Comparison of Idiopathic Intracranial Hypertension Patients With and Without Anemia

Background: Idiopathic intracranial hypertension (IIH) is a condition of elevated intracranial pressure without an identifiable cause. It mostly affects young obese women but has been reported in individuals newly diagnosed with anemia or with chronic anemia. The relationship between anemia and IIH is not well elucidated. This study aims to characterize the course of IIH in anemic patients. Methods: Consecutive patients with IIH were recruited from neuro-ophthalmology clinics. Subsequent retrospective chart review obtained information on symptoms, complete blood counts (CBCs), visual acuity, visual fields, and optic disc edema at baseline and follow-up. Anemia was diagnosed by hemoglobin <120 g/L (women) and <130 g/L (men). Results: One hundred twenty-three patients with IIH were recruited for this study, and 22.8% (28/123) had anemia. More anemic individuals had mild-to-moderate visual acuity impairment (logarithm of minimum angle of resolution 0.3-1, P = 0.01) and worse automated mean deviation ( P = 0.048). The median follow-up time was 47.4 weeks (interquartile range:20.1-91.8). Fifteen of 28 patients with anemia received anemia treatment and showed a trend toward increased hemoglobin. At follow-up, there were no differences in the visual acuity, but patients with anemia had worse automated mean deviation on visual fields ( P = 0.045). Conclusions: IIH patients with anemia had worse visual function at presentation and worse final visual field parameters. This suggests that CBCs should be obtained for patients with papilledema because it may influence final visual outcome.

Original Contribution Section Editors: Clare Fraser, MD Susan Mollan, MD Comparison of Idiopathic Intracranial Hypertension Patients With and Without Anemia Irina Sverdlichenko, BHSc, Caberry W. Yu, MD, Edward Margolin, MD, Jonathan A. Micieli, MD Background: Idiopathic intracranial hypertension (IIH) is a condition of elevated intracranial pressure without an identifiable cause. It mostly affects young obese women but has been reported in individuals newly diagnosed with anemia or with chronic anemia. The relationship between anemia and IIH is not well elucidated. This study aims to characterize the course of IIH in anemic patients. Methods: Consecutive patients with IIH were recruited from neuro-ophthalmology clinics. Subsequent retrospective chart review obtained information on symptoms, complete blood counts (CBCs), visual acuity, visual fields, and optic disc edema at baseline and follow-up. Anemia was diagnosed by hemoglobin ,120 g/L (women) and ,130 g/L (men). Results: One hundred twenty-three patients with IIH were recruited for this study, and 22.8% (28/123) had anemia. More anemic individuals had mild-to-moderate visual acuity impairment (logarithm of minimum angle of resolution 0.3– 1, P = 0.01) and worse automated mean deviation (P = 0.048). The median follow-up time was 47.4 weeks (interquartile range:20.1–91.8). Fifteen of 28 patients with anemia received anemia treatment and showed a trend toward increased hemoglobin. At follow-up, there were no differences in the visual acuity, but patients with anemia had worse automated mean deviation on visual fields (P = 0.045). Faculty of Medicine (IS), University of Toronto, Toronto, Canada; Division of Ophthalmology (CWY), Department of Surgery, McMaster University, Hamilton, Canada; Department of Ophthalmology and Vision Sciences (EM, JAM), University of Toronto, Toronto, Canada; and Kensington Vision and Research Centre (JAM), Toronto, Canada. The authors report no conflicts of interest. Statement of Ethics: Patient consent was obtained to publish the data included in this manuscript. All medical interventions have been performed according to the latest protocols of therapy. This study complies with the guidelines for human studies and was conducted ethically in accordance with the World Health Organization Declaration of Helsinki. This study protocol was reviewed and received approval by the University of Toronto Research Ethics Board Protocol #39135. Data Availability: The data sets