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Systematic review on physician's knowledge about radiation doses and radiation risks of computed tomography
European Journal of Radiology 76 (2010) 36–41
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European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Review
Systematic review on physician’s knowledge about radiation doses and radiation risks of computed tomography Lucian Krille a,∗ , Gaël P. Hammer a,1 , Hiltrud Merzenich a,2 , Hajo Zeeb b,3 a b
Institute of Medical Biostatistics, Epidemiology and Informatics, University Medical Center, Johannes Gutenberg - University Mainz, Obere Zahlbacher Str. 69, 55131 Mainz, Germany Bremen Institute for Prevention Research and Social Medicine (BIPS), Department of Prevention and Evaluation, Linzer Straße 10, D-28359 Bremen, Germany
a r t i c l e
i n f o
Article history: Received 6 July 2010 Accepted 5 August 2010 Keywords: Computed tomography Ionizing radiation Risk Knowledge Physicians Review
a b s t r a c t Background: The frequent use of computed tomography is a major cause of the increasing medical radiation exposure of the general population. Consequently, dose reduction and radiation protection is a topic of scientific and public concern. Aim: We evaluated the available literature on physicians’ knowledge regarding radiation dosages and risks due to computed tomography. Methods: A systematic review in accordance with the Cochrane and PRISMA statements was performed using eight databases. 3091 references were found. Only primary studies assessing physicians’ knowledge about computed tomography were included. Results: 14 relevant articles were identified, all focussing on dose estimations for CT. Overall, the surveys showed moderate to low knowledge among physicians concerning radiation doses and the involved health risks. However, the surveys varied considerably in conduct and quality. For some countries, more than one survey was available. There was no general trend in knowledge in any country except a slight improvement of knowledge on health risks and radiation doses in two consecutive local German surveys. Conclusions: Knowledge gaps concerning radiation doses and associated health risks among physicians are evident from published research. However, knowledge on radiation doses cannot be interpreted as reliable indicator for good medical practice. © 2010 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Computed tomography (CT) scanners are highly valuable and sometimes life-saving tools of modern diagnostic radiology. They provide detailed information quickly—an advantage in comparison to magnetic resonance imaging, particularly in emergency or perinatal and paediatric diagnostic. However, the benefit of CT is opposed by relatively high radiation exposures to the patient [1,2]. Ionizing radiation is a known carcinogen, and cancer risks depend on factors such as the type of radiation, exposure time, irradiated tissue and age [3,4]. Children have a higher risk per unit dose because their growing tissue is more susceptible to ionisation, and they have a longer life span to develop malignancies. Brenner et al. [5] estimated for the year 2000 that from the 600,000 abdominal and head CT examinations in children under the age of 15 years in the USA, 500 fatal cancers attributable to computed tomographies will occur in these children during their lifetime.
∗ Corresponding author. Tel.: +49 6131 17 3232; fax: +49 6131 17 471643. E-mail address: [email protected] (L. Krille). 1 Tel.: +49 06131 17 3122; fax: +49 06131 17 473122. 2 Tel.: +49 06131 17 3113. 3 Tel.: +49 0421 5959621; fax: +49 0421 5959665. 0720-048X/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2010.08.025
The radiation exposure from medical procedures, particularly from CT examinations, has been a topic of recent public and scientific discussion [6,7]. In some countries, including Germany, the absolute numbers of diagnostic procedures with ionising radiation (e.g. conventional X-ray examinations) has been declining [10]. On the other hand, the use of CT examinations has increased rapidly. Due to the substantially greater doses of CT examinations compared to conventional X-rays, the medical radiation exposure per person has been increasing [10,11]. Exposure can be reduced through dose reduction strategies (machine settings) or by lowering the number of prescribed computed tomographies [8,9]. There is some evidence that radiologists generally adhere to published guidelines on dose reduction [12,13]. However, physicians’ awareness of radiation risks and knowledge of suitable alternative examinations is a major requirement to reduce CT use in patients. To further elucidate this topic, we conducted a literature-based study to elucidate knowledge on radiation risks associated with CT among physicians. 2. Aim The aim of this systematic review was to search for all available publications on surveys assessing physicians’ knowledge on
L. Krille et al. / European Journal of Radiology 76 (2010) 36–41
radiation doses and radiation risks of computed tomographies. The review should answer the following questions:
(i) Do physicians correctly estimate the radiation doses of diagnostic imaging? (ii) Are physicians aware of the influence of the technical procedure and the patient’s characteristics on radiation dose? (iii) How precisely can physicians estimate the radiation dose of different diagnostic procedures relative to each other? (iv) Are the physicians aware of possible cancer risks? (v) Do physicians routinely inform their patients about possible health risks associated with CT examinations in the long term? (vi) Is radiation awareness influenced by the physicians’ education and professional experience?
