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Cataract risk of neuro-interventional procedures: a nationwide population-based matched-cohort study
Clinical Radiology xxx (2018) 1e6
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Cataract risk of neuro-interventional procedures: a nationwide population-based matched-cohort study K.L. Cheng a, b, c, J.Y. Huang d, C.L. Su e, K.C. Tung c, J.Y. Chiou f, g, * a
Department of Medical Imaging, Chung Shan Medical University Hospital, 110 Jianguo North Road, Taichung 40201, Taiwan b School of Medical Imaging and Radiological Sciences, Chung Shan Medical University, 110 Jianguo North Road, Taichung 40201, Taiwan c Department of Veterinary Medicine, National Chung Hsing University, 250 Kuo Kuang Road, Taichung 40201, Taiwan d Department of Medical Research, Chung Shan Medical University Hospital, 110 Jianguo North Road, Taichung 40201, Taiwan e Department of Public Health, Chung Shan Medical University, 110 Jianguo North Road, Taichung 40201, Taiwan f School of Health Policy and Management, Chung Shan Medical University, 110 Jianguo North Road, Taichung 40201, Taiwan g Department of Medical Management, Chung Shan Medical University Hospital, 110 Jianguo North Road, Taichung 40201, Taiwan
art icl e i nformat ion Article history: Received 16 May 2017 Accepted 4 May 2018
AIM: To demonstrate the risk of cataract associated with radiation exposure from neurointerventional procedures. MATERIALS AND METHODS: This was a nationwide population-based, matched-cohort study. The exposed group (group E) comprised patients diagnosed with an aneurysm, cerebrovascular system anomaly, or subarachnoid haemorrhage who underwent a neurointerventional procedure, such as brain digital subtraction angiography or endovascular embolisation. The comparison group (group C) included subjects who were never exposed to radiation from neuro-interventional procedures and were propensity score-matched by the date of enrolment, age, sex, and associated comorbidities. Multiple Cox proportional hazard regression analysis was used to estimate the hazard ratio (HR) of cataract risk due to radiation exposure while adjusting for potential confounding factors. RESULTS: There were 838 patients and 3,352 matched subjects in groups E and C, respectively. The incidence of cataracts was significantly greater among subjects in group E (adjusted HR [aHR] ¼ 1.88; 95% confidence interval [CI] ¼ 1.08e3.26), especially those aged >40 years (aHR ¼ 2.14; 95% CI ¼ 1.16e3.94). The number of computed tomography examinations was positively correlated, but not statistically significant, with an increased risk of cataract occurrence. CONCLUSIONS: Neuro-interventional procedures might be significantly associated with an increased risk of cataract occurrence. Ó 2018 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
* Guarantor and correspondent: J.Y. Chiou, School of Health Policy and Management, Chung Shan Medical University, Department of Medical Management, Chung Shan Medical University Hospital, No.110, Sec.1, Jianguo N. Rd. Taichung, Taiwan. Tel.: þ886 4 2473 0022, ext.:11789. E-mail address: [email protected] (J.Y. Chiou). https://doi.org/10.1016/j.crad.2018.05.019 0009-9260/Ó 2018 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Cheng KL, et al., Cataract risk of neuro-interventional procedures: a nationwide population-based matchedcohort study, Clinical Radiology (2018), https://doi.org/10.1016/j.crad.2018.05.019
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K.L. Cheng et al. / Clinical Radiology xxx (2018) 1e6
Introduction Neuro-interventional procedures, such as brain digital subtraction angiography and endovascular embolisation, are widely accepted as a choice of diagnosis and treatment of acute subarachnoid haemorrhage (SAH), unruptured aneurysms, and intracranial vascular anomalies1e5; however, interventional neuroradiological procedures may convey clinically significant doses of radiation to the eyes of the patient, even when performed by experienced neuroradiologists with modern fluoroscopy imaging systems.6e8 Therefore, possible side effects of radiation remain a concern in this scenario. Many animal studies,9 as well as human studies of atomic bomb survivors10,11 and workers that clean up after nuclear accidents,12 have consistently shown that radiation exposure increases the risk of cataract occurrence. In response to these studies, various types of equipment have been recommended to protect medical personnel from occupational radiation exposure to reduce the risk of radiation-induced side effects13; however, eye protective shields are not commonly used for patients receiving neuro-interventional procedures because of the appearance of artefacts that decrease image quality. Although the benefits of neuro-interventional procedures are believed to outweigh the possible risks of radiationinduced eye lens injuries, these procedures still pose a higher risk of cataract and thus warrant further assessment. To date, no study has investigated the association between radiation exposure from neuro-interventional procedures and the risk of cataract occurrence in patients. Therefore, the purpose of the present study was to investigate the association between cataract development and radiation exposure from neuro-interventional procedures among patients registered in the Taiwan National Health Insurance Research Database (NHIRD).
Materials and methods Database The single-payer compulsory social Taiwan National Health Insurance (NHI) programme was instituted in 1995 and covered almost 99% of the Taiwanese population in 2004. For this study, data were retrieved from the Longitudinal Health Insurance Database 2000 (LHID 2000), a subset of the NHIRD, which contains one million beneficiaries randomly sampled from the original claims data of the 2000 Registry for Beneficiaries of the NHIRD. All registration and claim data of the LHID 2000 from 1 January 2000 to 31 December 2013 were collected for analysis. To protect patient privacy, all personal information was encrypted by scrambling the associated identification codes before release to the researchers. Disease identification in the NHIRD was based on the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM). As incorrect codes and diagnoses result in severe penalties imposed by the NHI administration, the accuracy and
validity of the diagnoses of disease in the NHIRD are highly reliable.14,15 A longitudinal database and retrospective cohort study design were used to reveal the association between radiation exposure and cataract occurrence. The study protocol was approved by the Institutional Review Board of Chung Shan Medical University Hospital (Taichung City, Taiwan).