generated during and/or analyzed during this study are not available. Address correspondence to Jonathan A. Micieli, MD, Kensington Vision and Research Centre, 340 College Street, Suite 501, Toronto, ON, Canada, M5T 3A9; E-mail: [e-mail] Sverdlichenko et al: J Neuro-Ophthalmol 2023; 43: 535-540 Conclusions: IIH patients with anemia had worse visual function at presentation and worse final visual field parameters. This suggests that CBCs should be obtained for patients with papilledema because it may influence final visual outcome. Journal of Neuro-Ophthalmology 2023;43:535–540 doi: 10.1097/WNO.0000000000001715 © 2022 by North American Neuro-Ophthalmology Society I diopathic intracranial hypertension (IIH) is a disease in which patients experience elevated intracranial pressure (ICP) that cannot be attributed to an identifiable cause (1). It most often affects obese women of childbearing age, with an estimated annual worldwide incidence of 12–20 per 100,000 in this population (1). Patients with IIH may experience headaches and pulsatile tinnitus, and the most feared complication is permanent vision loss due to papilledema (1). IIH management entails reducing ICP and preserving visual function while relieving symptoms, with weight loss as the mainstay of treatment (1). Additional treatment options include medical therapy such as acetazolamide and surgical treatments such as optic nerve sheath fenestration or cerebrospinal fluid (CSF) shunting for more severe cases to prevent irreversible vision loss (1). In addition to weight, anemia has been documented as a risk factor for IIH development (2). Although this is often seen with iron-deficiency anemia (3), other types of anemia have been described, such as hemolytic anemia (4) and sickle cell disease (5). Case series have reported patients presenting with symptoms of IIH who were not obese and had no recent weight gain (6). For example, 4 of 8 patients described by Mollan et al (7) were not obese but presented with iron-deficiency anemia and papilledema. Similarly, Waisberg et al (2) documented 5 cases of fulminant IIH and severe iron-deficiency anemia, with 2 patients who were nonobese and had no recent weight gain. Larger prevalence studies have also reported an association between anemia and IIH (8,9). 535 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Despite this evidence, there is uncertainty regarding the relationship between anemia and IIH. For example, a case series by Stiebel-Kalish found that anemia was not a significant predictor of visual outcomes in adolescents with IIH (10). In addition, some case controls have failed to find an association between anemia and IIH (11). Finally, there is limited information regarding the influence of anemia on the course of IIH disease, with most data coming from case reports, and only one study having investigated this topic on a large scale (12). Therefore, the goal of this study was to characterize the differences in initial presentation and visual outcome among IIH patients with and without anemia. METHODS Participants This was a retrospective chart review of all consecutive patients with IIH who presented at tertiary neuroophthalmology clinics associated with the University of Toronto between July 2018 and February 2021. Inclusion criteria were consecutive patients meeting 2013 revised criteria derived from the modified Dandy criteria for IIH diagnosis (1). The criteria include having papilledema, normal neurological examination except cranial nerve abnormalities, normal neuroimaging, normal CSF composition, and elevated lumbar puncture opening pressure $25.0 cm of water. Included patients with IIH had complete blood counts (CBCs) collected within 6 months of initial presentation. Demographic information, including age, sex, and body mass index (BMI), based on self-reported weight were recorded. Complete Blood Count Consecutive patients with IIH were assessed for CBC, including hemoglobin, mean corpuscular volume (MCV), platelets, and leukocytes. In addition, hemoglobin values obtained within 3 months of final follow-up were recorded. Anemia was diagnosed based on the World Health Organization criteria (hemoglobin ,120g/L for women and ,130g/L for men) and classified as mild (hemoglobin .110g/L), moderate (hemoglobin 80–109g/L), and severe (hemoglobin ,80g/L) (13). Anemia was also stratified as microcytic (MCV , 80 fL), normocytic (MCV 80–100 fL), and macrocytic (MCV . 