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3.3. Manual searches Manual searches of the American Journal of Roentgenology, the British Journal of Cancer, the British Medical Journal and British Journal of Radiology were done for the period from September 2008 (BJR: September 2007) until September 2009.
3.4. Data abstraction and quality scoring All articles were rated according to a subjective four-grade quality classification (flawed, weak, good, very good) by the following criteria: (i) avoidance of selection bias and interview effects, (ii) complete study description, (iii) reproducibility of the study, (iv) response rate and (v) population size. There were no definite thresholds for classification.
3. Methods
3.5. Analysis and proving of reported values
3.1. Literature search strategy
We did not conduct a meta-analysis because of strong disparities between the studies. We used information as provided in the original papers and did not perform any new calculations, e.g. percentage of correct answers. Reported doses where cited as originally written and the assignment of correct doses was not reassessed as mean doses varied for different surveys due to technological improvement in computed tomography dose reduction.
This systematic review was conducted following the recommendations of the Cochrane Handbook [14] for systematic reviews and the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement [15]. The search was performed between May and September 2009. There was no limit for the year of publication. The research question was subdivided into the three dimensions: “health personnel”, “knowledge”, “radiation” and their synonyms. These three dimensions were chosen to increase the sensitivity of the search strategy, which was purposively wider than the final inclusion criteria. The final analysis contained primary research articles on surveys measuring physician knowledge of radiation dosage and radiation risks of computed tomographies. The protocol for identifying papers was as follows: beginning with three core papers on physician’s knowledge, we analysed key elements of their titles, abstracts and keywords in light of the three dimensions and constructed a query suitable for PubMed. MeSH (Medical Subject Headings, PubMed) terms were used, but we also searched for keywords in abstracts and titles and reviewed the resulting articles. In addition, the references of the relevant articles were reviewed. Using the information from all identified titles, abstracts and keywords, new queries were iteratively compiled and executed in PubMed. Every new query was required to retrieve all previously found relevant articles. In this recursive manner, five consecutive, enhanced queries were compiled. As a further enhancement, the results of the third query were compared to a query that was independently compiled by a senior researcher; and the relevant new articles were used in compiling the fourth query. After the fourth query, exclusion criteria (no case reports; no animal studies; no mammographies) were added and the scope was narrowed to obtain the final, fifth query. The fifth query thus consisted of four parts relating to (1) radiation; (2) knowledge; (3) health personnel and (4) exclusions. The full query is displayed in Appendix A.
3.2. Databases The final query was then converted to and executed in the literature databases Web of Science, SCIRUS, EMBASE, CCMED (Current Contents Medicine), CDSR (Cochrane Database of Systematic Reviews), DARE (Cochrane Database of Abstracts of Reviews of Effectiveness) and HECLINET (Health Care Literature Information Network), resulting in two further included articles. For all included articles, referring comments and letters were also reviewed.
4. Results 4.1. Search The PubMed search returned 2661 citations. The additional searches in seven other databases provided an additional 430 citations. Among the resulting 3091 reviewed citations, 31 were classified as possibly relevant. The poor hit ratio originates from the very distinct titles, abstracts and use of keywords of the relevant articles resulting in a necessarily very broad search strategy. One article was excluded because it contained no reference to radiation [30], another excluded survey assessed the attitude, but not knowledge on radiation [31], three were excluded because of their publication type [32–34], eight articles did not consider the radiation of computed tomographies [31,35–41] and seven surveys did not aim at physicians [31,35,39,40,42–44]. Two very brief articles [45,46] could not be classified due to missing abstracts and inaccessible content. The reviewed comments and letters revealed no further information. The manual searches delivered no new citations. Finally, 14 papers [16–29] matched the inclusion criteria and were considered for a detailed review. Twelve of the included fourteen articles were found in PubMed. The detailed distribution of citation matches, included articles per database and query is shown in Table 1.
4.2. Conduct of the surveys All articles describe surveys conducted in Europe, Turkey, Israel or North America in the period 1996–2009. The surveys were very heterogeneous. Their designs included face-to-face, written and online surveys. The number of interviewed persons ranged from 68 to 313; the response rates ranged from 20% to 96%. Three articles were rated as weak, five as good and six as very good. Different groups of physicians were interviewed. An overview is presented in Table 2. All included surveys used effective doses except the one by Quinn [27], who used equivalent doses. Doses were never asked to be estimated as distinct values but in terms of ranges or equivalents.
