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Clinical science
Prevalence and risk factors of epiretinal membrane in a cohort with cardiovascular disease risk, compared with the Blue Mountains Eye Study
  1. Sarah B Wang1,
  2. Paul Mitchell1,
  3. Adam JH Plant1,
  4. Kevin Phan2,
  5. Gerald Liew1,
  6. Joseph Chiha2,
  7. Aravinda Thiagalingam2,
  8. George Burlutsky1,
  9. Bamini Gopinath1
  1. 1Centre for Vision Research, Department of Ophthalmology and, Westmead Millennium Institute, University of Sydney, Sydney, New South Wales, Australia
  2. 2Centre for Heart Research, Westmead Millennium Institute, University of Sydney, Sydney, New South Wales, Australia
  1. Correspondence to Dr Bamini Gopinath, Department of Ophthalmology, Centre for Vision Research, University of Sydney, Westmead Millennium Institute Westmead Hospital, Hawkesbury Rd, Westmead, Sydney, NSW 2145, Australia; bamini.gopinath{at}sydney.edu.au

Abstract

Aims To describe the prevalence of idiopathic and secondary epiretinal membranes (ERM) in a clinical cohort (Australian Heart Eye Study, AHES) and compare to the Blue Mountains Eye Study, and to determine whether associations exist between idiopathic ERM and the extent and severity of coronary artery disease (CAD).

Methods The AHES is an observational study that surveyed 1680 participants who presented to a tertiary referral hospital for the evaluation of potential CAD by coronary angiography. Severity and extent of CAD was assessed using three scoring systems: (1) segment/vessel scores, (2) Gensini and (3) extent scores. Two types of ERM were identified: a more severe form, termed ‘preretinal macular fibrosis’ (PMF) in which retinal folds were identified; and a less severe form termed ‘cellophane macular reflex’ (CMR), without visible retinal folds.

Results Overall prevalence of ERM was 7.0% (n=115), with CMR and PMF each 3.5%. 72.7% of ERM cases were idiopathic (no secondary cause identified). Prevalence of PMF, but not CMR, was significantly higher than the corresponding age-standardised prevalence in the baseline Blue Mountains Eye Study (p<0.001). There was no significant association between extent and severity of CAD and idiopathic ERM.

Conclusions This study suggests that cardiovascular disease (specifically severity and extent of CAD) is not associated with ERM. However, there may be a greater prevalence of severe ERM (PMF) in a high cardiovascular risk cohort relative to a population-based cohort.

  • Retina

https://doi.org/10.1136/bjophthalmol-2015-306776

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    Introduction

    The formation of epiretinal membranes (ERM) as proliferations at the vitreoretinal junction occur commonly with age,1 ,2 especially with posterior vitreous detachment.3 Despite the fact that in most cases, ERM does not cause serious impairment of vision, diagnosis of such lesions is important because definitive surgical treatment has been developed and may be necessary for more severe cases.3

    ERMs may be classified into an early asymptomatic form, termed cellophane macular reflex (CMR), and a more severe form in which retinal folds may be visualised, termed preretinal macular fibrosis (PMF).4 ERMs may also be classified into an idiopathic and a secondary form. Most ERMs are idiopathic, meaning they occur in the absence of ocular comorbidities other than posterior vitreous detachment.5 Secondary ERMs are those cases that occur after accounting for age and ocular pathologies known to be associated with ERM, including retinal detachment, retinal vascular occlusion, macular hole, refractive error and following cataract surgery.1 ,2 ,6–8

    Previous studies have attempted to account for idiopathic ERM by searching for its possible associations with other potential systemic risk factors. These factors include diabetes,2 hypercholesterolaemia2 and history of smoking (which may be protective).8 However, these associations have been inconsistent across different studies, with several failing to find an association between these risk factors and ERM.6 ,9–11 There is, therefore, a need to investigate other possible associations between pertinent systemic diseases and idiopathic ERM.

    Consequently, the aims of this study were to: (1) describe the prevalence of idiopathic and secondary ERM (PMF, CMR and any ERM) in a unique clinical cohort of patients with high cardiovascular risk presenting for coronary angiography (the Australian Heart Eye Study, AHES) and to test for differences in prevalence by age and sex, (2) compare the age-standardised prevalence of idiopathic ERM in the AHES with baseline prevalence from the Blue Mountains Eye Study (BMES-1) and (3) determine whether associations exist between the extent and severity of coronary artery disease (CAD) and the prevalence of idiopathic ERM (PMF, CMR and any ERM).

    This study is the first to investigate whether associations exist between cardiovascular disease, as quantified by coronary angiography, and idiopathic ERM.