Study participants The exposed group (group E) was comprised of patients newly diagnosed with brain aneurysm (ICD-9-CM code 437.3), cerebrovascular system anomaly (ICD-9-CM code 747.81), or subarachnoid haemorrhage (ICD-9-CM code 430) who underwent a neuro-interventional procedure, such as brain digital subtraction angiography or endovascular embolisation, from 1 January 2002 to 31 December 2011. The index date was the first day of receiving a neurointerventional procedure. The number of computed tomography (CT) examinations 365 days before and 30 days after the index date was also recorded. Patients diagnosed with cataract (ICD-9-CM code 366.xx) or head and neck cancer (ICD-9-CM codes 140e149 and 160e161) before the index date and missing of demographic data were excluded. Only patients aged 20e50 years were enrolled to minimise the possibility of senile cataract (Fig 1).
Selected controls The control group (group C) was comprised of patients who never underwent brain digital subtraction angiography, endovascular embolisation, and CT, who were retrieved from the LHID 2000 and matched at a propensity score ratio of 1:4 with cases enrolled in group E. The index date of group C was matched to that of group E. Propensity score matching was used to control for the confounding factors of age, sex, and pre-existing comorbidity, such as diabetes mellitus (ICD-9-CM code 250.xx), hypertension (ICD-9-CM code 401.xx-405.xx), chronic obstructive pulmonary disease (COPD; ICD-9-CM code 496.xx), coronary artery disease (ICD-9-CM code 411.xx-414.xx), and autoimmune diseases, including rheumatoid arthritis (ICD-9CM code 714.0), systemic lupus erythematosus (ICD-9-CM code 710.0), ankylosing spondylitis (ICD-9-CM code 720.0), and psoriasis (ICD-9-CM code 696).
Identification of cataract Subjects with a major event of cataract development were identified by the indication of at least two clinical visits with a cataract diagnosis (ICD-9-CM code 366.xx) from 2002 to 2013. All participations were tracked from the index date to the date that major event occurred or the date of censor, which included withdraw from the NHIRD or the end of the study (December 2013).
Statistical analysis The two-tailed t-test and chi-square test were used to identify differences in continuous and categorical baseline
Please cite this article in press as: Cheng KL, et al., Cataract risk of neuro-interventional procedures: a nationwide population-based matchedcohort study, Clinical Radiology (2018), https://doi.org/10.1016/j.crad.2018.05.019
K.L. Cheng et al. / Clinical Radiology xxx (2018) 1e6
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Figure 1 Study flowchart. LHID: Longitudinal Health Insurance Database; ICD-9-CM, International Classification of Diseases, Ninth Revision, Clinical Modification. Brain fluoroscopic intervention, including brain digital subtraction angiography and endovascular embolisation. Brain aneurysm: ICD-9-CM code 437.3. Cerebrovascular system anomalies: ICD-9-CM code 747.81. SAH: subarachnoid haemorrhage, ICD-9-CM code 430. PSM: propensity score matching.
characteristics, respectively. The time to event analysis was conducted to evaluate the relative risk of cataract incidence between groups C and E. Poisson regression analysis was conducted to calculate the rate of cataract incidence and the associated 95% confidence interval (95% CI). Multiple Cox proportional hazard regression analysis was used to estimate the hazard ratio (HR) (95% CI) of cataract incidence due to radiation exposure, while adjusting for potential confounding factors. SAS software was used for all statistical analyses and a probability (p) value of < 0.05 was considered statistically significant.
Results As shown in Table 1, there were no significant differences in the baseline demographic characteristics of age, sex, and comorbidities (i.e., diabetes mellitus, hypertension, COPD, autoimmune disease, and coronary artery disease) between groups C and E. The risk of cataracts was estimated using a
multiple Cox proportional hazard model and the results are presented in Table 2. After adjusting for age, sex, and comorbidities, the adjusted hazard ratio (aHR) of neurointerventional procedures as independent risk factors for cataract occurrence was 1.88 (95% CI ¼ 1.08e3.26, p¼0.025). Other independent risks for cataract occurrence were age (aHR in an increment of 1 year ¼ 1.15; 95% CI ¼ 1.09e1.20) and diabetes mellitus (aHR ¼ 2.92; 95% CI ¼ 1.29e6.59). The crude incidence rate and aHR for cataracts due to neuro-interventional procedures stratified by age (20e29, 30e39, and 40e49 years) are shown in Table 3. Among subjects aged 20e29 years, the crude incidence rate (per 105 person-months) of cataracts was 0.00 (95% CI ¼ 0.00e16.67) in group E and the crude incidence rate of cataracts was 4.06 (95% CI ¼ 1.31e12.58) in group C. Among subjects aged 30e39 years, the aHR was 2.23 (95% CI ¼ 0.55e8.98). Among subjects aged 40e49 years, the aHR was 2.14 (95% CI ¼ 1.16e3.94). Furthermore, the number of CT examinations from 365 days before to 30 days after the index date was
Please cite this article in press as: Cheng KL, et al., Cataract risk of neuro-interventional procedures: a nationwide population-based matchedcohort study, Clinical Radiology (2018), https://doi.org/10.1016/j.crad.2018.05.019
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K.L. Cheng et al. / Clinical Radiology xxx (2018) 1e6
Table 1 Demographic data of the study population.