100 fL) (14). Symptoms and Visual Function Patients with IIH were assessed on initial and final presentation for symptoms, visual measures, and physical examination findings. Symptoms of interest included headaches, transient visual obscurations (TVO), pulsatile tinnitus, and diplopia. The best-corrected visual acuity (BCVA) was measured using the Snellen chart and was converted to logarithm of minimum angle of resolution (logMAR) and stratified into normal vision (logMAR 536 #0.3), mild to moderate visual impairment (logMAR 0.3–1), and severe impairment/blindness (logMAR $1) (15). Visual field findings were quantified using the automated 24-2 SITA-Fast Mean Deviation (MD). Finally, physical examination included optic disc edema, which was quantified by optical coherence tomography retinal nerve fiber layer (OCT-RNFL) average thickness. The average visual acuity, automated MD, and OCT-RNFL of both eyes were used for analysis. Follow-Up and Treatment of Idiopathic Intracranial Hypertension The median time between initial and final presentation was recorded. Patient management including medical therapy, surgical interventions, and weight loss was recorded. For patients with IIH presenting with anemia, treatment of anemia was assessed. Statistical Analysis Statistical analysis was performed using IBM SPSS. Means and SD were reported for continuous data and percentages of the total sample for categorical data. Linear regression analysis was performed between continuous variables. Twotailed P values were considered statistically significant if , 0.05. RESULTS Patients With Idiopathic Intracranial Hypertension Anemia vs Nonanemia: Initial Presentation A total of 123 patients with IIH were included in this study, 95 without anemia and 28 with anemia. The distribution of hemoglobin levels are shown in Figure 1. For those with anemia, the anemia was considered mild in 16 (57.1%) patients, moderate in 7 (25.0%) patients, and severe in 5 (17.9%) patients. The anemia was microcytic in 13 (46.4%) patients, normocytic in 14 (50.0%) patients, and macrocytic in 1 (3.6%) patient. There were no differences between patients with IIH anemia and nonanemia in female sex (92.9%, 26/28 vs 94.7%, 90/95, P = 0.71) and age at presentation (32.0 years, SD:10.4 vs 31.2 years, SD: 9.5, P = 0.71). There was also no difference in BMI distribution (P = 0.78). Over half of the participants had BMI $30.0 kg/m2 (anemia 73.1%, 19/26 vs nonanemia 75.3%, 70/ 93); less than 20 percent had BMI 25.0–29.9 kg/m2 (anemia 19.2%, 5/26 vs nonanemia 20.4%, 19/93); the smallest proportion of patients had BMI #24.9 kg/m2 (anemia 7.7%, 2/26 vs nonanemia 4.3%, 4/93). Compared with patients with nonanemia, patients with anemia had significantly lower mean hemoglobin (103.5g/L, SD: 18.3 vs 134.6g/L, SD: 10.2, P , 0.001) and MCV (80.8 fL, SD: 8.1 vs 86.2 fL, SD: 4.9, P = 0.002) (Table 1). However, Sverdlichenko et al: J Neuro-Ophthalmol 2023; 43: 535-540 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. Distribution of hemoglobin at presentation in patients with idiopathic intracranial hypertension. there were no differences between patients with anemia and nonanemia in mean platelet count or leukocytes. Patients with anemia and nonanemia IIH were evaluated for differences in their initial symptom presentation, physical examination findings, and visual findings (Table 1). With respect to initial symptoms, there were no differences between patients with anemia and nonanemia. The most common symptoms at presentation in anemia and nonanemia groups were headaches (75.0% and 77.9%), followed by pulsatile tinnitus (39.2% and 51.6%), TVO (25.0% and 28.4%), and diplopia (10.7% and 8.4%). Patients with anemia were more likely to have mild-tomoderate visual acuity impairment compared with patients with nonanemia (14.3%, 8/56 eyes vs 3.7%, 7/190 eyes, P = 0.01). Patients with anemia