Idiopathic Intracranial Hypertension and Anemia: A Matched Case-Control Study

Background: An association between idiopathic intracranial hypertension (IIH) and anemia has been speculated from previous case reports and case series. Retrospective studies to date have not used matched case controls to compare standardized complete blood count (CBC) values for the presence of anemia. Methods: At our tertiary care facility, 50 patients with IIH were matched with 50 case-control patients to compare CBC values from laboratory affiliates with standardized ranges. Results: No significant difference was found for any CBC parameters for IIH vs control patients. For female IIH and control patients as well as male IIH patients, values for red blood cell count, hemoglobin (HGB), and hematocrit (HCT) tended to trend on the lower end of "normal" range, whereas this was not seen in male control patients. Conclusions: In this retrospective, matched case-control study, no significant association was found between IIH and anemia when comparing standardized CBC values. In accordance with previous studies, the prevalence of anemia may be relatively higher in the IIH population due to a prominent demographic overlap of females of child-bearing age.

Clinical Research: Epidemiology Meets Neuro-Ophthalmology Section Editors: Heather E. Moss, MD, PhD Stacy L. Pineles, MD Idiopathic Intracranial Hypertension and Anemia: A Matched Case-Control Study Weijie Violet Lin, MD, Shauna Berry, DO, Mohammad Obadah Nakawah, MD, Ama Sadaka, MD, Andrew G. Lee, MD Background: An association between idiopathic intracranial hypertension (IIH) and anemia has been speculated from previous case reports and case series. Retrospective studies to date have not used matched case controls to compare standardized complete blood count (CBC) values for the presence of anemia. Methods: At our tertiary care facility, 50 patients with IIH were matched with 50 case-control patients to compare CBC values from laboratory affiliates with standardized ranges. Results: No significant difference was found for any CBC parameters for IIH vs control patients. For female IIH and control patients as well as male IIH patients, values for red blood cell count, hemoglobin (HGB), and hematocrit (HCT) tended to trend on the lower end of "normal" range, whereas this was not seen in male control patients. Conclusions: In this retrospective, matched case-control study, no significant association was found between IIH and anemia when comparing standardized CBC values. In accordance with previous studies, the prevalence of anemia may be relatively higher in the IIH population due to a prominent demographic overlap of females of childbearing age. Journal of Neuro-Ophthalmology 2020;40:163-168 doi: 10.1097/WNO.0000000000000872 © 2019 by North American Neuro-Ophthalmology Society Departments of Medicine, Surgery, and Pediatrics (WVL), Santa Clara Valley Medical Center, Stanford University Hospitals, San Jose, California; Blanton Eye Institute (SB, AS, AGL), Houston Methodist Hospital, Houston, Texas; Houston Methodist Neurological Institute (MON), Houston Methodist Hospital, Houston, Texas; Departments of Ophthalmology (AGL), Neurology, and Neurosurgery, Weill Cornell Medical College, New York, New York; Department of Ophthalmology (AGL), Utah Medical Branch, Galveston, Texas; Department of Ophthalmology (AGL), Utah Maryland Anderson Cancer Center, Houston, Texas; Department of Ophthalmology (AGL), Baylor College of Medicine, Houston, Texas; Department of Ophthalmology (AGL), Center for Space Medicine, Houston, Texas; Department of Ophthalmology (AGL), Texas A&M College of Medicine, College Station, Texas; and Department of Ophthalmology (AGL), University of Iowa Hospitals and Clinics, Iowa City, Iowa The authors report no conflicts of interest. Address correspondence to Andrew G. Lee, MD, Blanton Eye Institute, Houston Methodist Hospital, 6560 Fannin Street, Ste. 450, Houston, TX 77030; E-mail: [e-mail] Lin et al: J Neuro-Ophthalmol 2020; 40: 163-168 I diopathic intracranial hypertension (IIH), also known as pseudotumor cerebri, is a condition of increased intracranial pressure of unknown origin that has a predilection for obese young females. Although the exact pathophysiology remains unknown, several associations have been proposed including obesity (1-5), hormonal disorders (e.g., polycystic ovarian syndrome) (2-4,6), coagulation disorders (3,4,6,7), and the use of certain medications (e.g., tetracycline derivatives (8,9) and retinoids (9-11)). Several case reports have also described a possible association between IIH and anemia (e.g., iron-deficiency anemia (12-14), hemolytic anemia (15), congenital/acquired aplastic anemia (16-19), and sickle cell disease) (20,21). In the IIH Treatment Trial (IIHTT), blood samples were obtained at screening evaluation and 6-month follow-up visits, with the intent to screen for toxic levels of vitamin A metabolites as a possible cause of IIH (22,23). Although acetazolamide was not reported to cause anemia (aplastic anemia) in