Age (mean SD), years Sex Female Male Comorbidities Diabetes mellitusa Hypertensionb COPDc Autoimmune diseased Coronary artery diseasee
Comparison group (n¼3,352)
Exposure group (n¼838)
p-Value
36.32 8.85
36.15 8.73
0.61 0.72
1421 1931
(42.4%) (57.6%)
361 477
(43.1%) (56.9%)
103 442 154 26 69
(3.07%) (13.2%) (4.59%) (0.78%) (2.02%)
30 109 39 7 23
(3.58%) (13.0%) (4.65%) (0.84%) (2.69%)
0.45 0.89 0.94 0.86 0.17
Except for age and p-values, data are number (%) of patients. The p-values for comparisons between the two categorical groups were determined with the chi-square test. Continuous data were compared with the two-tailed t-test. All chronic conditions were defined by administrative claims using International Classification of Diseases, Ninth Revision, Clinical Modification (ICD9-CM) codes. SD, standard deviation. a Diabetes mellitus: ICD-9-CM code 250.xx. b Hypertension: ICD-9-CM code 401.xx-405.xx. c Chronic obstructive pulmonary disease (COPD): ICD-9-CM code 496.xx. d Autoimmune diseases: rheumatoid arthritis (ICD-9-CM code 714.0), systemic lupus erythematosus (ICD-9-CM code 710.0), ankylosing spondylitis (ICD-9-CM code 720.0), and psoriasis (ICD-9-CM code: 696). e Coronary artery disease: ICD-9-CM code 411.xx-414.xx.
Table 2 Multiple Cox proportional hazard model for cataract formation.
Exposure Age (per year) Sex Female Male Comorbidities Diabetes mellitus Hypertension COPD Autoimmune disease Coronary artery disease
aHR
95% CI
p-Value
1.88 1.15
1.08e3.26 1.09e1.20
0.025 <.001
Reference 0.94
0.57e1.56
0.823
2.92 1.03 0.80 2.08 2.68
1.29e6.59 0.54e1.94 0.28e2.27 0.29e15.18 0.82e8.76
0.010 0.936 0.679 0.470 0.104
aHR, adjusted hazard ratio; CI, confidence interval; COPD, chronic obstructive pulmonary disease.
classified into four groups (Table 4). When compared with patients who underwent one or two CT scans, the aHR was 0.80 (95% CI ¼ 0.13e4.85), 1.52 (95% CI ¼ 0.41e5.58), and 1.88 (95% CI ¼ 0.41e8.65) for patients who did not receive a CT examination and those who underwent CT examinations 3e4 times and 5 times, respectively, and the p value for the trend was 0.345. In addition, the risk of cataract was higher among patients who received more than one CT examination within a single year, but there was no significant association between CT and risk of cataracts among those who underwent neuro-interventional procedures.
Discussion The results of this nationwide population-based matched-cohort study demonstrated the effects of neuro-
interventional procedures on cataract occurrence. After correction with a propensity score-matched model, exposure to neuro-interventional procedures was found to be significantly correlated with an increased risk of cataract development (aHR ¼ 1.88, 95% CI ¼ 1.08e3.26). Subsequent analysis demonstrated that exposed subjects aged >40 years were at a twofold increased risk of cataract occurrence (aHR ¼ 2.14, 95% CI ¼ 1.16e3.94), as compared to matched controls. These data reinforce previous findings that radiation exposure due to neuro-interventional procedures might be associated with an increased risk of cataract occurrence, further demonstrating the necessity of postprocedural ophthalmological examinations. The lens of the eye has long been considered as one of the most radiosensitive tissues in the human body.16 Iatrogenic radiation-induced cataract formation among medical personnel is well documented in the literature, especially for interventional cardiologists,17e19 radiologists,20,21 and radiographers.22,23 Other epidemiologic studies of Chernobyl clean-up workers12 and Japanese atomic bomb survivors10,11 also demonstrated associations between radiation exposure and cataract occurrence; however, few studies have focused on the occurrence of cataract among patients exposed to medical radiation from CT examinations.24e26 The present study is the first to demonstrate an association between neuro-interventional procedures and cataract occurrence in patients. The Taiwanese NHI programme covers all reimbursements for neuro-interventional procedures and allows access to data for nationwide longitudinal studies. In accordance with the findings of previous studies, the results of the present study indicate that neuro-interventional procedures increase the risk of cataract occurrence by 87.7%. Sandborg et al. found that the maximum radiation dose to the eye lens during interventional neuroradiological procedures is between 289 and 515 mSv, depending on the different procedures.27 In 2012, the International Commission on Radiological Protection guidelines lowered the single-dose threshold for cataract induction from 5 to 0.5 Gy28; however, an increased cataract occurrence was also found in 8,607 Chernobyl clean-up workers, of whom most received a cumulative dose of <0.5 Gy.12 Although exact dose estimation in the present study was difficult, Sandborg et al. had concluded that the doses to the eye lens during neuro-interventional procedures might be sufficiently higher than the threshold of cataract formation. Likewise, the findings of the present retrospective study comparing an exposed group with an age-, sex-, and comorbiditymatched control group further demonstrated an increased rate of cataract occurrence in patients receiving neurointerventional procedures. Cataract formation is an age-related disease that is promoted by radiation exposure. Hence, the elderly might be more vulnerable to biochemical and biophysical changes of the lens in response to radiation exposure.29 As radiationinduced cataract formation is more common before the age of 50 years22 and the prevalence of cataracts among the Taiwanese population aged >50 years is 51%,30 the cohort of this study was limited to subjects aged <50 years.