also had worse visual field defects, as measured by mean deviation on automated perimetry, compared with patients with nonanemia (mean: 25.7, SD: 8.1 vs mean: 23.4, SD: 4.2, P = 0.048). There were no differences in mean opening pressure on lumbar puncture or average OCT-RNFL thickness between groups. TABLE 1. Initial presentation of symptoms, physical examination, and visual findings of IIH patients with and without anemia % (Total) Mean (SD) Category, Measure CBC findings Platelets (x109/L) Leukocytes (x109/L) Hemoglobin (g/L) MCV (fL) Symptoms Headache TVO Pulsatile tinnitus Diplopia Visual acuity logMAR #0.3 logMAR 0.3–1 logMAR $1 Automated MD OCT RNFL (mm) Anemia N = 28 Nonanemia N = 95 P 305.2 (68.6) 7.7 (2.0) 103.5 (18.3) 80.8 (8.1) 294.0 (60.9) 8.2 (2.3) 134.6 (10.2) 86.2 (4.9) 0.44 0.26 ,0.001 0.002 75.0% (21) 25.0% (7) 39.2% (11) 10.7% (3) N = 56 eyes 83.9% (47) 14.3% (8) 1.8% (1) 25.7 (8.1) 211.0 (114.0) 77.9% (74) 28.4% (27) 51.6% (49) 8.4% (8) N = 190 eyes 95.3% (181) 3.7% (7) 1.0% (2) 23.4 (4.2) 188.4 (102.2) 0.75 0.72 0.25 0.71 0.01 0.048 0.19 CBC, complete blood count; Automated MD, automated 24-2 SITA-Fast Mean Deviation; IIH, idiopathic intracranial hypertension; MCV, mean corpuscular volume; OCT RFNL, optical coherence tomography retinal nerve fiber layer; TVO, transient visual obscurations; logMAR, logarithm of minimum angle of resolution. Sverdlichenko et al: J Neuro-Ophthalmol 2023; 43: 535-540 537 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Subgroup analysis was performed based on severity of anemia to evaluate differences in initial symptom presentation and visual findings. Patients with mild anemia were compared with those with moderate-to-severe anemia, and no differences were found on prevalence of headaches (mild 75.0%, 12/16 vs moderate-to-severe 75.0%, 9/12, P = 1.0), pulsatile tinnitus (mild 43.8%, 7/16 vs moderate-tosevere 33.3%, 4/12, P = 0.58), TVO (mild 37.5%, 6/16 vs moderate-to-severe 8.3%, 1/12, P = 0.078), or diplopia (mild 12.5%, 2/16 vs moderate-to-severe 8.3%, 1/12, P = 0.72). Furthermore, there were no differences on BCVA (mean logMAR mild 0.12, SD: 0.36 vs moderate-tosevere 0.16, SD: 0.19, P = 0.60), OCT RNFL average thickness (mild 206.2, SD: 100.8 mm vs moderate-tosevere 217.3, SD: 131.6 mm, P = 0.73), or automated MD (mild 27.0, SD: 10.2 vs moderate-to-severe 23.9, SD: 3.4, P = 0.11). Multivariate linear regression controlling for age, sex, and BMI demonstrated that the presence of anemia was a significant predictor of automated MD at presentation (Adjusted R square 0.124, P = 0.002). Patients With Idiopathic Intracranial Hypertension Anemia vs Nonanemia: Follow-Up The median follow-up time for all patients with IIH was 47.4 weeks (interquartile range: 20.1–91.8). Over half of the participants received treatment with acetazolamide (anemia 66.7%, 14/21 vs nonanemia 54.2%, 45/83, P = 0.29), and less than 10 percent underwent surgical treatment (anemia 9.5%, 2/21 vs nonanemia 6.0%, 5/83, P = 0.57). Patients with anemia reported less weight loss at followup than patients with nonanemia (anemia 23.8%, 5/21 vs nonanemia 49.4%, 41/83, P = 0.03). For patients with anemia, 53.6% (15/28) were treated for their anemia with iron or red blood cell transfusion. Eleven patients with anemia had hemoglobin results at follow-up. Subgroup analysis for these patients showed an increase in hemoglobin approaching significance (initial: 100.3g/L, SD:19.2 vs follow-up:115.4g/L, SD: 16.2, P = 0.06). Symptoms, physical examination, and visual findings were evaluated at follow-up for patients with IIH (Table 2). There were no differences between patients with anemia and nonanemia in symptoms such as headaches, pulsatile tinnitus, or TVO. Patients with anemia were more likely to endorse diplopia at follow-up compared with patients with nonanemia (19.0%, 4/21 vs 4.9% 4/82, P = 0.03). Both groups showed improvement in their optic disc edema, with more participants showing resolution in their edema. There were no significant differences on physical examination findings between groups. For visual findings, patients with anemia improved in their visual acuity from initial