    Methods

    Study population and data collection

    The AHES is a clinical cohort study of 1680 participants who presented to a major tertiary referral hospital servicing the greater western Sydney area (Westmead Hospital, Sydney, Australia) between June 2009 and January 2012 to evaluate potential CAD by coronary angiography.

    All eligible patients presenting for assessment of suspected CAD were included in this study. Exclusion criteria: patients with a history of coronary artery bypass graft or coronary artery stent. These patients were excluded because the Gensini and extent scoring systems used have not been validated in this group. Participants were also excluded if they had incomplete information on ERM signs or absent Gensini or extent scores.

    Assessment of ERM

    All participants had digital retinal photographs taken after pharmacological mydriasis. Seven standard early treatment diabetic retinopathy study 45° fields were taken on a digital camera (Canon CR-DGI, Tokyo, Japan). All photographs were graded in a masked manner.

    The classification and grading system for ERM was the same as in the BMES-1,12 adopted from Klein et al.13 Two types of ERM were identified: a more severe form, termed PMF, in which superficial retinal folds and traction lines were identified and a less severe form, termed CMR, without visible retinal folds. Eyes with both CMR and PMF present were classified as having PMF.

    All cases were classified into idiopathic and secondary ERM in the same manner as the BMES-1, as described previously.12

    Assessment of CAD

    Routine diagnostic coronary angiography was performed after 6 h fasting via either the femoral or radial artery using a catheter of known dimension (5–7 Fr). Selective coronary injections of Ultravist (Schering) were filmed in standard projections on a Siemens biplane radiographic unit (Siemens Healthcare, Germany).

    All angiograms were analysed offline by a trained cardiologist masked to the results of the adjunctive investigations and retinal grading. The coronary artery segments were defined using the Syntax system, which divides the arterial tree into 16 segments based on the modified American Heart Association classification.14 For each segment, the severity of obstruction was documented using several grades: normal, 1%–25%, 25%–50%, 50%–74%, 75%–99% and 100% (occluded). Each lesion that was visually scored as greater than 50% luminal obstruction in a vessel that was ≥1.5 mm diameter was further analysed using quantitative coronary analysis (QCA). QCA was performed using validated computerised edge-detection software (QCAPlus, Sanders Data Systems, Palo Alto, California, USA).

    Coronary angiograms were scored according to three methods to document both the severity and extent of CAD:

    1. Vessel and segment score (severity score): vessel scores were calculated based on the number of vessels with significant obstructive coronary disease. The American College of Cardiology taskforce definition from 2011 uses 50% stenosis to define significant vessel disease.15 This definition was used for the left main coronary, right coronary, left anterior descending and left circumflex arteries. Scores ranged from 0 to 4, depending on the vessels with greater than 50% stenosis.16 Left main artery stenosis was scored as double vessel disease, as per the coronary artery surgery study scoring system.17 The segment score was reported based on the number of obstructive lesions present in the 16 segments.

    2. Gensini score (severity score): this has been described previously.18 Briefly, the coronary arterial tree was divided into segments with multiplying factors according to the functional importance of any given segment (5 for the left main trunk to 0.5 for the most distal segments) and the percentage reduction in luminal diameter of each narrowing was assigned a score (0, 1, 2, 4, 8, 16 or 32), according to the degree of stenosis. The sum of the scores of all segments gives the Gensini score, which places emphasis on the severity of the disease.16

    3. Extent score: the extent score was proposed by Sullivan et al19 to define the proportion of the coronary arterial tree with angiographically detectable coronary atheroma. The proportion of each vessel involved by atheroma, identified by lumen irregularity, was multiplied by a factor for each vessel, which is related to the length of that vessel. The scores for each vessel were added to give a total score out of 100. This percentage represents the proportion of the coronary intimal surface area containing coronary atheroma.16

    Statistical methods

    All analyses were performed using SAS statistical software (V.9.2, SAS Institute, Cary, North Carolina, USA). Statistical significance was defined as p value <0.05.

    Cases of ERM without signs of diabetic retinopathy, retinal vein occlusion, following cataract surgery and other known secondary causes were classified as idiopathic ERM, and were analysed separately. Age-specific and sex-specific ERM prevalence (both idiopathic and overall) was determined for PMF, CMR and any ERM. χ2 tests were used to determine whether there were significant age-specific or sex-specific differences in the prevalence of ERM (PMF, CMR and any ERM). McNemar’s test was used to determine whether there were significant differences in prevalence between left and right eyes in patients with bilateral ERM (PMF, CMR and any ERM).

    The prevalence of idiopathic ERM in the AHES, standardised by age, was retrospectively compared with the idiopathic ERM prevalence in participants aged over 50 years from BMES-1.