Please cite this article in press as: Cheng KL, et al., Cataract risk of neuro-interventional procedures: a nationwide population-based matchedcohort study, Clinical Radiology (2018), https://doi.org/10.1016/j.crad.2018.05.019
K.L. Cheng et al. / Clinical Radiology xxx (2018) 1e6
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Table 3 Associations of risk for cataract formation due to radiation exposure by age. Age
20e29 years
n Follow-up person-months Cataract events Crude incidence rate (95% CI)a Adjusted hazard ratio (95% CI)b
30e39 years
40e49 years
Comparison
Exposure
Comparison
Exposure
Comparison
Exposure
883 73,951 3 4.06 (1.31e12.58) Reference
222 18,000 0 0.00 (0.00e16.67) -
1,055 83,746 7 8.36 (3.99e17.54) Reference
270 19,161 3 15.66 (5.05e48.55) 2.23 (0.55e8.98)
1,414 109,090 34 31.17 (22.27e43.62) Reference
346 23,880 15 62.82 (37.87e104.20) 2.14 (1.16e3.94)
a
Per 105 person-months. Adjusted for age, sex, and comorbidities (i.e., diabetes mellitus, hypertension, chronic obstructive pulmonary disease, coronary artery disease, and autoimmune disease). b
Table 4 Risk of cataract formation according to number of CT examinations.
No. of CT examinations 0 (n¼51) 1-2 (n¼624) 3-4 (n¼118) 5 (n¼45) p for the trend
aHRa
95% CI
p-Value
0.80 Reference 1.52 1.88 -
0.13e4.85 0.41e5.58 0.41e8.65 -
0.811 0.530 0.418 0.345
b
aHR, adjusted hazard ratio; CI, confidence interval. a Adjusted for age, sex, and comorbidities. b The number of CT examinations was calculated from e365 days to þ30 days from the index date.
The results of the present study showed a trend of increased risk of cataract occurrence in response to radiation exposure with increasing age, especially for subjects aged >40 years (aHR ¼ 2.14; 95% CI ¼ 1.16e3.94). These results are in accordance with the findings of a study by Chodick et al. of 35,705 radiological technologists in the US who were followed for almost 20 years. An increased risk of cataract occurrence with age per year was found both in the present study (14.7%) and that by Chodick et al. (15%)22; however, the results of the present study also indicate that radiation exposure later in life might be associated with an increased risk of cataract occurrence.23 In contrast to the study by Chodick et al., there was no incidence of cataract among subjects aged 20e29 years in the present study. This discrepancy might be due to the smaller number of subjects or the shorter follow-up time in the present study. Until now, only three population-based studies have explored the potential association between CT radiation exposure and cataract occurrence. Of these, the Beaver Dam Eye Study conducted in the US found a modest positive association,24 while the Blue Mountains Eye Study conducted in Australia found no statistically significant association between CT and cataract occurrence.25 Both of these studies used self-reported exposure to CT examinations, thus the potential bias of self-reported questionnaires should be considered. Another populated-based study conducted by the NHIRD of Taiwan found a positive dosedependent relationship between head and neck CT exposure and cataract occurrence.26 CT is an important technique to evaluate intracranial vascular anomalies and subarachnoid haemorrhage,31 and almost all subjects in
group E underwent CT examinations both before and after neuro-interventional procedures. In order to delineate the confounding effect of repeated CT examinations on cataract formation, subgroup analysis based on the number of CT studies was performed, which demonstrated a trend, but not statistically significance, of an increased risk of cataract occurrence associated with increasing CT frequency. This finding was in contrast to a report by Yuan et al. [26], which may have resulted from a discrepancy in the study design limited to the effects of CT in the exposed group. The present study had several limitations. First, diagnosis of cataract was fully dependent on ICD-9 codes, thus the severity of cataract could not be clearly identified. To improve diagnostic accuracy, only cases of cataract, as confirmed by two outpatient visits, were included for analysis; however, sampled claims data from every hospital in Taiwan are randomly checked by peer review for verification of diagnostic accuracy. Second, the NHIRD only provides information about the frequency of neurointerventional procedures and CT examinations; however, different hospitals employ different protocols and treatment strategies. Therefore, the exact radiation dose from every examination included in this study could not be determined. Hence, these data disallow a recommendation for a safe limitation of radiation exposure for neurointerventional procedures. Third, ethnic and racial disparities can affect cataract occurrence32; therefore, generalising these results to different racial groups is limited. In conclusion, as the use of neuro-interventional procedures is widespread with increasing frequency, the results of the present study offer additional information to demonstrate the long-term health issues of radiation exposure derived from brain fluoroscopic diagnostic and therapeutic interventions. This nationwide populationbased study using the Taiwan NHIRD showed a possible association between neuro-interventional procedures and cataract occurrence, as exposure to neuro-interventional procedures might be significantly associated with an increased risk of cataract occurrence, especially for patients aged >40 years. These results suggest informing patients regarding the possible cataract risk before neurointerventional procedures and also suggest the need for regular ophthalmological examinations after neurointerventional procedures to ensure early detection of cataract formation.