presentation, and differences were no longer significant (P = 0.10); over 90% of patients had normal vision (anemia 95.2%, 40/42 eyes vs nonanemia, 94.5%, 155/ 164 eyes). However, automated MD continued to be worse in patients with anemia (anemia 25.6, SD:6.4 vs nonanemia 23.2, SD:5.7, P = 0.045). There were still no differences in OCT-RNFL average thickness. Subgroup analysis was conducted to compare outcomes of anemic patients who received ICP-lowering therapy only vs those who received medical therapy and anemia treatment. The results showed no differences between groups on final BCVA (mean logMAR medication only 0.05, SD: 0.07 vs dual therapy 0.2, SD: 0.4, P = 0.10), OCT RNFL average thickness (medication only 105.7, SD: 30.9 mm vs dual therapy 105.7, SD: 29.2 mm, P = 1.0), and automated MD (medication only 28.6, SD: 7.6 vs dual therapy 27.1, SD: 6.7, P = 0.6). Finally, multivariate TABLE 2. Final presentation of symptoms, physical examination, and visual findings of IIH patients with and without anemia % (Total) Mean (SD) Category, Measure Symptoms Headache TVO Pulsatile tinnitus Diplopia Visual acuity logMAR #0.3 logMAR 0.3–1 logMAR $1 LP opening pressure (cmH2O) Automated MD OCT RNFL (mm) Anemia N = 21 Nonanemia N = 82 61.9% (13) 14.3% (3) 38.1% (8) 19.0% (4) N = 42 eyes 95.2% (40) 2.4% (1) 2.4% (1) 39.9 (11.3) 25.6 (6.4) 118.0 (41.0) 47.6% (39) 12.2% (10) 30.5% (25) 4.9% (4) N = 164 eyes 94.5% (155) 5.5% (9) 0 36.6 (9.0) 23.20 (5.7) 121.8 (54.9) P 0.24 0.78 0.50 0.03 0.10 0.30 0.045 0.62 Automated MD, automated 24-2 SITA-Fast Mean Deviation; IIH, idiopathic intracranial hypertension; LP, lumbar puncture; OCT RFNL, optical coherence tomography retinal nerve fiber layer; TVO, transient visual obscurations; logMAR, logarithm of minimum angle of resolution. 538 Sverdlichenko et al: J Neuro-Ophthalmol 2023; 43: 535-540 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution linear regression modeling controlling for age, sex, and BMI demonstrated that anemia was a significant predictor of mean deviation at the final follow-up (adjusted R square 0.089, P = 0.017). CONCLUSIONS The relationship between anemia and IIH has previously been recognized in the literature. However, data on the course of disease in anemic patients with IIH relied mostly on case reports. Our study demonstrates that IIH patients with anemia have similar symptoms and physical examination findings at presentation. However, patients with anemia have worse visual acuity and visual field findings compared with patients with nonanemia. After ICPlowering therapy and/or anemia treatment, patients with anemia showed comparable improvement in symptoms, except diplopia, relative to patients with nonanemia. They also improved in visual acuity but continued to have worse visual field mean deviation than patients with nonanemia at the final follow-up. Given the potential causal relationship of anemia and IIH and differences in visual outcomes, CBCs should be ordered in patients with papilledema. The results of our retrospective analysis are consistent with previous case series in that there were worse visual findings in IIH patients with anemia compared with those without anemia (2,6,7). However, on conducting subgroup analysis, no differences were seen on initial symptoms and visual findings of patients with mild vs moderate-to-severe anemia. After initial presentation, most patients with anemia were treated with acetazolamide and at least half were treated for anemia, showing a trend toward increased hemoglobin and improvement of symptoms, physical examination, and visual findings. However, when conducting subgroup analysis of patients treated with acetazolamide only vs those treated for their ICP and anemia, no differences were found on final visual outcomes. The lack of statistical differences seen on subgroup analyses may be due to the low number of patients with anemia in our study sample, making it difficult to discern statistical significance. One retrospective observational study by Ma et al (12) compared the initial presentation and follow-up of IIH patients with and without anemia. Similar to our study, there were no differences in