patients studied in the IIHTT, the possible role of anemia as a cause for IIH was not studied (24). In this retrospective study, we compare 50 patients seen at a single neuro-ophthalmology clinic with IIH and 50 controls (matched for age, sex, and race) to determine whether anemia is associated with IIH. To the best of our knowledge, this is the first and only matched case-control study reporting on the possible association between IIH and anemia, utilizing standardized values from complete blood counts (CBC), in the English language ophthalmic literature. METHODS We retrospectively reviewed the electronic medical records of 95 consecutive patients seen for the primary diagnosis of IIH (ICD-10 code G93.2). All patients were seen in a single neuro-ophthalmology clinic (Blanton Eye Institute at Houston Methodist Hospital [HMH]) between the dates of June 2016 through November 2018. Patients were included only if they met the full modified Dandy criteria 163 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Research: Epidemiology Meets Neuro-Ophthalmology TABLE 1. Characteristics of IIH and control groups IIH Group (N = 50) Mean age (SD) Sex Self-identified race Overweight or obese Average time between initial clinic visit and CBC draw (SD) Anemia diagnosis Primary diagnosis for clinic visit Control Group (N = 50) P 40.8 years (13.3) 88% female 52% Caucasian 26% Black 10% Hispanic 4% Asian 8% Other/NA 25 patients 4.12 months (4.79) 40.8 years (13.3) 88% female 70% Caucasian 12% Black 8% Hispanic 4% Asian 6% Other/NA 17 patients 4.94 months (4.15) 0.569 1.0 0.385 Historical: 8 Current: 1 IIH/pseudotumor cerebri Historical: 6 Current: 0 10 unspecified eye disorders 8 allergic dermatitis/conjunctivitis/blepharitis 6 dry eye 5 refractive error 4 DM with or without ocular involvement 3 glaucoma/glaucoma suspect 2 nystagmus/exophoria 2 floaters 2 migraine 2 uveitis 1 microbial conjunctivitis 1 senile cataract 1 keratoconus 1 chalazion 1 SCH 1 orbital fracture 0.401 0.105 0.292 CBC, complete blood count; DM, diabetes mellitus; IIH, idiopathic intracranial hypertension; SCH, subconjunctival hemorrhage. for IIH and had a CBC taken within 1 year (before or after) of the date of confirmed diagnosis of IIH. For patients with multiple CBCs within this time period, the single time point closest to the initial diagnosis of IIH was selected. Patients were excluded if they did not meet the modified Dandy criteria for IIH or if they did not have a CBC from the HMH laboratory (or affiliate). Patients were also excluded if they had any underlying systemic autoimmune or hematologic neoplastic disorders or were using any medication (other than acetazolamide) that could cause anemia or IIH. All charts were reviewed for sex, age, comorbid conditions, and date of diagnosis. Of the initial 95 cases with confirmed IIH diagnosis, 45 patients were excluded because of lack of CBC from HMH laboratories within 1 year, and 50 cases were included. Another 50 patients were selected as controls from other non-IIH eye clinic patients seen within the same time period (June 2016-November 2018) at the HMH Blanton Eye TABLE 2. Female patients (N = 44): complete blood count values and comparison with the paired t test IIH Group (Mean, SD) Red blood cell count (RBC, 4.2-5.5 m/uL) Hemoglobin (HGB, 12-16 g/dL) Hematocrit (HCT, 37%-47%) Mean corpuscular volume (MCV, 82-100 fL) Mean corpuscular hemoglobin concentration (MCHC, 31-37 g/dL) Platelets (PLT, 150-400 k/ml) 4.36 12.61 38.63 89.07 32.66 (0.58) (1.58) (4.65) (7.39) (1.46) 262 (67.8) Control Group (Mean, SD) 4.36 12.81 38.69 88.78 33.07 P (0.41) (1.46) (3.82) (6.43) (1.01) 0.975 0.535 0.943 0.844 0.178 244 (67.5) 0.220 IIH, idiopathic intracranial hypertension; MCV, mean corpuscular volume. 164 Lin et al: J Neuro-Ophthalmol 2020; 40: 163-168 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Research: Epidemiology Meets Neuro-Ophthalmology TABLE 3. Male patients (N = 6): complete blood count values and comparison with the paired t test IIH Group (Mean, SD) Red blood cell count (RBC, 4.4-6 m/mL) Hemoglobin (HGB, 14-18 g/dL) Hematocrit (HCT, 41%-51%) Mean corpuscular volume (MCV, 82-100 fL) Mean corpuscular hemoglobin concentration (MCHC, 31-37 g/dL) Platelets (PLT, 150-400 k/ml) 4.84 14.65 44.25 91.37 33.12 218.80 (0.41) (1.57) (4.71) (4.01) (1.00) (31.12) Control Group (Mean, SD) 5.05 15.37 45.50 90.83 33.77 256.33 (0.75) (1.48) (4.24) (6.47) (0.70) (86.56) P 0.323 0.280 0.434 0.896 0.165 0.230 MCV, mean corpuscular volume. Institute. These patients were first identified by lack of IIH or intracranial pathology diagnosis. They were matched to the cases, on a 1:1 basis, by sex and age (within 1 month, by birth date). Self-reported race was also matched if corresponding patients could be identified within that sex-age subset. From the remaining list, control patients were randomly selected, and electronic medical records were checked for a CBC within the specified criteria (same as for IIH patients, as detailed). If no corresponding CBC was available, another patient was