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L. Krille et al. / European Journal of Radiology 76 (2010) 36–41
Table 1 Details of performed searches. Query
Website
Database
Date of execution
Raw hits
New hits
New publications to be included
1 2 3 SRa 4 5 5a 5a 5a 5a 5a 5a 5a Totals
PubMed PubMed PubMed PubMed PubMed PubMed ISI SCIRUS Medpilot Medpilot Medpilot Medpilot Medpilot
Medline Medline Medline Medline Medline Medline Web of Science SCIRUS EMBASE CCMED CDSR DARE HECLINET
2009-05-07 2009-05-11 2009-05-20 2009-06-18 2009-07-14 2009-08-28 2009-09-03 2009-09-03 2009-09-03 2009-09-03 2009-09-03 2009-09-03 2009-09-03
33 244 725 1781 745 608 368 84 22 0 0 0 0
33 211 609 1504 5 299 343 73 14 0 0 0 0 3091
8 2 0 1 1 0 1 1 0 0 0 0 0 14
CCMED, Current Contents Medicine; CDSR, Cochrane Database of Systematic Reviews; DARE, Cochrane Database of Abstracts of Reviews of Effectiveness; HECLINET, Health Care Literature Information Network. a Senior researcher.
4.3. Dose estimations Regarding the dose estimations, incorrect answers can be classified as underestimation or overestimation. Overestimation may lead to fewer referrals for CT examinations due to radiation protection, whereby underestimation of dose may increase CT indications. A common reference dose is that of conventional chest radiograph in adults. Knowledge of dose was evaluated in four English [17,22,26,29] and two German [18,21] surveys, one focussing on hospital physicians, the other on paediatricians in practices and hospitals. In the United Kingdom (UK) the dose of a conventional adult chest radiograph was estimated correctly by 22–24% of all physicians [22,29]; however, no participant in the study conducted by Shiralkar et al. in the UK estimated the dose correctly [26]. The German studies were performed consecutively in the same study region, with increasing proportions of correct answers in all categories. In the latest German survey [18], 59% of participants correctly estimated the dose of an adult chest radiograph, with only 5% underestimating it. Concerning paediatric chest radiographs, the proportion of correct answers was somewhat lower (52%), and the proportion of underestimations was higher (29%), while for a standard adult CT examination, only 41% estimated the dose correctly, and 28% underestimated it. Grooves et al. reported similar proportions in the UK [17]. The dose from paediatric CT examinations was estimated correctly by 35% of participants in a survey of registered paediatricians
in Germany [18]. The lower proportion of correct answers is accompanied by a significantly higher proportion of underestimations regarding CT doses: 56% of participants underestimated the radiation dose resulting from paediatric CT examinations. In the UK, about 7% of survey participants estimated this dose correctly [17]. 4.4. Equivalents and relations In most surveys, the physicians were asked to estimate the dose of a procedure equivalent to a standard adult chest radiograph [16,18–29]. Irrespective of the quality or design of the survey, the proportions of correct equivalence estimations ranged from 1% in Canada [23] to 22% in the USA [24]. The proportion of physicians underestimating CT doses ranges from 60% up to 87% as shown in Table 3. One study evaluated relative doses in terms of higher, equal or lower. 11% of participants incorrectly answered that a standard adult CT chest examination leads to a lower dose than a standard adult radiograph [21]. In this study, the relation between the doses of a standard adult chest CT examination and a paediatric CT chest examination was only known to 42% of respondents. 4.5. Non-radiating examinations Six studies [20,22,23,25,26,29] included a question on radiation exposure from ultrasonography. Between 4% and 24% of the participating physicians thought ultrasound (US) was an examination using ionizing radiation. Similarly, 11–28% thought that magnetic
Table 2 Characteristics of included surveys. First author
Year of publication
Survey conduct
Unclear conduct
Arslanoglu [25] Gumus [20] Groves [17] Jacob [29] Heyer [21] Heyer [18] Lee [24] b Lee [24] c Quinn [27] Rassin [16] Renston [28] Rice [19] Shiralkar [26] Soye [22] Thomas [23]
2007 2008 2006 2004 2006 2009 2004 2004 1997 2005 1996 2007 2008 2008 2006
Written Written Face-to-face Written Written Written Written Written Written Written Written Online Written Written Written
Yes
a b c
3 = weak; 2 = good; 1 = very good. Emergency doctors. Radiologists.