initial symptoms such as vision loss, TVO, and diplopia. By contrast, they found that patients with anemia had a higher prevalence of pulsatile tinnitus. The patients with anemia also showed worse visual acuity, having a higher prevalence of moderate vision impairment at baseline than patients with nonanemia, which improved at follow-up. The study by Ma et al also found worse visual field defects in patients with anemia. However, in contrast to our results, their visual field findings improved such that there were no differences between groups at follow-up. It is important to note that patients with IIH in our study differed with respect to participant Sverdlichenko et al: J Neuro-Ophthalmol 2023; 43: 535-540 weight, as over 70% of our patients were obese. Furthermore, patients with anemia in this study had less weight loss at follow-up than patients with nonanemia. Because weight loss is the mainstay of treatment in IIH, the comparatively lower weight loss of patients with anemia may be a potential reason why they continued to show worse visual field mean deviation. Correcting anemia has been shown to induce weight loss, and because we did not have final hemoglobin levels for all patients, it is possible that some individuals did not have increased final hemoglobin, which could have influenced their weight loss (16). Only one-third of participants in Ma et al had BMI $28.0 kg/m2. Patients with IIH with higher BMIs tend to have worse visual outcomes, including visual field defects; thus, the high initial BMI and minimal weight loss in our patients may account for differences in final visual fields identified between the 2 studies (17). The exact mechanism of how anemia relates to IIH is unclear, but several theories have been posited. One theory is that iron-deficiency anemia (IDA) creates a hypercoagulable state, having been associated with venous and arterial thrombosis (18); this may cause abnormal blood flow in the blood vessels because of reduced deformability and increased viscosity of microcytic red blood cells. In addition, it may cause reactive thrombocytosis by lack of inhibition of thrombopoiesis (19). Accordingly, one study looking at the clinical records of 615 consecutive adults with IDA reported a prevalence of thrombocytosis of 13.3% (20). These processes may lead to increased venous pressure which decreases the rate of CSF resorption, thus causing a rise in ICP (18). Other potential theories include cerebral vasodilation occurring in response to cerebral hypoxia because of acute anemia episodes, contributing to raised ICP (6). Our study has several strengths. We recruited patients from multiple different centers across Toronto, Canada, thus increasing the generalizability of our findings. Our study was also able to elucidate the influence of anemia on the presentation and course of IIH disease by investigating various clinical parameters. Nonetheless, our study has certain limitations. We did not have access to the charts of family physicians or hematologists and were therefore limited in our ability to specify the type of anemia or treatment regimen. Our classification relied mainly on the MCV. Finally, because our inclusion criteria for patients with IIH were the collection of CBC within 6 months of initial presentation, it is difficult to comment on their anemia status at the time of diagnosis, only that they occurred close together temporally. The literature has documented a potential relationship between anemia and IIH. However, this study elucidated this further by showing that while patients with IIH and anemia have worse visual findings at initial presentation, with appropriate ICP-lowering therapy, surgery and/or anemia treatment, anemic patients with IIH have 539 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution improvement in their clinical findings and visual acuity comparable with that of patients with nonanemia. Automated MD continued to be worse in IIH patients with anemia at the final follow-up. 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Sverdlichenko et al: J Neuro-Ophthalmol 2023; 43: 535-540 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.