Please cite this article in press as: Cheng KL, et al., Cataract risk of neuro-interventional procedures: a nationwide population-based matchedcohort study, Clinical Radiology (2018), https://doi.org/10.1016/j.crad.2018.05.019
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Acknowledgements This study has received funding from Chung Shan Medical University, Taiwan (grant no.: CSMU-INT-104-04).
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Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Cataract risk of neuro-interventional procedures: a nationwide population-based matched-cohort study K.L. Cheng a, b, c, J.Y. Huang d, C.L. Su e, K.C. Tung c, J.Y. Chiou f, g, * a
Department of Medical Imaging, Chung Shan Medical University Hospital, 110 Jianguo North Road, Taichung 40201, Taiwan b School of Medical Imaging and Radiological Sciences, Chung Shan Medical University, 110 Jianguo North Road, Taichung 40201, Taiwan c Department of Veterinary Medicine, National Chung Hsing University, 250 Kuo Kuang Road, Taichung 40201, Taiwan d Department of Medical Research, Chung Shan Medical University Hospital, 110 Jianguo North Road, Taichung 40201, Taiwan e Department of Public Health, Chung Shan Medical University, 110 Jianguo North Road, Taichung 40201, Taiwan f School of Health Policy and Management, Chung Shan Medical University, 110 Jianguo North Road, Taichung 40201, Taiwan g Department of Medical Management, Chung Shan Medical University Hospital, 110 Jianguo North Road, Taichung 40201, Taiwan
art icl e i nformat ion Article history: Received 16 May 2017 Accepted 4 May 2018
AIM: To demonstrate the risk of cataract associated with radiation exposure from neurointerventional procedures. MATERIALS AND METHODS: This was a nationwide population-based, matched-cohort study. The exposed group (group E) comprised patients diagnosed with an aneurysm, cerebrovascular system anomaly, or subarachnoid haemorrhage who underwent a neurointerventional procedure, such as brain digital subtraction angiography or endovascular embolisation. The comparison group (group C) included subjects who were never exposed to radiation from neuro-interventional procedures and were propensity score-matched by the date of enrolment, age, sex, and associated comorbidities. Multiple Cox proportional hazard regression analysis was used to estimate the hazard ratio (HR) of cataract risk due to radiation exposure while adjusting for potential confounding factors. RESULTS: There were 838 patients and 3,352 matched subjects in groups E and C, respectively. The incidence of cataracts was significantly greater among subjects in group E (adjusted HR [aHR] ¼ 1.88; 95% confidence interval [CI] ¼ 1.08e3.26), especially those aged >40 years (aHR ¼ 2.14; 95% CI ¼ 1.16e3.94). The number of computed tomography examinations was positively correlated, but not statistically significant, with an increased risk of cataract occurrence. CONCLUSIONS: Neuro-interventional procedures might be significantly associated with an increased risk of cataract occurrence. Ó 2018 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
* Guarantor and correspondent: J.Y. Chiou, School of Health Policy and Management, Chung Shan Medical University, Department of Medical Management, Chung Shan Medical University Hospital, No.110, Sec.1, Jianguo N. Rd. Taichung, Taiwan. Tel.: þ886 4 2473 0022, ext.:11789. E-mail address: [email protected] (J.Y. Chiou). https://doi.org/10.1016/j.crad.2018.05.019 0009-9260/Ó 2018 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
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Introduction Neuro-interventional procedures, such as brain digital subtraction angiography and endovascular embolisation, are widely accepted as a choice of diagnosis and treatment of acute subarachnoid haemorrhage (SAH), unruptured aneurysms, and intracranial vascular anomalies1e5; however, interventional neuroradiological procedures may convey clinically significant doses of radiation to the eyes of the patient, even when performed by experienced neuroradiologists with modern fluoroscopy imaging systems.6e8 Therefore, possible side effects of radiation remain a concern in this scenario. Many animal studies,9 as well as human studies of atomic bomb survivors10,11 and workers that clean up after nuclear accidents,12 have consistently shown that radiation exposure increases the risk of cataract occurrence. In response to these studies, various types of equipment have been recommended to protect medical personnel from occupational radiation exposure to reduce the risk of radiation-induced side effects13; however, eye protective shields are not commonly used for patients receiving neuro-interventional procedures because of the appearance of artefacts that decrease image quality. Although the benefits of neuro-interventional procedures are believed to outweigh the possible risks of radiationinduced eye lens injuries, these procedures still pose a higher risk of cataract and thus warrant further assessment. To date, no study has investigated the association between radiation exposure from neuro-interventional procedures and the risk of cataract occurrence in patients. Therefore, the purpose of the present study was to investigate the association between cataract development and radiation exposure from neuro-interventional procedures among patients registered in the Taiwan National Health Insurance Research Database (NHIRD).