Yes
Yes Yes
Yes
Researcher present Yes Yes Yes Yes
Response rate (%)
Interviewed subjects
Country
Qualitya
? 42 80 64 96 76 ? ? 76 76 32 20 ? 31 40
117 102 161 240 124 137 45 39 120 68 313 147 130 153 220
Turkey Turkey England England Germany Germany USA USA England Israel USA USA England England Canada
3 3 1 2 1 1 2 2 2 3 1 1 3 2 1
Table 3 Ionizing radiation knowledge regarding doses and applications among physicians; percentage of correct answers per topic. First author
Arslanoglu [25] Gumus [20] Groves [17] Heyer [21] Heyer [18] Jacob [29] Leea [24] Leeb [24] Quinn [27] Rassin [16] Renston [28] Rice [19] Shiralkar [26]
Soye [22] Thomas [23]
Year Number interviewed Dose equivalent: CT vs. chest radiograph: % correct answers Dose equivalent: CT vs. chest radiograph: % underestimations Dose equivalent: ST vs. chest radiograph: % underestimations Dose relation: CT vs. chest radiograph: % correct answers Dose relation: CT vs. chest radiograph: % underestimations Dose relation: adult vs. child % correct answers Dose relation: adult vs. child % underestimations US and ionizing radiation, % false answers MRI and ionizing radiation, % false answers % confirming risk increase % correctly estimated risk increase % communicating risks and benefits Positive influence of course attendance on overall knowledge found
2007 117 8,2
2008 102 17
2008 153
83
73
2006 161
2006 124
2009 137
2003 240 18
2004 39 13
74
76
1997 120 9 60
2005 68
1996 313
2007 147 19
62
93
76
∼70
93.1
2008 130 6
2006 220 1-13 99-87
97
63-94
89 12
42 58 4
24
11
22
10 8.4
14
52 16
28 12.5
No
23
Yes
9
47
22
15
70
53 31
5
10
8
20
4
19
23 No
Yes
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2004 45 22
No
US, ultrasound; MRI, magnetic resonance imaging. a Emergency doctors. b Radiologists.
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L. Krille et al. / European Journal of Radiology 76 (2010) 36–41
resonance imaging (MRI) emits ionizing radiation, as reported by seven studies [18,20–22,25,26,29]. Again, the responses vary by year of publication, country, study design and study quality. In contrast to the higher proportion of correct dose estimations in the second of the two consecutive German studies, the proportion of correct responses concerning MRI as not involving ionizing radiation decreased from 2006 to 2009 [18,21]. 4.6. Risk awareness and risk communication In seven surveys, the physicians were asked if a single exposure to ionizing radiation due to a CT examination would increase the lifetime cancer risk. In one survey [16], 70% correctly confirmed that there is a small risk increase. In three other surveys [19,20,24], this figure was somewhat lower. A very low number of correct answers (2.5%) were reported from three further surveys [22,24,29]. Lee et al. [24] interviewed radiologists and emergency doctors. Of the radiologists, 47% confirmed a risk increase while only 9% of the emergency doctors did so. Two investigators also asked respondents to quantify the risk increase. While every second physician was aware of the risk increase in these studies, some 31% [19] and 16% [20] were able to give a correct approximation of the risk increase. In the study by Shiralkar et al. [26], 53% of participants were aware of a risk increase. However, only 23% of all doctors informed the patients about benefits and risks of the examination. Despite the fact that only 9% of the emergency physicians interviewed by Lee et al. were aware of a risk increase, 22% of them stated that they were speaking about CT risks and benefits with the patients [24]. The radiologists from the same survey, of whom 47% were aware of a risk increase, informed their patients less frequently (15%) [24]. 4.7. Influence of education and experience Nine surveys considered at least one possible influencing factor for knowledge. However, no significant influence was found concerning type of education [17,21,24] or speciality [21]. Neither the type of workplace [17] nor the duration of professional experience [18,19,21,24] was associated with reported knowledge. Attendance of a radiation protection course positively influenced overall knowledge in two [22,29] out of five [18,23,27] surveys. 5. Discussion We performed a broad systematic literature review in eight databases, resulting in 3091 articles. 14 primary research articles on physicians’ knowledge of radiation dose from computed tomography and other diagnostic procedures and associated risks were included in our final analysis. A common finding was a moderate, in some cases even low level of knowledge and radiation risk awareness. The included surveys varied markedly in design and study conduct. Four surveys were performed as face-to-face interviews. In such “direct” interviews, the answers reflect the current knowledge of the interviewees. Ten surveys used written questionnaires. This approach allows the respondents to gather some information before answering the survey questions. Finally, three investigations combined both methods. In several studies, the methods were not fully described. Furthermore, the detailed survey questions varied considerably. Most surveys concentrated on dose estimations, but used different approaches and focused on a varying range of procedures or patients. Comparisons are therefore hampered, and only broad conclusions can be drawn. Another limitation arises from the low numbers of interviewed persons in the single surveys.