    Multivariate analyses using logistic regression models adjusted for age and sex were used to estimate ORs and 95% CIs in order to determine whether associations exist between coronary angiographic scores (vessel score, segment score, Gensini score and extent score) and prevalence of idiopathic ERM (CMR, PMF, any ERM).

    Results

    A total of 1664 participants had information on ERM prevalence and complete data on CAD extent and severity, and were included in the analyses. Of these, 1210 (72.7%) were idiopathic cases of ERM, with no secondary cause identified. The mean age of participants was 61.1±11.7 years. Table 1 summarises the baseline characteristics of the study population.

    View this table:
    Table 1

    Demographic and clinical characteristics of participants*

    The overall prevalence of ERM was 7.0% (n=115), with near equal prevalence (3.5%) of the more severe form, PMF (n=59), and the less severe form, CMR (n=56). The prevalence of idiopathic ERM was 5.9% (n=71), including 2.7% (n=33) with PMF and 3.2% (n=38) with CMR. Table 2 and figures 1 and 2 show the prevalence of PMF, CMR and any ERM, stratified by age and sex, in overall and idiopathic ERM, respectively. There were no significant differences in PMF, CMR and any ERM frequencies between men and women (p>0.05). There were significant differences in PMF, CMR and any ERM frequencies between different age groups, with frequency tending to increase with age. This was the case for both idiopathic and secondary ERM cases.

    View this table:
    Table 2

    Prevalence (%) of epiretinal membranes overall (n=1664) and idiopathic (n=1210) by age and sex in the AHES

    Figure 1
    Figure 1

    Prevalence of preretinal macular fibrosis (PMF), cellophane macular reflex (CMR) and any epiretinal membrane (ERM), stratified by age in years.

    Figure 2
    Figure 2

    Prevalence of preretinal macular fibrosis (PMF), cellophane macular reflex (CMR) and any epiretinal membrane (ERM), stratified by sex.

    Of the total number of ERM cases, 35.2% of participants had bilateral ERM (any ERM n=25, PMF n=13, CMR n=12). There were no significant differences in ERM frequencies between left and right eyes, for any category of ERM (PMF, CMR and any ERM).

    Table 3 indicates that the prevalence of idiopathic PMF was higher in the AHES than the BMES (age-standardised prevalence 4.0% and 2.0%, respectively) (p=0.0002). There were no significant differences in the prevalence of idiopathic CMR between the two studies (p=0.50).

    View this table:
    Table 3

    Age-standardised prevalence of idiopathic epiretinal membrane (ERM) in the baseline Blue Mountains Eye Study (BMES-1) and Australian Heart Eye Study (AHES), for patients aged ≥50 years

    No significant associations were found between the extent and severity of CAD, as measured by coronary angiography (vessel, segment, Gensini, extent scores) and ERM (PMF, CMR and any ERM) (p>0.05). For instance, for the association between Gensini/extent scores and any ERM, age–sex adjusted OR were 1.52 (95% CI 0.59 to 3.95, p=0.39) and 1.53 (95% CI 0.58 to 4.01, p=0.39), respectively.

    Discussion

    This is the first study to investigate whether an association exists between cardiovascular disease, as quantified by coronary angiography measures of CAD, and idiopathic ERM. The extent and severity of CAD were not associated with either the severe (PMF) or mild (CMR) form of ERM.

    Previous studies have demonstrated strong associations between ERM and age, as well as ocular conditions inherent to the eye, such as posterior vitreous detachment, retinal vein occlusion, diabetic retinopathy, previous cataract surgery and refractive error.1 ,2 ,6–8 It is thought that in these conditions, retinal pigment epithelium, glial cells, fibrous astrocytes, fibrocytes, myofibroblasts and other proliferative factors migrate behind the retina.20–22

    In contrast, although some previous studies have linked ERM to systemic diseases such as diabetes, hypertension and hypercholesterolaemia, there have been no consistent associations established in this regard.2 ,8 The results of the present study join the ranks of this growing body of literature that suggests that local rather than systemic factors appear to play the most important role in the aetiology of ERM.

    However, this study found a significantly higher prevalence of the more severe form of idiopathic ERM (PMF) relative to the age-standardised rates from a large-scale population-based study, the BMES. The prevalence of PMF in the AHES was double than that in the BMES-1. In contrast, prevalence of CMR and idiopathic ERM were comparable between the two studies. It is unlikely that the interstudy variation in PMF frequency can be accounted for by differences in grading protocols between studies. All retinal photographs in the AHES were assessed by the same grader as the BMES.12 Moreover, PMF is defined by the visualisation of distinct retinal folds, and can therefore be more objectively characterised on retinal imaging than CRM.2 The fact that PMF prevalence was significantly greater in a high-risk cardiovascular cohort compared with a population-based cohort suggests that there may be a link between cardiovascular disease and more severe forms of idiopathic ERM.2

    However, it is important to note that two population-based studies, the Singapore Indian (SINDI) Eye Study and the Singapore Malay Eye Study (SiMES), have also identified significantly higher prevalence of PMF, but not CMR, relative to the BMES.10 ,23 Therefore, it remains to be established whether the aetiology of ERM also extends beyond local factors in the ocular environment to systemic causes, including cardiovascular disease.

    Trends in ERM prevalence

    The idiopathic rates of ERM in our study were similar to those reported by the SiMES (n=3280),23 but lower than that reported by the Funagata Study (n=1723).1 The overall rate of ERM reported in our study was similar to that of the Melbourne Collaborative Cohort Study (n=21 241)24 and the SINDI Eye Study (n=3400),10 but lower than that of the Los Angeles Latino Eye Study (n=5982)6 and the Multi-Ethnic Study of Atherosclerosis (n=5960).2 The latter discrepancy is likely grounded on ethnic differences between the study samples, with Fraser-Bell et al concluding that the prevalence of ERM is higher among Latino populations.6 In contrast, the major ethnicity of participants in the AHES was Caucasian (68.0%).

    The overall ERM prevalence in our study was higher than that of the Handan Eye Study of a rural Chinese population (n=7557),8 as well as that of the Beijing Eye Study (n=4439).25 This is in accordance with the hypothesis that the prevalence of ERM may be lower in Chinese populations.8 ,25 However, it is worth noting that the Multi-Ethnic Study of Atherosclerosis found a higher rate of ERM among Chinese participants compared with white, black and Hispanic populations.2

    The prevalence of bilateral ERM in this study was 35.2%, similar to that reported by the BMES-1 (31.0%).12 The bilateral nature of the disease has previously been explained by the fact that posterior vitreous detachment, which mostly occurs prior to ERM, is often bilateral.6

    The prevalence of both idiopathic and secondary ERM followed an upward trend for all participants other than those aged over 80 years, in whom there was a decreased prevalence. It has been hypothesised that participants in this age group tend to exhibit more severe cataract, which introduces media opacities within retinal photographs. This may cause an underestimation of the prevalence of ERM in this age group.9

    Study strengths and weaknesses

    Strengths of this study included its direct quantification of CAD through routine coronary angiography and its unique clinical cohort consisting of patients symptomatic for cardiovascular disease. Another key strength was that all retinal photographs were assessed by the same grader who assessed this lesion in the BMES, using standardised and reproducible protocols.

    One limitation of the study is the bias that is introduced when drawing comparisons between two discrete studies, the AHES and BMES. The same grader was employed in both studies, and we standardised the age-specific crude ERM prevalence in the AHES against the age-specific rates and age-specific sample sizes of the BMES population. However, this does not account for other inherent differences between the studies, such as the use of different cameras.

    A second limitation is that spectral domain optical coherence tomography (SD-OCT) was not used in this study. The main reason for not implementing SD-OCT was logistical in nature, due to a lack of funding, resources, time and space for the equipment. With these obstacles in view, a decision was made to omit SD-OCT investigations, as they were unlikely to detect anything more than mild, clinically insignificant ERMs. A third limitation is that there was a small sample size of patients with both ERM and CAD, which limited the power of statistical analysis of these two variables of interest. It is also possible that this may help to explain the non-significant finding when the potential association between CAD and ERM was analysed. Finally, the cross-sectional design of this study rendered it difficult to infer causal relationships.

    In conclusion, this study joins a growing body of literature that has attempted to trace the aetiology of idiopathic ERM to systemic factors such as cardiovascular disease, diabetes, hypertension and hypercholesterolaemia. While the link between CAD and ERM remains inconclusive, the search for systemic clues to the onset of ERM remains important, especially because definitive surgical intervention is in place for ERM.

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    Footnotes

    • Contributors All authors are justifiably credited with authorship, according to the authorship criteria. In detail, SBW: analysis and interpretation of data, drafting of manuscript, final approval given. PM, KP, JC, AJHP, AT, BG: conception, design, data acquisition, critical revision of manuscript, final approval given. GB: analysis and interpretation of data, critical revision of manuscript, final approval given.

    • Competing interests None declared.

    • Patient consent Obtained.

    • Ethics approval Obtained from the Western Sydney Local Health Network Human Research Ethics Committee (Westmead) for the AHES.

    • Provenance and peer review Not commissioned; externally peer reviewed.

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