randomly selected from the matched age-sex (age-gender- race, if available) list. Control patients with diagnoses of hematologic disease other than anemia, systemic lupus erythematosus, intracranial malignancies, or other space-occupying pathologies, were excluded. Previous/active diagnoses of anemia and other diseases were identified through the electronic medical record under historical and active problem lists in the Epic Systems electronic medical record as well as previous diagnoses in the patient history. CBCs were recorded only from the HMH laboratory (or affiliates) because of variances in "normal" ranges when conducted at different laboratories, thus facilitating comparison of values directly. Parameters included red blood cell count (RBC), hemoglobin (HGB), hematocrit (HCT), mean corpuscular volume, mean corpuscular hemoglobin concentration, and platelet count (PLT) as a control. Two-tailed, paired (dependent) t-tests were used to compare the means of our study population with matched controls (25). Statistical significance was defined as a P value of less than 0.05. The authors affirm that this study was approved by the institutional review board at HMH and complies with the standards of the Declaration of Helsinki. RESULTS Fifty patients met inclusion criteria for our study. As is consistent with previously noted demographics of IIH (1,5), our study population includes relatively young patients (average age of 40.8 years) and were mostly women (88%). Additional descriptive data are included in Table 1, comparing demographics of the study group with the control group. A paired t test or x2 test, as appropriate, was used to confirm the lack of significant differences in the characteristics of these 2 groups. Lin et al: J Neuro-Ophthalmol 2020; 40: 163-168 FIG. 1. Complete blood count value distributions. Box and whisker plot of (A) RBC count, (B) hemoglobin (HGB), and (C) hematocrit (HCT) for male and female, control, and IIH patients. For female control and IIH patients, the range is plotted at the lower end of the normal distribution, including below normal range. For male IIH patients, the range also spans at the lower end of normal distributions, but not for male control patients. IIH, idiopathic intracranial hypertension. 165 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Research: Epidemiology Meets Neuro-Ophthalmology TABLE 4. Previous case series and studies Study Type N Conclusion Severe iron deficiency anemia in 5 patients with confirmed PTC In review of literature, 17 patients found to have isolated raised ICP associated with anemia as the most likely diagnosis Among pediatric patients, 43% of PTC cases can be linked to an etiological factor, including infection, CVT, anemia, and drugs A case series of 3 patients with sickle cell disease (1 SC-SC and 2 with SCD-SS) that developed pseudotumor cerebri. All 3 initially presented with headaches. All 3 patients had elevated opening pressures on lumbar puncture with normal CSF studies and imaging. All 3 had papilledema with no signs of retinopathy. All 3 patients responded to medical therapy. A case-control study of 50 patients. Conditions that have been associated with PTC are no more common than in the patient population than the age-matched control population, including iron-deficiency anemia, thyroid disease, pregnancy, antibiotic, and oral conceptive use 8 cases of the 77 newly diagnosed IIH cases had microcytic anemia on examination. 7 cases resolved after the anemia was corrected. They determined the incidence of the association between IIH and anemia to be 10.3%. The authors recommend full blood studies in all patients with IIH. Followed 96 patients with IIH, trending age, ICP, obesity, hypertension, anemia (identified as HGB ,11), and renal failure. Found that puberty is a risk factor for increased ICP. No association remarked for anemia. Biousse (27) Retrospective + meta-analysis 5 + 17 Deg erliyurt (29) Henry et al (21) Retrospective 53 Case series 3 Giuseffi et al (26) Case-control study 50 Mollan (29) Case review 77 StiebelKalish (30) Retrospective study 96 IIH, idiopathic intracranial hypertension. Mean CBC values and comparisons with paired T-tests are displayed in Table 2 for female patients and Table 3 for male patients. Separate analyses were conducted for these 2 groups because of different physiologic ranges of RBC, HGB, and HCT for male vs female patients, which did not allow for direct comparison of raw values. For both sets of patients, no significant difference was found for any CBC values. A small number (9 IIH patients and 6 control patients) of patients were found to have a historical or standing diagnosis of anemia. All were found in female patients. In IIH patients, all cases were iron-deficiency anemia, except 1 case of resolved aplastic anemia. In control patients, all cases were irondeficiency anemia except 2 cases of pernicious anemia. Figure 1 shows the distribution of RBC (A), HGB (B), and HCT (C) (the more typical indicators of anemia) of our patient and control populations, compared