The results may be confounded as all published studies tend to use different questions and different bench-marks. Considerable differences in medical and educational practices as well as health systems issues exist between the various countries. In addition, average effective doses for different examinations may vary between countries, which makes overall judgements using a common standard difficult. Interestingly, the publications covered the years 1996 and 2004–2009 only, with a gap between 1997 and 2004. Possibly, the article by Brenner et al. in 2001 [5] stimulated the discussion on health risks due to computed tomography. The surveys after 2004 focused on CT and radiation dosage and might be motivated by the increased scientific interest. The two surveys before 1997 addressed computed tomographies only among other radiological examinations. In Germany, an increase in awareness was noted in the two consecutive studies in the same study region. Overall, the reports from Germany showed higher proportions of correct answers compared to those from the other countries. However, only a few questions are directly comparable with other surveys (Table 3). The awareness of the ongoing survey among the target population (hospital physicians) may have contributed to these results. The second German survey was performed in the same geographical region, and aimed at paediatricians outside and inside hospitals, who may have been informed about the earlier investigation. Additionally one may assume a priori higher awareness among paediatricians concerning radiation risks of children. The overall relatively poor results concerning knowledge of radiation exposure and risk awareness are difficult to interpret. No trends over time were discernible in any country but Germany. All other successive surveys were not conducted in the same region, and differed in terms of methodology, limiting comparability. The findings must therefore be interpreted with caution and may only be seen as rough indicators for medical CT related practice. Our study questions focussed on physicians’ knowledge of radiation doses and related risks. Most of the identified surveys evaluated knowledge on doses in quantitative numerical terms. From the perspective of radiation protection, the underlying rationale would be to assume that good knowledge about medical radiation risks leads to fewer CT indications and reduced radiation exposure in children. However, this assumption can be questioned. The review has shown that a better knowledge about the radiation doses does not necessarily imply a reduced CT use in the diagnostic process. Additionally, knowledge evaluation by asking for quantitative numerical terms may be criticised. Accordingly it might be more appropriate to obtain information on issues such as the knowledge of recommended primary examinations, given a specified case scenario. We are currently conducting a survey among physicians which includes such an approach.
6. Conclusions We conducted a systematic literature review to include all available information on physicians’ knowledge about CT radiation doses and associated health risks. Only a minority of physicians were well informed about these topics in almost all studies we found. However the different methodologies of the 14 included studies render an interpretation difficult. Nevertheless, this systematic review implies that radiation protection awareness among physicians particularly for CT could be improved.
Competing interests The authors declare no competing interest.
L. Krille et al. / European Journal of Radiology 76 (2010) 36–41
Appendix A. Fifth and final query for medline (“radiation”[TI] OR “Radiation Dosage”[Mesh Terms] OR “Radiation, Ionizing”[Mesh Terms] OR “Tomography, X-Ray Computed”[Mesh Terms] OR “Diagnostic Imaging”[Mesh Terms]) AND (“awareness”[TI] OR “knowledge”[TI] OR “knowledge”[Mesh Terms] OR “Awareness”[Mesh Terms] OR “Health Knowledge, Attitudes, Practice”[Mesh Terms] OR “Clinical Competence”[Mesh Terms]) AND (“physicians”’[TIAB] OR “physicians”[TIAB] OR “physician”[TIAB] OR “radiologists”’[TIAB] OR “radiologists”[TIAB] OR “radiologist”[TIAB] OR “doctors”’[TIAB] OR “doctors”[TIAB] OR “doctor”[TIAB] OR “paediatricians”’[TIAB] OR “paediatricians”[TIAB] OR “paediatrician”[TIAB] OR “pediatricians”’[TIAB] OR “pediatricians”[TIAB] OR “pediatrician”[TIAB] OR “Physicians”[MeSH Terms]) NOT (“Case Study”[TI] OR “Case Report”[TI] OR “Case Studies”[TI] OR “Case Histories”[TI] OR “case reports” [Publication Type] OR “News” [Publication Type] OR “Review”[PT]) NOT (“animals”[mh] NOT (“humans”[mh] and “animals”[mh])) NOT mammogra*[TI] References [1] Mettler FA, Wiest PW, Locken JA, Kelsey CA. CT scanning: patterns of use and dose. J Radiol Prot 2000;20:353–9. [2] Shrimpton PC, Hillier MC, Lewis MA, Dunn M. National survey of doses from CT in the UK: 2003. Br J Radiol 2006;79:968–80. [3] Monson RR, Cleaver JE, Abrams HL, et al. Health risks from exposure to low levels of ionizing radiation (BEIR VII-Phase 2). Washington, DC: The National Academies Press; 2006. [4] UNSCEAR (United Nations Scientific Committee on the Effects of Atomic Radiation). Sources and effects of ionizing radiation (volume II: effects). Vienna: United Nations; 2000. [5] Brenner DJ, Elliston CD, Hall EJ, Berdon WE. Estimated risks of radiation-induced fatal cancer from pediatric CT. Am J Roentgenol 2001;176:289–96. [6] Rehani MM, Berry M. Radiation doses in computed tomography. The increasing doses of radiation need to be controlled. Br Med J 2000;320:593–4. [7] Heyer CM, Peters S, Lemburg S. Structure of the meeting of the German radiological society and scientific discourse pertaining to radiation dose and dose reduction: an analysis of 1998–2008. Rofo 2009;181:1065–72. [8] Berdon EW, Brenner DJ, Brody AJ, et al. The ALARA (as low as reasonably achievable) concept in pediatric CT intelligent dose reduction. Pediatr Radiol 2002;32:217–313. [9] Shah NB, Platt SL. ALARA: is there a cause for alarm? Reducing radiation risks from computed tomography scanning in children. Curr Opin Pediatr 2008;20:243–7. [10] Bundesministerium für Umwelt, Naturschutz, Reaktorsicherheit. Umweltradioaktivität und Strahlenbelastung im Jahr 2007. Berlin: Bundesregierung Deutschland; 2008. [11] Aldrich J, Hufton A, Kalra MK, et al. Dose reduction in CT while maintaining diagnostic confidence: a feasibility/demonstration study. Vienna: International Atomic Energy Agency; 2009. [12] Galanski M, Nagel H, Stamm G. Paediatrische CT-Expositionspraxis in der BRD: Ergebnisse 2005/06. Hannover: Medizinische Hochschule Hannover; 2006. [13] Galanski M, Nagel HD, Stamm G. CT-Expositionspraxis in der Bundesrepublik Deutschland: Ergebnisse 1999. Frankfurt: Zentralverband Elektrotechnik und Elektroindustrie (ZVEI); 2000. [14] Higgins J, Green S. Cochrane handbook for systematic reviews of intervention (version 5.0.1.). Oxford: The Cochrane Collaboration; 2008. [15] Moher D, Liberati A, Tetzlaff J, Altman DG, for the PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009;62:1006–12. [16] Rassin M, Granat P, Berger M, Silner D. Attitude and knowledge of physicians and nurses about ionizing radiation. J Rad Nur 2005;24:26–30.
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European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Review
Systematic review on physician’s knowledge about radiation doses and radiation risks of computed tomography Lucian Krille a,∗ , Gaël P. Hammer a,1 , Hiltrud Merzenich a,2 , Hajo Zeeb b,3 a b
Institute of Medical Biostatistics, Epidemiology and Informatics, University Medical Center, Johannes Gutenberg - University Mainz, Obere Zahlbacher Str. 69, 55131 Mainz, Germany Bremen Institute for Prevention Research and Social Medicine (BIPS), Department of Prevention and Evaluation, Linzer Straße 10, D-28359 Bremen, Germany
a r t i c l e
i n f o
Article history: Received 6 July 2010 Accepted 5 August 2010 Keywords: Computed tomography Ionizing radiation Risk Knowledge Physicians Review
a b s t r a c t Background: The frequent use of computed tomography is a major cause of the increasing medical radiation exposure of the general population. Consequently, dose reduction and radiation protection is a topic of scientific and public concern. Aim: We evaluated the available literature on physicians’ knowledge regarding radiation dosages and risks due to computed tomography. Methods: A systematic review in accordance with the Cochrane and PRISMA statements was performed using eight databases. 3091 references were found. Only primary studies assessing physicians’ knowledge about computed tomography were included. Results: 14 relevant articles were identified, all focussing on dose estimations for CT. Overall, the surveys showed moderate to low knowledge among physicians concerning radiation doses and the involved health risks. However, the surveys varied considerably in conduct and quality. For some countries, more than one survey was available. There was no general trend in knowledge in any country except a slight improvement of knowledge on health risks and radiation doses in two consecutive local German surveys. Conclusions: Knowledge gaps concerning radiation doses and associated health risks among physicians are evident from published research. However, knowledge on radiation doses cannot be interpreted as reliable indicator for good medical practice. © 2010 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Computed tomography (CT) scanners are highly valuable and sometimes life-saving tools of modern diagnostic radiology. They provide detailed information quickly—an advantage in comparison to magnetic resonance imaging, particularly in emergency or perinatal and paediatric diagnostic. However, the benefit of CT is opposed by relatively high radiation exposures to the patient [1,2]. Ionizing radiation is a known carcinogen, and cancer risks depend on factors such as the type of radiation, exposure time, irradiated tissue and age [3,4]. Children have a higher risk per unit dose because their growing tissue is more susceptible to ionisation, and they have a longer life span to develop malignancies. Brenner et al. [5] estimated for the year 2000 that from the 600,000 abdominal and head CT examinations in children under the age of 15 years in the USA, 500 fatal cancers attributable to computed tomographies will occur in these children during their lifetime.
∗ Corresponding author. Tel.: +49 6131 17 3232; fax: +49 6131 17 471643. E-mail address: [email protected] (L. Krille). 1 Tel.: +49 06131 17 3122; fax: +49 06131 17 473122. 2 Tel.: +49 06131 17 3113. 3 Tel.: +49 0421 5959621; fax: +49 0421 5959665. 0720-048X/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2010.08.025
The radiation exposure from medical procedures, particularly from CT examinations, has been a topic of recent public and scientific discussion [6,7]. In some countries, including Germany, the absolute numbers of diagnostic procedures with ionising radiation (e.g. conventional X-ray examinations) has been declining [10]. On the other hand, the use of CT examinations has increased rapidly. Due to the substantially greater doses of CT examinations compared to conventional X-rays, the medical radiation exposure per person has been increasing [10,11]. Exposure can be reduced through dose reduction strategies (machine settings) or by lowering the number of prescribed computed tomographies [8,9]. There is some evidence that radiologists generally adhere to published guidelines on dose reduction [12,13]. However, physicians’ awareness of radiation risks and knowledge of suitable alternative examinations is a major requirement to reduce CT use in patients. To further elucidate this topic, we conducted a literature-based study to elucidate knowledge on radiation risks associated with CT among physicians. 2. Aim The aim of this systematic review was to search for all available publications on surveys assessing physicians’ knowledge on
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radiation doses and radiation risks of computed tomographies. The review should answer the following questions:
(i) Do physicians correctly estimate the radiation doses of diagnostic imaging? (ii) Are physicians aware of the influence of the technical procedure and the patient’s characteristics on radiation dose? (iii) How precisely can physicians estimate the radiation dose of different diagnostic procedures relative to each other? (iv) Are the physicians aware of possible cancer risks? (v) Do physicians routinely inform their patients about possible health risks associated with CT examinations in the long term? (vi) Is radiation awareness influenced by the physicians’ education and professional experience?
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3.3. Manual searches Manual searches of the American Journal of Roentgenology, the British Journal of Cancer, the British Medical Journal and British Journal of Radiology were done for the period from September 2008 (BJR: September 2007) until September 2009.
3.4. Data abstraction and quality scoring All articles were rated according to a subjective four-grade quality classification (flawed, weak, good, very good) by the following criteria: (i) avoidance of selection bias and interview effects, (ii) complete study description, (iii) reproducibility of the study, (iv) response rate and (v) population size. There were no definite thresholds for classification.
3. Methods
3.5. Analysis and proving of reported values
3.1. Literature search strategy
We did not conduct a meta-analysis because of strong disparities between the studies. We used information as provided in the original papers and did not perform any new calculations, e.g. percentage of correct answers. Reported doses where cited as originally written and the assignment of correct doses was not reassessed as mean doses varied for different surveys due to technological improvement in computed tomography dose reduction.
This systematic review was conducted following the recommendations of the Cochrane Handbook [14] for systematic reviews and the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement [15]. The search was performed between May and September 2009. There was no limit for the year of publication. The research question was subdivided into the three dimensions: “health personnel”, “knowledge”, “radiation” and their synonyms. These three dimensions were chosen to increase the sensitivity of the search strategy, which was purposively wider than the final inclusion criteria. The final analysis contained primary research articles on surveys measuring physician knowledge of radiation dosage and radiation risks of computed tomographies. The protocol for identifying papers was as follows: beginning with three core papers on physician’s knowledge, we analysed key elements of their titles, abstracts and keywords in light of the three dimensions and constructed a query suitable for PubMed. MeSH (Medical Subject Headings, PubMed) terms were used, but we also searched for keywords in abstracts and titles and reviewed the resulting articles. In addition, the references of the relevant articles were reviewed. Using the information from all identified titles, abstracts and keywords, new queries were iteratively compiled and executed in PubMed. Every new query was required to retrieve all previously found relevant articles. In this recursive manner, five consecutive, enhanced queries were compiled. As a further enhancement, the results of the third query were compared to a query that was independently compiled by a senior researcher; and the relevant new articles were used in compiling the fourth query. After the fourth query, exclusion criteria (no case reports; no animal studies; no mammographies) were added and the scope was narrowed to obtain the final, fifth query. The fifth query thus consisted of four parts relating to (1) radiation; (2) knowledge; (3) health personnel and (4) exclusions. The full query is displayed in Appendix A.
3.2. Databases The final query was then converted to and executed in the literature databases Web of Science, SCIRUS, EMBASE, CCMED (Current Contents Medicine), CDSR (Cochrane Database of Systematic Reviews), DARE (Cochrane Database of Abstracts of Reviews of Effectiveness) and HECLINET (Health Care Literature Information Network), resulting in two further included articles. For all included articles, referring comments and letters were also reviewed.
4. Results 4.1. Search The PubMed search returned 2661 citations. The additional searches in seven other databases provided an additional 430 citations. Among the resulting 3091 reviewed citations, 31 were classified as possibly relevant. The poor hit ratio originates from the very distinct titles, abstracts and use of keywords of the relevant articles resulting in a necessarily very broad search strategy. One article was excluded because it contained no reference to radiation [30], another excluded survey assessed the attitude, but not knowledge on radiation [31], three were excluded because of their publication type [32–34], eight articles did not consider the radiation of computed tomographies [31,35–41] and seven surveys did not aim at physicians [31,35,39,40,42–44]. Two very brief articles [45,46] could not be classified due to missing abstracts and inaccessible content. The reviewed comments and letters revealed no further information. The manual searches delivered no new citations. Finally, 14 papers [16–29] matched the inclusion criteria and were considered for a detailed review. Twelve of the included fourteen articles were found in PubMed. The detailed distribution of citation matches, included articles per database and query is shown in Table 1.
4.2. Conduct of the surveys All articles describe surveys conducted in Europe, Turkey, Israel or North America in the period 1996–2009. The surveys were very heterogeneous. Their designs included face-to-face, written and online surveys. The number of interviewed persons ranged from 68 to 313; the response rates ranged from 20% to 96%. Three articles were rated as weak, five as good and six as very good. Different groups of physicians were interviewed. An overview is presented in Table 2. All included surveys used effective doses except the one by Quinn [27], who used equivalent doses. Doses were never asked to be estimated as distinct values but in terms of ranges or equivalents.
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Table 1 Details of performed searches. Query
Website
Database
Date of execution
Raw hits
New hits
New publications to be included
1 2 3 SRa 4 5 5a 5a 5a 5a 5a 5a 5a Totals
PubMed PubMed PubMed PubMed PubMed PubMed ISI SCIRUS Medpilot Medpilot Medpilot Medpilot Medpilot
Medline Medline Medline Medline Medline Medline Web of Science SCIRUS EMBASE CCMED CDSR DARE HECLINET
2009-05-07 2009-05-11 2009-05-20 2009-06-18 2009-07-14 2009-08-28 2009-09-03 2009-09-03 2009-09-03 2009-09-03 2009-09-03 2009-09-03 2009-09-03
33 244 725 1781 745 608 368 84 22 0 0 0 0
33 211 609 1504 5 299 343 73 14 0 0 0 0 3091
8 2 0 1 1 0 1 1 0 0 0 0 0 14
CCMED, Current Contents Medicine; CDSR, Cochrane Database of Systematic Reviews; DARE, Cochrane Database of Abstracts of Reviews of Effectiveness; HECLINET, Health Care Literature Information Network. a Senior researcher.
4.3. Dose estimations Regarding the dose estimations, incorrect answers can be classified as underestimation or overestimation. Overestimation may lead to fewer referrals for CT examinations due to radiation protection, whereby underestimation of dose may increase CT indications. A common reference dose is that of conventional chest radiograph in adults. Knowledge of dose was evaluated in four English [17,22,26,29] and two German [18,21] surveys, one focussing on hospital physicians, the other on paediatricians in practices and hospitals. In the United Kingdom (UK) the dose of a conventional adult chest radiograph was estimated correctly by 22–24% of all physicians [22,29]; however, no participant in the study conducted by Shiralkar et al. in the UK estimated the dose correctly [26]. The German studies were performed consecutively in the same study region, with increasing proportions of correct answers in all categories. In the latest German survey [18], 59% of participants correctly estimated the dose of an adult chest radiograph, with only 5% underestimating it. Concerning paediatric chest radiographs, the proportion of correct answers was somewhat lower (52%), and the proportion of underestimations was higher (29%), while for a standard adult CT examination, only 41% estimated the dose correctly, and 28% underestimated it. Grooves et al. reported similar proportions in the UK [17]. The dose from paediatric CT examinations was estimated correctly by 35% of participants in a survey of registered paediatricians
in Germany [18]. The lower proportion of correct answers is accompanied by a significantly higher proportion of underestimations regarding CT doses: 56% of participants underestimated the radiation dose resulting from paediatric CT examinations. In the UK, about 7% of survey participants estimated this dose correctly [17]. 4.4. Equivalents and relations In most surveys, the physicians were asked to estimate the dose of a procedure equivalent to a standard adult chest radiograph [16,18–29]. Irrespective of the quality or design of the survey, the proportions of correct equivalence estimations ranged from 1% in Canada [23] to 22% in the USA [24]. The proportion of physicians underestimating CT doses ranges from 60% up to 87% as shown in Table 3. One study evaluated relative doses in terms of higher, equal or lower. 11% of participants incorrectly answered that a standard adult CT chest examination leads to a lower dose than a standard adult radiograph [21]. In this study, the relation between the doses of a standard adult chest CT examination and a paediatric CT chest examination was only known to 42% of respondents. 4.5. Non-radiating examinations Six studies [20,22,23,25,26,29] included a question on radiation exposure from ultrasonography. Between 4% and 24% of the participating physicians thought ultrasound (US) was an examination using ionizing radiation. Similarly, 11–28% thought that magnetic
Table 2 Characteristics of included surveys. First author
Year of publication
Survey conduct
Unclear conduct
Arslanoglu [25] Gumus [20] Groves [17] Jacob [29] Heyer [21] Heyer [18] Lee [24] b Lee [24] c Quinn [27] Rassin [16] Renston [28] Rice [19] Shiralkar [26] Soye [22] Thomas [23]
2007 2008 2006 2004 2006 2009 2004 2004 1997 2005 1996 2007 2008 2008 2006
Written Written Face-to-face Written Written Written Written Written Written Written Written Online Written Written Written
Yes
a b c
3 = weak; 2 = good; 1 = very good. Emergency doctors. