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Eye lens radiation exposure and repeated head CT scans: A problem to keep in mind
European Journal of Radiology 81 (2012) 1896–1900
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Eye lens radiation exposure and repeated head CT scans: A problem to keep in mind Morgane Michel a , Sophie Jacob a , Gilles Roger b , Béatrice Pelosse c , Dominique Laurier a , Hubert Ducou Le Pointe d , Marie-Odile Bernier a,∗ a
Institute for Radiological Protection and Nuclear Safety, IRSN/DRPH/SRBE/Laboratoire d’Epidémiologie, BP 17, 92 262 Fontenay-aux-Roses, France Otolaryngology Department, Trousseau Hospital, Paris, France c Ophthalmology Department, Trousseau Hospital, Paris, France d Radiology Department, Trousseau Hospital, Paris, France b
a r t i c l e
i n f o
Article history: Received 21 December 2010 Accepted 15 March 2011 Keywords: X-ray computed tomography Ionizing radiation Cataract Children
a b s t r a c t Objectives: The deterministic character of radiation-induced cataract is being called into question, raising the possibility of a risk in patients, especially children, exposed to ionizing radiation in case of repeated head CT-scans. This study aims to estimate the eye lens doses of a pediatric population exposed to repeated head CTs and to assess the feasibility of an epidemiological study. Methods: Children treated for a cholesteatoma, who had had at least one CT-scan of the middle ear before their tenth birthday, were included. Radiation exposure has been assessed from medical records and telephone interviews. Results: Out of the 39 subjects contacted, 32 accepted to participate. A total of 76 CT-scans were retrieved from medical records. At the time of the interview (mean age: 16 years), the mean number of CT per child was 3. Cumulative mean effective and eye lens doses were 1.7 mSv and 168 mGy, respectively. Conclusion: A relatively high lens radiation dose was observed in children exposed to repeated CT-scans. Due to that exposure and despite the difficulties met when trying to reach patients’ families, a large scale epidemiological study should be performed in order to assess the risk of radiation-induced cataracts associated with repeated head CT. © 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Medical exposure to ionizing radiation – most of which is for diagnostic purposes – represents 40% of the total annual radiation exposure of the public in France [1]. The number of radiological examinations has been increasing over the past few years. CT-scans, while accounting for only 10% of the X-rays examinations, take up to 50% of the collective dose [2]. They can be responsible for nonnegligible doses to radiosensitive organs. Among those, the eye is known to be sensitive to high doses of ionizing radiation which are a known risk factor for cataract along with age, ocular trauma, diabetes, long-term steroid treatment, ultraviolet exposure and smoking [3]. Current radiation protection standards formulated by the National Council on Radiation Protection (NCRP) and the International Commission on Radiological Protection (ICRP) are based on the assumption that radiationinduced cataracts fall in the class of deterministic effects and appear
∗ Corresponding author. Tel.: +33 1 58 35 72 25; fax: +33 1 46 57 03 86. E-mail address: [email protected] (M.-O. Bernier). 0720-048X/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2011.03.051
only if a threshold dose (currently considered to be of 2 Gray (Gy) in case of one exposure, 5 Gy for fractioned exposures) is exceeded [4]. However, several epidemiological and experimental studies strongly suggest a stochastic hypothesis (without a threshold effect), showing cataract formation for doses as low as 100 mGy [5]. That is the case in astronauts and pilots [6], Chernobyl cleanup workers [7], survivors of atomic bombing of Hiroshima and Nagasaki [8] and radiologic technologists [9]. Several studies have focused on children’s exposure to radiation and seem to indicate that children’s lenses are particularly sensitive to radiation effects [8,10–12]. During head CT, the absorbed radiation dose to the lens is reported to vary between 10 mGy and 60 mGy depending on the protocol and the type of machine [2,13–15]. During long-term follow-up of chronic diseases, patients – and particularly children – may be submitted to repeated head CT and therefore potentially at risk of developing radiation-induced cataracts. This study aims to describe a pediatric population exposed to repeated head CTs in a French otolaryngology department in order to characterize the target population, estimate radiation doses to the lens and to assess the methodological difficulties, which could be encountered in an epidemiological study.
M. Michel et al. / European Journal of Radiology 81 (2012) 1896–1900
2. Materials and methods 2.1. Patients Using the database of the otolaryngology department of the Trousseau children hospital (Paris, France), children who had been treated for a cholesteatoma and had been subjected to at least one head CT were included. Cholesteatoma – an abnormal growth of keratinizing squamous epithelium in the middle ear – was chosen because it does not interfere with the onset of cataract and is not associated with known risk factors of cataract: it requires neither steroid treatment nor radiotherapy and is not associated with diabetes. Furthermore, as patients often require more than one surgery to eradicate the disease or its relapses they are likely to have more than one CT-scan, and since exploring the middle ear region requires thin slices and an X-ray beam that goes straight through the eye, patients are exposed to non-negligible radiation dose to the lens. 2.2. Inclusion criteria Patients were eligible to participate in our study if they lived in France and had had one or more CT of the middle ear before their tenth birthday for a cholesteatoma or other similar disease treated in the otolaryngology department of the Trousseau hospital. The first CT-scan had had to be carried out before December 31, 2006 in order to achieve a latency of at least 3 years between the X-ray exposure and the interview. 2.3. Exclusion criteria Children with a history of congenital cataract or radiotherapy for cancer treatment were excluded. 2.4. Data collection A first contact with the parents of the eligible children was carried out via postal mail. It presented the study and its goals as well as proposed a later interview. The interview was done by phone by a medical doctor. The parents’ agreement to participate in the study was obtained and the necessary data were collected with the help of a questionnaire. The computed database of all the collected information was agreed by the Commission Nationale Informatique et Libertés (CNIL) who ensures that data privacy laws are enforced in France. One hundred and thirty-three patients were eligible (see Fig. 1). Of the 133 letters that were sent, 23 came back ‘address unknown’. Forty-four phone numbers turned out to be incorrect or disconnected. An additional 50 potential subjects could not be reached and for the most part we could not ascertain whether their phone number was correct despite the fact that none of the corresponding letters had returned. Six parents contacted our office of their own initiative. In the end we could reach 39 parents (29%) out of whom 32 accepted to answer our questions. The medical records of 25 of those children could then be obtained in order to check the information reported by the parents and extract the technical parameters of the archived head CT scans.
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The second part investigated known risk factors for cataract: prematurity, history of ocular trauma, diabetes and steroid treatment. The interview also allowed us to ask the parents whether they would be willing to let their child participate in a later epidemiological study that would assess the risk of radiation-induced cataract after head CT and require an ophthalmologic examination at the Trousseau hospital. 2.6. Determination of the radiation dose to the lens To estimate radiation exposure, we calculated both absorbed organ doses and effective dose (ED). Organ dose expresses the energy deposited to a specific organ and constitutes a rather appropriate dosimetric indicator. ED – which is usually used in the radioprotection field – is a dosimetric indicator that is thought to represent the overall health detriment to the whole body. The underlying risk coefficients (averaged over several populations of both genders and all ages) used to calculate this quantity should be taken with caution for pediatric populations. The software “CT expo” which can calculate organ doses and ED for two categories of children (babies and young children) [16] was used to estimate organ doses for each exposed patient according to several technical parameters associated with the examination. These parameters included the anatomical region of the body that was irradiated, tube voltage, current, slice thickness and type of CT machine. Parameters values were obtained either from radiological films stored in the medical files when they were available or from the specific radiological protocols of the Trousseau hospital’s radiology department. For the latter, two different CT machines were used chronologically in the department before and after April 2003. Lens dose associated with a CT-scan of the middle ear was 61 mGy and 50 mGy and ED was 0.5 and 0.6 mSv respectively for the two periods. These protocols were considered to be consistent with the usual practices in the field of pediatric radiology and those doses were then applied to the CT for which no individual data could be obtained. 3. Results 3.1. Patient characteristics Thirty-two patients treated for cholesteatoma between 1990 and 2005 were included in our study. Fifteen had been treated before 2000. Mean age at first diagnosis was 5.9 ± 1.8 years and the mean number of surgeries was 3.6 ± 1.7 (min 1–max 9). The mean age at the questionnaire time was 16.4 ± 4.3 years. The most frequently encountered risk factor for cataract development was steroid treatment which had frequently been prescribed for asthma. It was present in 16 subjects (50%) but only 4 could describe the long-term treatment (over 12 months) that can be associated with cataract. The other observed risk factors of cataract were prematurity in 1 case, ocular trauma in 2 cases and diabetes in 1 case. No child had a history of congenital cataract or radiotherapy. Out of the 32 patients, 14 (43.8%) had had other radiological exams centering on the head and neck region during childhood (in addition to the CTs). Most of these radiological examinations were orthodontics X-rays (57.1%) although 3 children had additional head CT for diseases other than their cholesteatoma.
2.5. Medical questionnaire The questionnaire was twofold. The first part focused on the exposure to ionizing radiation for medical purposes. It included the number of head CT, the date and place of the examinations and where the radiological images were archived (at home or at the hospital). We also searched for other radiological examinations of the head region.
3.2. Distribution of the number of CT-scans per patient and estimation of the cumulative dose Based on the medical files of 25 out of the 32 patients, a total of 76 head CTs were retrieved, with an average of 3.0 CTs per child. The number of CTs per child ranged from 1 to 5, with 40% who had been exposed to 4 CTs or more. Compared to the 95 head CTs reported
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M. Michel et al. / European Journal of Radiology 81 (2012) 1896–1900
133 letters sent
23 returned to sender “address unknown”
133 phone numbers called
44 wrong or
39 families contacted,
50 unreachable families, all of
disconnected numbers,
including 6 who called of
whom had supposedly
including 21 for which
their own initiative and 2
received the information
the information letter
for whom the information
letter.
had come back.
letter had come back.
-
19 treated > 2000
-
30 treated > 2000
-
25 treated < 2000
-
9 treated < 2000
-
39 treated > 2000
-
11 treated < 2000
Refusal to participate: 2 had Down syndrome 1 did not speak French fluently 1 had never had a head CT 3 gave no reason
32 answered the questionnaire Fig. 1. Participation rate.
during the interview, there was an over-declaration by the parents of the number of CTs their child had been subjected to: an additional 1.5 head CT per child was reported in the questionnaire and the divergences ranged from −2 to +8 CTs per child (see Table 1). The exclusion of the 2 patients who had 10 or more reported CT scans decreased the discrepancies between interview data and medical records, with only 0.9 additional CT scan per child reported by the parents (ranging from −2 to +5). Mean age at the first CT scan was 6.4 years. Mean delay between the first CT scan and the date of the interview was 9 years (min 4–max 18). The mean value of dose received by the lens per CT was 60 mGy, based on either individual parameters reported on the film or the radiology department’s protocol parameters, depending on which was available. The CTs performed at the Trousseau hospital were associated with a lower lens dose compared to those carried out in other hospitals (mean 53 ± 9 mGy vs. 71 ± 27 mGy respectively). Estimation of lens dose value from the radiological films could be performed for 39 CT-scans, 29 of which had been carried out at the Trousseau hospital. A comparison of the doses obtained with those individual parameters and with the radiology department’s protocols showed very similar results, with a mean
Table 1 Comparison of the number of performed CTs and doses estimates between medical files and questionnaires.
Number of head CT per child Mean ± SD Minimum–maximum Number of children exposed to 1 Head CT n (%) 2 Head CT n (%) 3 Head CT n (%) ≥ 4 Head CT n (%) Unknown n (%) Cumulative effective dose (mSv) Mean ± SD Minimum–maximum Cumulative dose to the lens (mGy) Mean ± SD Minimum–maximum Age at first CT (years) Mean ± SD Minimum–maximum
Questionnaire (N = 32)
Medical files (N = 25)
4.6 ± 3.2 1–16
3.0 ± 1.2 1–5
2 (6.4) 6 (19.4) 4 (12.9) 16 (50.0) 4 (12.9)
3 (12.0) 6 (24.0) 6 (24.0) 10 (40.0) –
2.7 ± 2.0 0.5–9.0
1.7 ± 0.7 0.5–2.8
256 ± 194 50–970
168 ± 71 50–292
6.7 ± 2.4 2.0–14.0
6.4 ± 1.9 2.8–10.7
SD: standard deviation; CT: computed tomography.
M. Michel et al. / European Journal of Radiology 81 (2012) 1896–1900
lens dose per CT of 57 mGy and 55 mGy, respectively. Between the first CT scan and the date of the interview (mean age 16 years), the mean cumulative dose to the eye lens was 168 mGy and the cumulative ED was 1.7 mSv per child. 3.3. Acceptability of the epidemiological study Out of the 32 parents and/or children (when they had reached their majority) questioned, 26 (81.3%) were potentially interested in participating in a study that would assess the relationship between X-ray exposure and cataract and would include an ophthalmologic examination. 4. Discussion This study reports estimation of radiation doses to the lens for children exposed to repeated CT of the middle ear for a cholesteatoma diagnosis. We observed a rather high number of CT-scans per child with a corresponding high eye lens dose. The mean calculated lens dose associated with an examination was 60 mGy, greater or in the range of doses reported in other studies [2,14,15]. The mean cumulative lens dose was 168 mGy, reaching 292 mGy according to the number of CTs performed by child. No previous estimation of cumulative ionizing radiation exposure in otolaryngology pediatric populations has ever been done but a few studies have looked at cumulative radiation doses from medical exposure received by children for other diagnostic purposes, although none had cataract risk in mind [17,18]. Only one study assessed the estimated lens doses from head CT in patients with shunt-treated hydrocephalus who were followed routinely by head CT-scans [18]. Each child had had an average of 10 head CT. Mean ED was 1.2 mSv and mean lens dose was 52 mGy which is inferior to what we found. That difference comes from the fact that CT-scans exploring the middle ear region lead to higher doses due to the requirement of the examination itself [19]. The values of radiation doses received by the lenses were calculated with the software CT expo [16], which allows calculating organ doses for a pediatric population. The estimation of doses was performed taking into account the technical parameters extracted from the Trousseau hospital radiology department protocol or on the individual technical parameters available on the film of the CT. A comparison of doses obtained with the protocol of Trousseau hospital and with individual parameters showed a good agreement between the two methods. This result could be explained by the good standardization of this very specific examination, but also by the fact that the majority of the examinations were performed in this hospital. The relatively high level of the mean cumulative eyes dose, raise the question of carefully estimating the benefit-risk ratio of each diagnostic CT examination and highlight the need of the procedure optimization. The level of the received doses to the lens in our study came close to what was reported in epidemiological studies focusing on the risk of lens opacities associated with radiation exposure in children [8,11,20]. In an exposed/non-exposed study on children who had been treated for facial hemangioma during their infancy, Hall et al. [11] reported a mean lens dose of 400 mGy in the exposed group who had received radiotherapy. They found an increased risk for both posterior subcapsular and cortical lens opacities in the exposed group (37% vs. 20%). Another smaller study [20] of 20 subjects who had also received radiotherapy in infancy for a facial hemangioma with mean doses to the lens on the untreated side ranging from 20 mGy to 120 mGy also found posterior subcapsular lens opacities in 13 of those subjects 30–45 years later, although it lacked a control group. Environmental studies have also looked at the risk of cataracts for low doses of ionizing radiation in children.
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Day et al. [10] studied the prevalence of lens changes in Ukrainian children living in contaminated territories around Chernobyl. They included close to 1000 exposed and non-exposed children between the age of 5 and 17 and found a significant increase in posterior subcapsular opacities in the exposed group (3.6% vs. 1.1%) but unfortunately they did not report estimated doses. In the study exploring radiation induced cataract in the survivors of Hiroshima and Nagasaki atomic bombing [8], 84% of the subjects were exposed to less than 1 Gy at the lens and mean age at exposure was 8.8 years old. This study reported a significant association between ionizing radiation and both posterior subcapsular and cortical opacities, with an Odds ratio at 1 Gy of 1.41 and 1.29 respectively. The estimated threshold was not significantly different from 0, raising the possibility that there might be no threshold. Studies among adults confirm those findings, reporting an increased risk of posterior subcapsular opacities in populations exposed to a median lens dose of 123 mGy [7]. Further investigations are still necessary in order to assess the risk of radiation-induced cataracts in case of repeated head CTs. This work allowed us to test the feasibility of such an epidemiological study. We observed that the chosen target population was of interest. Indeed, including only patients treated for cholesteatoma was a strength of our study because they had been exposed to a high number of head CT with specific radiological protocols associated with high lens doses. The patients were also very young at their first CT and had very few risk factors of cataract. The comparison of the number of CT scans obtained through phone interviews with that from medical records highlighted the over-declaration by the parents of the number of CT-scans to which their child had been subjected. A memory bias should be suspected. However, after exclusion of the 3 patients who had 10 or more reported CT scans, the discrepancies between interview data and medical records were minimized. This leads us to believe that for a later, larger study it could be more expedient to retrieve the medical files of the sole children whose parents report an abnormally high number of CT-scans. The limited number of the reached patients from the initial database remains a subject of concern. A specific effort to improve the number of contacted participants by sending a second letter at a later time, but also contacting the general practitioner of the child will be done. Pooling several national studies using the same protocol design would be of great interest to improve the number of the children included in the study and then to increase the statistical power of the analysis. Discussion at an international level is already ongoing. Including children treated for a disease other than cholesteatoma such as chronic otitis media would also be another way to have a greater number of eligible patients but the presence of other risk factors for cataract will need to be carefully assessed. No ophthalmologic examination was included in this preliminary study. Taking into account the results of this feasibility study, we plan now to launch an epidemiological study to assess the risk of lens opacities associated with exposure to head CT-scans during childhood. The design of the study will be a crosssectional study exposed/unexposed, comparing the frequency of lens opacities between a group of exposed children and a group of non-exposed children. 5. Conclusion This study showed that children subjected to repeated head CTs for a chronic otolaryngologic disease are exposed to rather high lens doses of radiation. This supports the necessity of carefully estimating the benefit-risk ratio of each CT and of optimizing the CT procedures in order to diminish doses to the lens. Moreover these findings strengthen the pertinence for a large-scale epidemiological study on the risk of cataract in patients exposed to an irradiation of the head for diagnostic purposes.
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References [1] Billon S, Morin A, Caer S, Baysson H, Gambard JP, Backe JC, et al. French population exposure to radon, terrestrial gamma and cosmic rays. Radiat Prot Dosimetry 2005;113:314–20. [2] UNSCEAR.Effects of ionizing radiation. New York: Radiation UNSCotEoA; 2006. [3] Leske MC, Chylack LT, Wu, SY. The lens opacities case–control study. Risk factors for cataract. Arch Ophthalmol 1991;109:244–51. [4] I.C.P.R. The 2007 recommendations of international commission on radiological protection. Oxford: Elsevier: PR Publication 103; 2007. [5] Ainsbury EA, Bouffler SD, Dorr W, Graf J, Muirhead CR, Edwards AA, et al. Radiation cataractogenesis: a review of recent studies. Radiat Res 2009;172:1–9. [6] Chylack LT, Peterson LE, Feiveson AH, Wear M, Manuel FK, Tung W, et al. NASA study of cataract in astronauts (NASCA). Report 1: cross-sectional study of the relationship of exposure to space radiation and risk of lens opacity. Radiat Res 2009;172:10–20. [7] Worgul BV, Kundiyev YI, Sergiyenko NM, Chumak VV, Vitte PM, Medvedovsky C, et al. Cataracts among Chernobyl clean-up workers: implications regarding permissible eye exposures. Radiat Res 2007;167:233–43. [8] Minamoto A, Taniguchi H, Yoshitani N, Mukai S, Yokoyama T, Kumagami T, et al. Cataract in atomic bomb survivors. Int J Radiat Biol 2004;80:339–45. [9] Chodick G, Bekiroglu N, Hauptmann M, Alexander BH, Freedman DM, Doody MM, et al. Risk of cataract after exposure to low doses of ionizing radiation: a 20-year prospective cohort study among US radiologic technologists. Am J Epidemiol 2008;168:620–31. [10] Day R, Gorin MB, Eller AW. Prevalence of lens changes in Ukrainian children residing around Chernobyl. Health Phys 1995;68:632–42.
[11] Hall P, Granath F, Lundell M, Olsson K, Holm LE. Lenticular opacities in individuals exposed to ionizing radiation in infancy. Radiat Res 1999;152:190–5. [12] Chen WL, Hwang JS, Hu TH, Chen MS, Chang WP. Lenticular opacities in populations exposed to chronic low-dose-rate gamma radiation from radiocontaminated buildings in Taiwan. Radiat Res 2001;156:71–7. [13] Zammit-Maempel I, Chadwick CL, Willis SP. Radiation dose to the lens of eye and thyroid gland in paranasal sinus multislice CT. Br J Radiol 2003;76:418–20. [14] Bassim MK, Ebert CS, Sit RC, Senior BA. Radiation dose to the eyes and parotids during CT of the sinuses. Otolaryngol Head Neck Surg 2005;133:531–3. [15] Yamauchi-Kawaura C, Fujii K, Aoyama T, Yamauchi M, Koyama S. Evaluation of radiation doses from MDCT-imaging in otolaryngology. Radiat Prot Dosimetry 2009;136:38–44. [16] Brix G, Lechel U, Veit R, Truckenbrodt R, Stamm G, Coppenrath EM, et al. Assessment of a theoretical formalism for dose estimation in CT: an anthropomorphic phantom study. Eur Radiol 2004;14:1275–84. [17] Donadieu J, Roudier C, Saguintaah M, Maccia C, Chiron R. Estimation of the radiation dose from thoracic CT scans in a cystic fibrosis population. Chest 2007;132:1233–8. [18] Holmedal LJ, Friberg EG, Borretzen I, Olerud H, Laegreid L, Rosendahl K. Radiation doses to children with shunt-treated hydrocephalus. Pediatr Radiol 2007;37:1209–15. [19] Kosling S, Bootz F. CT and MR imaging after middle ear surgery. Eur J Radiol 2001;40:113–8. [20] Wilde G, Sjostrand J. A clinical study of radiation cataract formation in adult life following gamma irradiation of the lens in early childhood. Br J Ophthalmol 1997;81:261–6.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Eye lens radiation exposure and repeated head CT scans: A problem to keep in mind Morgane Michel a , Sophie Jacob a , Gilles Roger b , Béatrice Pelosse c , Dominique Laurier a , Hubert Ducou Le Pointe d , Marie-Odile Bernier a,∗ a
Institute for Radiological Protection and Nuclear Safety, IRSN/DRPH/SRBE/Laboratoire d’Epidémiologie, BP 17, 92 262 Fontenay-aux-Roses, France Otolaryngology Department, Trousseau Hospital, Paris, France c Ophthalmology Department, Trousseau Hospital, Paris, France d Radiology Department, Trousseau Hospital, Paris, France b
a r t i c l e
i n f o
Article history: Received 21 December 2010 Accepted 15 March 2011 Keywords: X-ray computed tomography Ionizing radiation Cataract Children
a b s t r a c t Objectives: The deterministic character of radiation-induced cataract is being called into question, raising the possibility of a risk in patients, especially children, exposed to ionizing radiation in case of repeated head CT-scans. This study aims to estimate the eye lens doses of a pediatric population exposed to repeated head CTs and to assess the feasibility of an epidemiological study. Methods: Children treated for a cholesteatoma, who had had at least one CT-scan of the middle ear before their tenth birthday, were included. Radiation exposure has been assessed from medical records and telephone interviews. Results: Out of the 39 subjects contacted, 32 accepted to participate. A total of 76 CT-scans were retrieved from medical records. At the time of the interview (mean age: 16 years), the mean number of CT per child was 3. Cumulative mean effective and eye lens doses were 1.7 mSv and 168 mGy, respectively. Conclusion: A relatively high lens radiation dose was observed in children exposed to repeated CT-scans. Due to that exposure and despite the difficulties met when trying to reach patients’ families, a large scale epidemiological study should be performed in order to assess the risk of radiation-induced cataracts associated with repeated head CT. © 2011 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Medical exposure to ionizing radiation – most of which is for diagnostic purposes – represents 40% of the total annual radiation exposure of the public in France [1]. The number of radiological examinations has been increasing over the past few years. CT-scans, while accounting for only 10% of the X-rays examinations, take up to 50% of the collective dose [2]. They can be responsible for nonnegligible doses to radiosensitive organs. Among those, the eye is known to be sensitive to high doses of ionizing radiation which are a known risk factor for cataract along with age, ocular trauma, diabetes, long-term steroid treatment, ultraviolet exposure and smoking [3]. Current radiation protection standards formulated by the National Council on Radiation Protection (NCRP) and the International Commission on Radiological Protection (ICRP) are based on the assumption that radiationinduced cataracts fall in the class of deterministic effects and appear
∗ Corresponding author. Tel.: +33 1 58 35 72 25; fax: +33 1 46 57 03 86. E-mail address: [email protected] (M.-O. Bernier). 0720-048X/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2011.03.051
only if a threshold dose (currently considered to be of 2 Gray (Gy) in case of one exposure, 5 Gy for fractioned exposures) is exceeded [4]. However, several epidemiological and experimental studies strongly suggest a stochastic hypothesis (without a threshold effect), showing cataract formation for doses as low as 100 mGy [5]. That is the case in astronauts and pilots [6], Chernobyl cleanup workers [7], survivors of atomic bombing of Hiroshima and Nagasaki [8] and radiologic technologists [9]. Several studies have focused on children’s exposure to radiation and seem to indicate that children’s lenses are particularly sensitive to radiation effects [8,10–12]. During head CT, the absorbed radiation dose to the lens is reported to vary between 10 mGy and 60 mGy depending on the protocol and the type of machine [2,13–15]. During long-term follow-up of chronic diseases, patients – and particularly children – may be submitted to repeated head CT and therefore potentially at risk of developing radiation-induced cataracts. This study aims to describe a pediatric population exposed to repeated head CTs in a French otolaryngology department in order to characterize the target population, estimate radiation doses to the lens and to assess the methodological difficulties, which could be encountered in an epidemiological study.
M. Michel et al. / European Journal of Radiology 81 (2012) 1896–1900
2. Materials and methods 2.1. Patients Using the database of the otolaryngology department of the Trousseau children hospital (Paris, France), children who had been treated for a cholesteatoma and had been subjected to at least one head CT were included. Cholesteatoma – an abnormal growth of keratinizing squamous epithelium in the middle ear – was chosen because it does not interfere with the onset of cataract and is not associated with known risk factors of cataract: it requires neither steroid treatment nor radiotherapy and is not associated with diabetes. Furthermore, as patients often require more than one surgery to eradicate the disease or its relapses they are likely to have more than one CT-scan, and since exploring the middle ear region requires thin slices and an X-ray beam that goes straight through the eye, patients are exposed to non-negligible radiation dose to the lens. 2.2. Inclusion criteria Patients were eligible to participate in our study if they lived in France and had had one or more CT of the middle ear before their tenth birthday for a cholesteatoma or other similar disease treated in the otolaryngology department of the Trousseau hospital. The first CT-scan had had to be carried out before December 31, 2006 in order to achieve a latency of at least 3 years between the X-ray exposure and the interview. 2.3. Exclusion criteria Children with a history of congenital cataract or radiotherapy for cancer treatment were excluded. 2.4. Data collection A first contact with the parents of the eligible children was carried out via postal mail. It presented the study and its goals as well as proposed a later interview. The interview was done by phone by a medical doctor. The parents’ agreement to participate in the study was obtained and the necessary data were collected with the help of a questionnaire. The computed database of all the collected information was agreed by the Commission Nationale Informatique et Libertés (CNIL) who ensures that data privacy laws are enforced in France. One hundred and thirty-three patients were eligible (see Fig. 1). Of the 133 letters that were sent, 23 came back ‘address unknown’. Forty-four phone numbers turned out to be incorrect or disconnected. An additional 50 potential subjects could not be reached and for the most part we could not ascertain whether their phone number was correct despite the fact that none of the corresponding letters had returned. Six parents contacted our office of their own initiative. In the end we could reach 39 parents (29%) out of whom 32 accepted to answer our questions. The medical records of 25 of those children could then be obtained in order to check the information reported by the parents and extract the technical parameters of the archived head CT scans.
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The second part investigated known risk factors for cataract: prematurity, history of ocular trauma, diabetes and steroid treatment. The interview also allowed us to ask the parents whether they would be willing to let their child participate in a later epidemiological study that would assess the risk of radiation-induced cataract after head CT and require an ophthalmologic examination at the Trousseau hospital. 2.6. Determination of the radiation dose to the lens To estimate radiation exposure, we calculated both absorbed organ doses and effective dose (ED). Organ dose expresses the energy deposited to a specific organ and constitutes a rather appropriate dosimetric indicator. ED – which is usually used in the radioprotection field – is a dosimetric indicator that is thought to represent the overall health detriment to the whole body. The underlying risk coefficients (averaged over several populations of both genders and all ages) used to calculate this quantity should be taken with caution for pediatric populations. The software “CT expo” which can calculate organ doses and ED for two categories of children (babies and young children) [16] was used to estimate organ doses for each exposed patient according to several technical parameters associated with the examination. These parameters included the anatomical region of the body that was irradiated, tube voltage, current, slice thickness and type of CT machine. Parameters values were obtained either from radiological films stored in the medical files when they were available or from the specific radiological protocols of the Trousseau hospital’s radiology department. For the latter, two different CT machines were used chronologically in the department before and after April 2003. Lens dose associated with a CT-scan of the middle ear was 61 mGy and 50 mGy and ED was 0.5 and 0.6 mSv respectively for the two periods. These protocols were considered to be consistent with the usual practices in the field of pediatric radiology and those doses were then applied to the CT for which no individual data could be obtained. 3. Results 3.1. Patient characteristics Thirty-two patients treated for cholesteatoma between 1990 and 2005 were included in our study. Fifteen had been treated before 2000. Mean age at first diagnosis was 5.9 ± 1.8 years and the mean number of surgeries was 3.6 ± 1.7 (min 1–max 9). The mean age at the questionnaire time was 16.4 ± 4.3 years. The most frequently encountered risk factor for cataract development was steroid treatment which had frequently been prescribed for asthma. It was present in 16 subjects (50%) but only 4 could describe the long-term treatment (over 12 months) that can be associated with cataract. The other observed risk factors of cataract were prematurity in 1 case, ocular trauma in 2 cases and diabetes in 1 case. No child had a history of congenital cataract or radiotherapy. Out of the 32 patients, 14 (43.8%) had had other radiological exams centering on the head and neck region during childhood (in addition to the CTs). Most of these radiological examinations were orthodontics X-rays (57.1%) although 3 children had additional head CT for diseases other than their cholesteatoma.
2.5. Medical questionnaire The questionnaire was twofold. The first part focused on the exposure to ionizing radiation for medical purposes. It included the number of head CT, the date and place of the examinations and where the radiological images were archived (at home or at the hospital). We also searched for other radiological examinations of the head region.
3.2. Distribution of the number of CT-scans per patient and estimation of the cumulative dose Based on the medical files of 25 out of the 32 patients, a total of 76 head CTs were retrieved, with an average of 3.0 CTs per child. The number of CTs per child ranged from 1 to 5, with 40% who had been exposed to 4 CTs or more. Compared to the 95 head CTs reported
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133 letters sent
23 returned to sender “address unknown”
133 phone numbers called
44 wrong or
39 families contacted,
50 unreachable families, all of
disconnected numbers,
including 6 who called of
whom had supposedly
including 21 for which
their own initiative and 2
received the information
the information letter
for whom the information
letter.
had come back.
letter had come back.
-
19 treated > 2000
-
30 treated > 2000
-
25 treated < 2000
-
9 treated < 2000
-
39 treated > 2000
-
11 treated < 2000
Refusal to participate: 2 had Down syndrome 1 did not speak French fluently 1 had never had a head CT 3 gave no reason
32 answered the questionnaire Fig. 1. Participation rate.
during the interview, there was an over-declaration by the parents of the number of CTs their child had been subjected to: an additional 1.5 head CT per child was reported in the questionnaire and the divergences ranged from −2 to +8 CTs per child (see Table 1). The exclusion of the 2 patients who had 10 or more reported CT scans decreased the discrepancies between interview data and medical records, with only 0.9 additional CT scan per child reported by the parents (ranging from −2 to +5). Mean age at the first CT scan was 6.4 years. Mean delay between the first CT scan and the date of the interview was 9 years (min 4–max 18). The mean value of dose received by the lens per CT was 60 mGy, based on either individual parameters reported on the film or the radiology department’s protocol parameters, depending on which was available. The CTs performed at the Trousseau hospital were associated with a lower lens dose compared to those carried out in other hospitals (mean 53 ± 9 mGy vs. 71 ± 27 mGy respectively). Estimation of lens dose value from the radiological films could be performed for 39 CT-scans, 29 of which had been carried out at the Trousseau hospital. A comparison of the doses obtained with those individual parameters and with the radiology department’s protocols showed very similar results, with a mean
Table 1 Comparison of the number of performed CTs and doses estimates between medical files and questionnaires.
Number of head CT per child Mean ± SD Minimum–maximum Number of children exposed to 1 Head CT n (%) 2 Head CT n (%) 3 Head CT n (%) ≥ 4 Head CT n (%) Unknown n (%) Cumulative effective dose (mSv) Mean ± SD Minimum–maximum Cumulative dose to the lens (mGy) Mean ± SD Minimum–maximum Age at first CT (years) Mean ± SD Minimum–maximum
Questionnaire (N = 32)
Medical files (N = 25)
4.6 ± 3.2 1–16
3.0 ± 1.2 1–5
2 (6.4) 6 (19.4) 4 (12.9) 16 (50.0) 4 (12.9)
3 (12.0) 6 (24.0) 6 (24.0) 10 (40.0) –
2.7 ± 2.0 0.5–9.0
1.7 ± 0.7 0.5–2.8
256 ± 194 50–970
168 ± 71 50–292
6.7 ± 2.4 2.0–14.0
6.4 ± 1.9 2.8–10.7
SD: standard deviation; CT: computed tomography.
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lens dose per CT of 57 mGy and 55 mGy, respectively. Between the first CT scan and the date of the interview (mean age 16 years), the mean cumulative dose to the eye lens was 168 mGy and the cumulative ED was 1.7 mSv per child. 3.3. Acceptability of the epidemiological study Out of the 32 parents and/or children (when they had reached their majority) questioned, 26 (81.3%) were potentially interested in participating in a study that would assess the relationship between X-ray exposure and cataract and would include an ophthalmologic examination. 4. Discussion This study reports estimation of radiation doses to the lens for children exposed to repeated CT of the middle ear for a cholesteatoma diagnosis. We observed a rather high number of CT-scans per child with a corresponding high eye lens dose. The mean calculated lens dose associated with an examination was 60 mGy, greater or in the range of doses reported in other studies [2,14,15]. The mean cumulative lens dose was 168 mGy, reaching 292 mGy according to the number of CTs performed by child. No previous estimation of cumulative ionizing radiation exposure in otolaryngology pediatric populations has ever been done but a few studies have looked at cumulative radiation doses from medical exposure received by children for other diagnostic purposes, although none had cataract risk in mind [17,18]. Only one study assessed the estimated lens doses from head CT in patients with shunt-treated hydrocephalus who were followed routinely by head CT-scans [18]. Each child had had an average of 10 head CT. Mean ED was 1.2 mSv and mean lens dose was 52 mGy which is inferior to what we found. That difference comes from the fact that CT-scans exploring the middle ear region lead to higher doses due to the requirement of the examination itself [19]. The values of radiation doses received by the lenses were calculated with the software CT expo [16], which allows calculating organ doses for a pediatric population. The estimation of doses was performed taking into account the technical parameters extracted from the Trousseau hospital radiology department protocol or on the individual technical parameters available on the film of the CT. A comparison of doses obtained with the protocol of Trousseau hospital and with individual parameters showed a good agreement between the two methods. This result could be explained by the good standardization of this very specific examination, but also by the fact that the majority of the examinations were performed in this hospital. The relatively high level of the mean cumulative eyes dose, raise the question of carefully estimating the benefit-risk ratio of each diagnostic CT examination and highlight the need of the procedure optimization. The level of the received doses to the lens in our study came close to what was reported in epidemiological studies focusing on the risk of lens opacities associated with radiation exposure in children [8,11,20]. In an exposed/non-exposed study on children who had been treated for facial hemangioma during their infancy, Hall et al. [11] reported a mean lens dose of 400 mGy in the exposed group who had received radiotherapy. They found an increased risk for both posterior subcapsular and cortical lens opacities in the exposed group (37% vs. 20%). Another smaller study [20] of 20 subjects who had also received radiotherapy in infancy for a facial hemangioma with mean doses to the lens on the untreated side ranging from 20 mGy to 120 mGy also found posterior subcapsular lens opacities in 13 of those subjects 30–45 years later, although it lacked a control group. Environmental studies have also looked at the risk of cataracts for low doses of ionizing radiation in children.
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Day et al. [10] studied the prevalence of lens changes in Ukrainian children living in contaminated territories around Chernobyl. They included close to 1000 exposed and non-exposed children between the age of 5 and 17 and found a significant increase in posterior subcapsular opacities in the exposed group (3.6% vs. 1.1%) but unfortunately they did not report estimated doses. In the study exploring radiation induced cataract in the survivors of Hiroshima and Nagasaki atomic bombing [8], 84% of the subjects were exposed to less than 1 Gy at the lens and mean age at exposure was 8.8 years old. This study reported a significant association between ionizing radiation and both posterior subcapsular and cortical opacities, with an Odds ratio at 1 Gy of 1.41 and 1.29 respectively. The estimated threshold was not significantly different from 0, raising the possibility that there might be no threshold. Studies among adults confirm those findings, reporting an increased risk of posterior subcapsular opacities in populations exposed to a median lens dose of 123 mGy [7]. Further investigations are still necessary in order to assess the risk of radiation-induced cataracts in case of repeated head CTs. This work allowed us to test the feasibility of such an epidemiological study. We observed that the chosen target population was of interest. Indeed, including only patients treated for cholesteatoma was a strength of our study because they had been exposed to a high number of head CT with specific radiological protocols associated with high lens doses. The patients were also very young at their first CT and had very few risk factors of cataract. The comparison of the number of CT scans obtained through phone interviews with that from medical records highlighted the over-declaration by the parents of the number of CT-scans to which their child had been subjected. A memory bias should be suspected. However, after exclusion of the 3 patients who had 10 or more reported CT scans, the discrepancies between interview data and medical records were minimized. This leads us to believe that for a later, larger study it could be more expedient to retrieve the medical files of the sole children whose parents report an abnormally high number of CT-scans. The limited number of the reached patients from the initial database remains a subject of concern. A specific effort to improve the number of contacted participants by sending a second letter at a later time, but also contacting the general practitioner of the child will be done. Pooling several national studies using the same protocol design would be of great interest to improve the number of the children included in the study and then to increase the statistical power of the analysis. Discussion at an international level is already ongoing. Including children treated for a disease other than cholesteatoma such as chronic otitis media would also be another way to have a greater number of eligible patients but the presence of other risk factors for cataract will need to be carefully assessed. No ophthalmologic examination was included in this preliminary study. Taking into account the results of this feasibility study, we plan now to launch an epidemiological study to assess the risk of lens opacities associated with exposure to head CT-scans during childhood. The design of the study will be a crosssectional study exposed/unexposed, comparing the frequency of lens opacities between a group of exposed children and a group of non-exposed children. 5. Conclusion This study showed that children subjected to repeated head CTs for a chronic otolaryngologic disease are exposed to rather high lens doses of radiation. This supports the necessity of carefully estimating the benefit-risk ratio of each CT and of optimizing the CT procedures in order to diminish doses to the lens. Moreover these findings strengthen the pertinence for a large-scale epidemiological study on the risk of cataract in patients exposed to an irradiation of the head for diagnostic purposes.
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