Materials and methods Database The single-payer compulsory social Taiwan National Health Insurance (NHI) programme was instituted in 1995 and covered almost 99% of the Taiwanese population in 2004. For this study, data were retrieved from the Longitudinal Health Insurance Database 2000 (LHID 2000), a subset of the NHIRD, which contains one million beneficiaries randomly sampled from the original claims data of the 2000 Registry for Beneficiaries of the NHIRD. All registration and claim data of the LHID 2000 from 1 January 2000 to 31 December 2013 were collected for analysis. To protect patient privacy, all personal information was encrypted by scrambling the associated identification codes before release to the researchers. Disease identification in the NHIRD was based on the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM). As incorrect codes and diagnoses result in severe penalties imposed by the NHI administration, the accuracy and
validity of the diagnoses of disease in the NHIRD are highly reliable.14,15 A longitudinal database and retrospective cohort study design were used to reveal the association between radiation exposure and cataract occurrence. The study protocol was approved by the Institutional Review Board of Chung Shan Medical University Hospital (Taichung City, Taiwan).
Study participants The exposed group (group E) was comprised of patients newly diagnosed with brain aneurysm (ICD-9-CM code 437.3), cerebrovascular system anomaly (ICD-9-CM code 747.81), or subarachnoid haemorrhage (ICD-9-CM code 430) who underwent a neuro-interventional procedure, such as brain digital subtraction angiography or endovascular embolisation, from 1 January 2002 to 31 December 2011. The index date was the first day of receiving a neurointerventional procedure. The number of computed tomography (CT) examinations 365 days before and 30 days after the index date was also recorded. Patients diagnosed with cataract (ICD-9-CM code 366.xx) or head and neck cancer (ICD-9-CM codes 140e149 and 160e161) before the index date and missing of demographic data were excluded. Only patients aged 20e50 years were enrolled to minimise the possibility of senile cataract (Fig 1).
Selected controls The control group (group C) was comprised of patients who never underwent brain digital subtraction angiography, endovascular embolisation, and CT, who were retrieved from the LHID 2000 and matched at a propensity score ratio of 1:4 with cases enrolled in group E. The index date of group C was matched to that of group E. Propensity score matching was used to control for the confounding factors of age, sex, and pre-existing comorbidity, such as diabetes mellitus (ICD-9-CM code 250.xx), hypertension (ICD-9-CM code 401.xx-405.xx), chronic obstructive pulmonary disease (COPD; ICD-9-CM code 496.xx), coronary artery disease (ICD-9-CM code 411.xx-414.xx), and autoimmune diseases, including rheumatoid arthritis (ICD-9CM code 714.0), systemic lupus erythematosus (ICD-9-CM code 710.0), ankylosing spondylitis (ICD-9-CM code 720.0), and psoriasis (ICD-9-CM code 696).
Identification of cataract Subjects with a major event of cataract development were identified by the indication of at least two clinical visits with a cataract diagnosis (ICD-9-CM code 366.xx) from 2002 to 2013. All participations were tracked from the index date to the date that major event occurred or the date of censor, which included withdraw from the NHIRD or the end of the study (December 2013).
Statistical analysis The two-tailed t-test and chi-square test were used to identify differences in continuous and categorical baseline
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Figure 1 Study flowchart. LHID: Longitudinal Health Insurance Database; ICD-9-CM, International Classification of Diseases, Ninth Revision, Clinical Modification. Brain fluoroscopic intervention, including brain digital subtraction angiography and endovascular embolisation. Brain aneurysm: ICD-9-CM code 437.3. Cerebrovascular system anomalies: ICD-9-CM code 747.81. SAH: subarachnoid haemorrhage, ICD-9-CM code 430. PSM: propensity score matching.
characteristics, respectively. The time to event analysis was conducted to evaluate the relative risk of cataract incidence between groups C and E. Poisson regression analysis was conducted to calculate the rate of cataract incidence and the associated 95% confidence interval (95% CI). Multiple Cox proportional hazard regression analysis was used to estimate the hazard ratio (HR) (95% CI) of cataract incidence due to radiation exposure, while adjusting for potential confounding factors. SAS software was used for all statistical analyses and a probability (p) value of < 0.05 was considered statistically significant.
Results As shown in Table 1, there were no significant differences in the baseline demographic characteristics of age, sex, and comorbidities (i.e., diabetes mellitus, hypertension, COPD, autoimmune disease, and coronary artery disease) between groups C and E. The risk of cataracts was estimated using a
multiple Cox proportional hazard model and the results are presented in Table 2. After adjusting for age, sex, and comorbidities, the adjusted hazard ratio (aHR) of neurointerventional procedures as independent risk factors for cataract occurrence was 1.88 (95% CI ¼ 1.08e3.26, p¼0.025). Other independent risks for cataract occurrence were age (aHR in an increment of 1 year ¼ 1.15; 95% CI ¼ 1.09e1.20) and diabetes mellitus (aHR ¼ 2.92; 95% CI ¼ 1.29e6.59). The crude incidence rate and aHR for cataracts due to neuro-interventional procedures stratified by age (20e29, 30e39, and 40e49 years) are shown in Table 3. Among subjects aged 20e29 years, the crude incidence rate (per 105 person-months) of cataracts was 0.00 (95% CI ¼ 0.00e16.67) in group E and the crude incidence rate of cataracts was 4.06 (95% CI ¼ 1.31e12.58) in group C. Among subjects aged 30e39 years, the aHR was 2.23 (95% CI ¼ 0.55e8.98). Among subjects aged 40e49 years, the aHR was 2.14 (95% CI ¼ 1.16e3.94). Furthermore, the number of CT examinations from 365 days before to 30 days after the index date was
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Table 1 Demographic data of the study population.
Age (mean SD), years Sex Female Male Comorbidities Diabetes mellitusa Hypertensionb COPDc Autoimmune diseased Coronary artery diseasee
Comparison group (n¼3,352)
Exposure group (n¼838)
p-Value
36.32 8.85
36.15 8.73
0.61 0.72
1421 1931
(42.4%) (57.6%)
361 477
(43.1%) (56.9%)
103 442 154 26 69
(3.07%) (13.2%) (4.59%) (0.78%) (2.02%)
30 109 39 7 23
(3.58%) (13.0%) (4.65%) (0.84%) (2.69%)
0.45 0.89 0.94 0.86 0.17
Except for age and p-values, data are number (%) of patients. The p-values for comparisons between the two categorical groups were determined with the chi-square test. Continuous data were compared with the two-tailed t-test. All chronic conditions were defined by administrative claims using International Classification of Diseases, Ninth Revision, Clinical Modification (ICD9-CM) codes. SD, standard deviation. a Diabetes mellitus: ICD-9-CM code 250.xx. b Hypertension: ICD-9-CM code 401.xx-405.xx. c Chronic obstructive pulmonary disease (COPD): ICD-9-CM code 496.xx. d Autoimmune diseases: rheumatoid arthritis (ICD-9-CM code 714.0), systemic lupus erythematosus (ICD-9-CM code 710.0), ankylosing spondylitis (ICD-9-CM code 720.0), and psoriasis (ICD-9-CM code: 696). e Coronary artery disease: ICD-9-CM code 411.xx-414.xx.
Table 2 Multiple Cox proportional hazard model for cataract formation.
Exposure Age (per year) Sex Female Male Comorbidities Diabetes mellitus Hypertension COPD Autoimmune disease Coronary artery disease
aHR
95% CI
p-Value
1.88 1.15
1.08e3.26 1.09e1.20
0.025 <.001
Reference 0.94
0.57e1.56
0.823
2.92 1.03 0.80 2.08 2.68
1.29e6.59 0.54e1.94 0.28e2.27 0.29e15.18 0.82e8.76
0.010 0.936 0.679 0.470 0.104
aHR, adjusted hazard ratio; CI, confidence interval; COPD, chronic obstructive pulmonary disease.
classified into four groups (Table 4). When compared with patients who underwent one or two CT scans, the aHR was 0.80 (95% CI ¼ 0.13e4.85), 1.52 (95% CI ¼ 0.41e5.58), and 1.88 (95% CI ¼ 0.41e8.65) for patients who did not receive a CT examination and those who underwent CT examinations 3e4 times and 5 times, respectively, and the p value for the trend was 0.345. In addition, the risk of cataract was higher among patients who received more than one CT examination within a single year, but there was no significant association between CT and risk of cataracts among those who underwent neuro-interventional procedures.
Discussion The results of this nationwide population-based matched-cohort study demonstrated the effects of neuro-
interventional procedures on cataract occurrence. After correction with a propensity score-matched model, exposure to neuro-interventional procedures was found to be significantly correlated with an increased risk of cataract development (aHR ¼ 1.88, 95% CI ¼ 1.08e3.26). Subsequent analysis demonstrated that exposed subjects aged >40 years were at a twofold increased risk of cataract occurrence (aHR ¼ 2.14, 95% CI ¼ 1.16e3.94), as compared to matched controls. These data reinforce previous findings that radiation exposure due to neuro-interventional procedures might be associated with an increased risk of cataract occurrence, further demonstrating the necessity of postprocedural ophthalmological examinations. The lens of the eye has long been considered as one of the most radiosensitive tissues in the human body.16 Iatrogenic radiation-induced cataract formation among medical personnel is well documented in the literature, especially for interventional cardiologists,17e19 radiologists,20,21 and radiographers.22,23 Other epidemiologic studies of Chernobyl clean-up workers12 and Japanese atomic bomb survivors10,11 also demonstrated associations between radiation exposure and cataract occurrence; however, few studies have focused on the occurrence of cataract among patients exposed to medical radiation from CT examinations.24e26 The present study is the first to demonstrate an association between neuro-interventional procedures and cataract occurrence in patients. The Taiwanese NHI programme covers all reimbursements for neuro-interventional procedures and allows access to data for nationwide longitudinal studies. In accordance with the findings of previous studies, the results of the present study indicate that neuro-interventional procedures increase the risk of cataract occurrence by 87.7%. Sandborg et al. found that the maximum radiation dose to the eye lens during interventional neuroradiological procedures is between 289 and 515 mSv, depending on the different procedures.27 In 2012, the International Commission on Radiological Protection guidelines lowered the single-dose threshold for cataract induction from 5 to 0.5 Gy28; however, an increased cataract occurrence was also found in 8,607 Chernobyl clean-up workers, of whom most received a cumulative dose of <0.5 Gy.12 Although exact dose estimation in the present study was difficult, Sandborg et al. had concluded that the doses to the eye lens during neuro-interventional procedures might be sufficiently higher than the threshold of cataract formation. Likewise, the findings of the present retrospective study comparing an exposed group with an age-, sex-, and comorbiditymatched control group further demonstrated an increased rate of cataract occurrence in patients receiving neurointerventional procedures. Cataract formation is an age-related disease that is promoted by radiation exposure. Hence, the elderly might be more vulnerable to biochemical and biophysical changes of the lens in response to radiation exposure.29 As radiationinduced cataract formation is more common before the age of 50 years22 and the prevalence of cataracts among the Taiwanese population aged >50 years is 51%,30 the cohort of this study was limited to subjects aged <50 years.
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Table 3 Associations of risk for cataract formation due to radiation exposure by age. Age
20e29 years
n Follow-up person-months Cataract events Crude incidence rate (95% CI)a Adjusted hazard ratio (95% CI)b
30e39 years
40e49 years
Comparison
Exposure
Comparison
Exposure
Comparison
Exposure
883 73,951 3 4.06 (1.31e12.58) Reference
222 18,000 0 0.00 (0.00e16.67) -
1,055 83,746 7 8.36 (3.99e17.54) Reference
270 19,161 3 15.66 (5.05e48.55) 2.23 (0.55e8.98)
1,414 109,090 34 31.17 (22.27e43.62) Reference
346 23,880 15 62.82 (37.87e104.20) 2.14 (1.16e3.94)
a
Per 105 person-months. Adjusted for age, sex, and comorbidities (i.e., diabetes mellitus, hypertension, chronic obstructive pulmonary disease, coronary artery disease, and autoimmune disease). b
Table 4 Risk of cataract formation according to number of CT examinations.
No. of CT examinations 0 (n¼51) 1-2 (n¼624) 3-4 (n¼118) 5 (n¼45) p for the trend
aHRa
95% CI
p-Value
0.80 Reference 1.52 1.88 -
0.13e4.85 0.41e5.58 0.41e8.65 -
0.811 0.530 0.418 0.345
b
aHR, adjusted hazard ratio; CI, confidence interval. a Adjusted for age, sex, and comorbidities. b The number of CT examinations was calculated from e365 days to þ30 days from the index date.
The results of the present study showed a trend of increased risk of cataract occurrence in response to radiation exposure with increasing age, especially for subjects aged >40 years (aHR ¼ 2.14; 95% CI ¼ 1.16e3.94). These results are in accordance with the findings of a study by Chodick et al. of 35,705 radiological technologists in the US who were followed for almost 20 years. An increased risk of cataract occurrence with age per year was found both in the present study (14.7%) and that by Chodick et al. (15%)22; however, the results of the present study also indicate that radiation exposure later in life might be associated with an increased risk of cataract occurrence.23 In contrast to the study by Chodick et al., there was no incidence of cataract among subjects aged 20e29 years in the present study. This discrepancy might be due to the smaller number of subjects or the shorter follow-up time in the present study. Until now, only three population-based studies have explored the potential association between CT radiation exposure and cataract occurrence. Of these, the Beaver Dam Eye Study conducted in the US found a modest positive association,24 while the Blue Mountains Eye Study conducted in Australia found no statistically significant association between CT and cataract occurrence.25 Both of these studies used self-reported exposure to CT examinations, thus the potential bias of self-reported questionnaires should be considered. Another populated-based study conducted by the NHIRD of Taiwan found a positive dosedependent relationship between head and neck CT exposure and cataract occurrence.26 CT is an important technique to evaluate intracranial vascular anomalies and subarachnoid haemorrhage,31 and almost all subjects in
group E underwent CT examinations both before and after neuro-interventional procedures. In order to delineate the confounding effect of repeated CT examinations on cataract formation, subgroup analysis based on the number of CT studies was performed, which demonstrated a trend, but not statistically significance, of an increased risk of cataract occurrence associated with increasing CT frequency. This finding was in contrast to a report by Yuan et al. [26], which may have resulted from a discrepancy in the study design limited to the effects of CT in the exposed group. The present study had several limitations. First, diagnosis of cataract was fully dependent on ICD-9 codes, thus the severity of cataract could not be clearly identified. To improve diagnostic accuracy, only cases of cataract, as confirmed by two outpatient visits, were included for analysis; however, sampled claims data from every hospital in Taiwan are randomly checked by peer review for verification of diagnostic accuracy. Second, the NHIRD only provides information about the frequency of neurointerventional procedures and CT examinations; however, different hospitals employ different protocols and treatment strategies. Therefore, the exact radiation dose from every examination included in this study could not be determined. Hence, these data disallow a recommendation for a safe limitation of radiation exposure for neurointerventional procedures. Third, ethnic and racial disparities can affect cataract occurrence32; therefore, generalising these results to different racial groups is limited. In conclusion, as the use of neuro-interventional procedures is widespread with increasing frequency, the results of the present study offer additional information to demonstrate the long-term health issues of radiation exposure derived from brain fluoroscopic diagnostic and therapeutic interventions. This nationwide populationbased study using the Taiwan NHIRD showed a possible association between neuro-interventional procedures and cataract occurrence, as exposure to neuro-interventional procedures might be significantly associated with an increased risk of cataract occurrence, especially for patients aged >40 years. These results suggest informing patients regarding the possible cataract risk before neurointerventional procedures and also suggest the need for regular ophthalmological examinations after neurointerventional procedures to ensure early detection of cataract formation.
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K.L. Cheng et al. / Clinical Radiology xxx (2018) 1e6
Acknowledgements This study has received funding from Chung Shan Medical University, Taiwan (grant no.: CSMU-INT-104-04).
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