with "normal" ranges. Although not a statistically significant difference, the values for female patients and male IIH patients trend toward the lower end of the normal range, whereas for male control patients, the interquartile range fell more precisely within the normal ranges. CONCLUSIONS Although previous anecdotal case reports and a few case series have previously described a possible association with IIH and anemia, no large-scale prospective study of anemia 166 and IIH has been performed to date. In our matched case- control study, we did not find a statistically significant association for CBC values in patients diagnosed with IIH compared with controls. IIH is known to affect predominately younger-aged menstruating females of child-bearing age, who are more prone to be anemic from iron-deficiency anemia and menstruation-related blood loss. Therefore, there may be a noticeable overlap in the patients who have IIH and those who have anemia. In our study, the distribution of RBC, HGB, and HCT values did trend to the lower end of the "normal" distribution for both the female IIH patients and female controls. Interestingly, this trend was seen in the male IIH patients but not for the matched male controls. We believe that younger female patients are more likely to have lower RBC, HGB, and HCT values in general with or without the presence of IIH. The low number (n = 6) of included male patients in our study, however, precludes a meaningful statistical analysis and conclusion to be drawn regarding these findings. One point of note is that although multiple comparisons were made, no statistical correction was warranted because no statistically significant associations were found to reject the null hypothesis, and therefore, no Type I errors were encountered to correct. In evaluating results, the consideration of multiple comparisons can be weighed, but we do not believe this will significantly change our results or conclusions. Lin et al: J Neuro-Ophthalmol 2020; 40: 163-168 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Research: Epidemiology Meets Neuro-Ophthalmology Our study results are consistent with a previous case- control study (N = 50 IIH patients), which also reported a lack of association between IIH and iron deficiency anemia (26). By contrast, this previous study relied on reported diagnoses and prescribed iron supplementation instead of actual CBC values, and matching was not 1:1. Table 4 reviews other case series/studies (excludes isolated case reports) studying IIH and anemia, among other associations. A fraction of our female patients had historical diagnoses of anemia, with a similar number in the female control patients. Some case and control patients had asymptomatic and untreated lower (of normal range) RBC, HGB, and HCT values. It may be that patients who are anemic and also have IIH may have had worse symptoms (e.g., headaches) that were multifactorial, including anemia-related symptoms. In those cases with symptomatic anemia, treating the underlying anemia may lead to an improvement in symptoms but not necessarily intracranial pressure or IIH-related symptoms per se (13,21,27). However, it is important to note that although our study did not note a significant association between IIH and anemia, it does not necessarily mean that anemia may not cause IIH in certain specific cases, especially in cases with particularly severe anemia with HGB values less than 8-10 g/dL, such as reported in the studies conducted by Biousse et al and Mollan et al. (27,28) In our cases, only 2 female IIH cases had HGB of ,10 g/dL. However, the nature of these mechanisms has not been elucidated thus far in the literature. In conclusion, our study represents the first and only such retrospective, matched case-control study of IIH and CBCs from a standardized laboratory. We found no statistically significant difference in CBC values on 2-tailed, paired t-tests, although RBC, HGB, and HCT values tended to be lower in both IIH patients and female control patients. We recognize the limitations of our study including the retrospective design, ascertainment and selection bias in our tertiary care population, and sample size. Future prospective studies might be helpful to confirm our findings. Our work suggests that routine CBC may not be necessary in typical patients with IIH. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: W. V. Lin, S. Berry, M. O. Nakawah, A. Sadaka, and A. G. Lee; b. Acquisition of data: W. V. Lin and S. Berry; c. Analysis and interpretation of data: W. V. Lin, S. Berry, M. O. Nakawah, A. Sadaka, and A. G. Lee; Category 2: a. Drafting the manuscript: W. V. Lin, S. Berry, and A. G. Lee; b. Revising it for intellectual content: W. V. Lin, S. Berry, M. O. Nakawah, A. Sadaka, and A. G. Lee; Category 3: a. Final approval of the completed manuscript: W. V. Lin, S. Berry, M. O. Nakawah, A. Sadaka, and A. G. Lee. Acknowledgments The authors acknowledge the statistical consulting assistance of Genevara Allen, PhD. 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