0.04, 0.13) for all ages, 0.36 ( 0.16, 0.57) for subjects who were 50 or older, and 0.57 ( 0.24, 0.88) for subjects who were 60 or older. Of the 12 cases of arteritic anterior ischemic optic neuropathy in Missouri and Los Angeles County, only 1 person was Hispanic. All other cases of arteritic anterior MISSOURI LOS ANGELES COUNTY c A S 10 E S 1991- 1992 / \ A\ ALL CASES^\ DEFINITE NAION/-~~^^^ \ _ _ ^ FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC JAN 20 IE C A S 1° E S 1991- 1992, DEFINITE NAION FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC JAN MONTH MONTH FIG. 3. The number of cases of acute optic neuropathy with optic disc edema ( all cases) and nonarteritic anterior ischemic optic neuropathy ( NAION) observed each month in the State of Missouri and Los Angeles County, California. The population of Missouri was 5,117,073 and Los Angeles County was 8,863,164. / Ncuro- Ophthalmol, Vol. 14, No. 1, 1994 42 L. N. JOHNSON AND A. C. ARNOLD TABLE 1. Estimated mean annual incidence rates Age 50 and older Age 60 and older Arteritic anterior ischemic optic neuropathy Men Women Whites Hispanics Nonarteritic anterior ischemic optic neuropathy Men Women American Indian Whites Blacks Hispanics 0.36( 0.16,0.57) 0.49( 0.13,0.85) 0.27 ( 0.03, 0.50) 0.61 ( 0.31,0.91) 0.27 ( 0.00, 0.79) 2.30( 1.78,2.82) 2.52( 1.69,3.33) 2.14( 1.48,2.81) 13.10( 0.00,38.77) 2.77( 2.13,3.41) 0.32 ( 0.00, 0.96) 0.27 ( 0.00, 0.79) 0.57 ( 0.24, 0.88) 0.80( 0.21, 1.40) 0.40 ( 0.05, 0.75) 0.91 ( 0.47, 1.36) 0.50( 0.00,1.48) 3.25 ( 2.48, 4.02) 3.55( 2.30,4.81) 3.04 ( 2.07, 4.00) 25.81 ( 0.00, 76.40) 3.77 ( 2.86, 4.68) 0.55( 0.00, 1.62) 0.50( 0.00, 1.48) ischemic optic neuropathy occurred among white subjects. The estimated mean annual incidence rates for arteritic anterior ischemic optic neuropathy were 0.61 ( 0.31, 0.91) for whites and 0.27 ( 0.00, 0.79) for Hispanics among subjects who were 50 or older, and 0.91 ( 0.47, 1.36) for whites and 0.50 ( 0.00, 1.48) for Hispanics among subjects older than 60. There were 16 men ( 53.3%) and 14 women ( 46.7%) with nonarteritic anterior ischemic optic neuropathy in Missouri. In Los Angeles County, there were 10 men ( 43.5%) and 13 women ( 56.5%) with nonarteritic anterior ischemic optic neuropathy. The estimated mean annual incidence rates of nonarteritic anterior ischemic optic neuropathy for subjects who were 50 or older were 2.52 ( 1.69, 3.33) for men and 2.14 ( 1.48, 2.81) for women. The estimated mean annual incidence rates of nonarteritic anterior ischemic optic neuropathy for subjects who were 60 or older were 3.55 ( 2.30, 4.81) for men and 3.04 ( 2.07, 4.00) for women. There were 3 men and 3 women in Missouri and 4 men and 2 women in Los Angeles County with arteritic anterior ischemic optic neuropathy. The estimated mean annual incidence rates of arteritic anterior ischemic optic neuropathy were 0.49 ( 0.13, 0.85) for men and 0.27 ( 0.03, 0.50) for women older than 50, and 0.80 ( 0.21, 1.40) for men and 0.40 ( 0.05, 0.75) for women older than 60. The 95% confidence intervals would indicate that the rate of development of nonarteritic and arteritic anterior ischemic optic neuropathy was not different between men and women. COMMENT The study by Percy and colleagues ( 10) is the only study to our knowledge that provides the incidence rate of acute optic neuropathy in the United States. That study estimated the mean annual incidence of inflammatory optic neuritis- both retrobulbar optic neuritis and papillitis- in Olmstead County, Minnesota to be 6.4 per 100,000 for all ages. Our report is the first to our knowledge providing incidence rates of nonarteritic and arteritic anterior ischemic optic neuropathy. Our study of the State of Missouri and Los Angeles County documented annual incidence rates for all ages of 0.54 for nonarteritic anterior ischemic optic neuropathy and 0.09 for arteritic anterior ischemic optic neuropathy. The annual incidence rates for subjects age 50 or older were 2.30 for nonarteritic anterior ischemic optic neuropathy and 0.36 for arteritic anterior ischemic optic neuropathy. By canvassing neuro- ophthalmologists within the United States, Kelman estimated the annual incidence of nonarteritic anterior ischemic optic neuropathy to be 2.44 per 100,000 population for all ages ( oral communication with Shalom Kelman, M. D., May 21, 1991). The study by Kelman documented a much higher incidence rate of nonarteritic anterior ischemic optic neuropathy than our study, possibly arising from his use of case reports from 20 of approximately 275 neuro- ophthalmologists throughout the United States. Since neuro- ophthalmologists are more likely to evaluate patients with anterior ischemic optic neuropathy, this may falsely overestimate the true incidence of the disease. In contrast, our study design would underestimate the true disease incidence, since we restricted the age of patients with anterior ischemic optic neuropathy to 50 or older; some patients with anterior ischemic optic neuropathy could either be evaluated by nonophthalmologists or choose not to obtain medical evaluation; and our study utilized the United States census data- rather than the number of patients evaluated by all responding physicians- as the denominator when calculating the disease incidence in the population. Our study also has the limitations of most surveys regarding nonresponders. The study had nonresponse rates of 53% for Missouri and 63% for Los Angeles County for the initial survey card. The nonresponse rates for the second questionnaire were 28% for Missouri and 34% for Los Angeles County. However, telephone calls made to 22% of nonresponders over 5 consecutive months in Missouri indicated that less than 1% of nonresponders identified cases of nonarteritic anterior ischemic optic neuropathy. There was no difference between re-sponders and nonresponders in the proportion of nonarteritic anterior ischemic optic neuropathy cases evaluated, with approximately 3% of 1,074 / Neuro- Ophthalmol, Vol. 14, No. 1, 1994 ISCHEMIC OPTIC NEUROPATHY 43 responders identifying cases of nonarteritic anterior ischemic optic neuropathy. By extrapolation, since 1 nonarteritic anterior ischemic optic neuropathy case was identified in the telephone survey of 130 cases, there could be potentially 10 additional nonarteritic arteritic anterior ischemic optic neuropathy cases in the total group of 1,293 non-responders. This would increase the incidence of nonarteritic anterior ischemic optic neuropathy by 33%, resulting in an estimated incidence of 3.06 for individuals older than 50, and 0.72 for all ages. This study relied on the diagnostic accuracy of the respondents. Nevertheless, a recent study has been shown that ophthalmologists are accurate in identifying optic disc edema, and in the clinical setting described, the findings are likely to be correct ( 11). Indeed, the diagnosis of anterior ischemic optic neuropathy from the survey questionnaire was corroborated for all cases in which the neuro-ophthalmologic examination was performed. A study by Rizzo and Lessell ( 1) provided " gold standard"- although not infallible- criteria of nonarteritic anterior ischemic optic neuropathy consisting of absence of ocular pain, presence of optic disc edema, and age over 60. Idiopathic optic neuritis and anterior ischemic optic neuropathy share similar features, thus making it particularly difficult to differentiate these conditions in patients younger than 60. However, since most patients with nonarteritic anterior ischemic optic neuropathy in our study were older than 60, and these individuals had no previous neurologic symptoms compatible with multiple sclerosis, it is unlikely that there was misdiagnosis of optic neuritis for anterior ischemic optic neuropathy. The study indicated that nonarteritic anterior ischemic optic neuropathy is an important cause of blindness among the elderly. Nonarteritic anterior ischemic optic neuropathy appears to be the most common acute optic neuropathy of subjects older than 50, accounting for more than half of all acute optic neuropathies in this age group. Nonarteritic anterior ischemic optic neuropathy has been reported rarely in the black population, with less than 3% of 200 patients with nonarteritic anterior ischemic optic neuropathy being black in a study from Baltimore, Maryland ( 3). Additionally, only sporadic cases of black individuals with arteritic anterior ischemic optic neuropathy have been reported ( 7,12). Our data confirm the rarity of anterior ischemic optic neuropathy among blacks and document similar rarity among Hispanics. The racial discrepancy in the incidence of anterior ischemic optic neuropathy may result from responding physicians evaluating patient populations skewed toward nonblack patients, or that black individuals were underrepresented due to lack of access to ophthalmic care. However, the increased likelihood of nonarteritic anterior ischemic optic neuropathy among whites as compared with blacks ( odds ratio: 8.5; 95% confidence interval: 1.7, 44.1) may reflect a genetic predisposition. Indeed, a recent study has shown that the presence of human leukocyte antigen ( HLA- A29), a genetic marker located on chromosome 6, a potential risk factor for the development of nonarteritic anterior ischemic optic neuropathy ( 13). Also significant racial and ethnic differences have been recognized in optic nerve anatomy such that blacks have both larger optic nerves and increased cup- to- disc ratio ( 14,15). These factors may have protective effects against the development of nonarteritic anterior ischemic optic neuropathy among black individuals. Women are almost three times more likely to be affected by temporal arteritis than men ( 6,7). However, the incidence rates of arteritic anterior ischemic optic neuropathy was not dissimilar between men and women. Likewise, the incidence rates of nonarteritic anterior ischemic optic neuropathy among men and women were almost equal as had been documented in previous studies ( 3,4). All anterior ischemic optic neuropathy cases in this study had unilateral anterior ischemic optic neuropathy. A study by Beri and coworkers ( 4) documented an increased risk of developing bilateral, nonarteritic anterior ischemic optic neuropathy among young diabetic men who had previously experienced unilateral nonarteritic anterior ischemic optic neuropathy. The cause of nonarteritic anterior ischemic optic neuropathy is unknown, but local vascular disorder is suspected ( 16- 21). The study found a preponderance of individuals sustaining visual loss as they slept, with visual loss being discovered in the morning upon awakening. Thus, nonarteritic anterior ischemic optic neuropathy could be characterized as a silent or painless, opportunistic, blinding disease of the elderly. It is opportunistic due to the propensity to strike while the individual is asleep, in essence, the ophthalmologic equivalent of Ondine's curse ( 22). A study of the temporal relationship of acute ischemic strokes also found a significant number of strokes occurring in the early morning ( 23). This early morning time period is associated with increased platelet aggregation, increased hematocrit and blood viscosity, increased tendency for thrombosis, and reduced fibrinolytic activity. Although there are similarities between anterior ischemic optic neuropathy and stroke, / Neuro- Ophthitlmol, Vol. 14, No. 1, 1994 44 L. N. JOHNSON AND A. C. ARNOLD there are racial differences. The risk of developing anterior ischemic optic neuropathy is low in blacks as compared with whites. In contrast, blacks have a higher incidence and mortality rate from strokes than whites ( 2- T- 27). 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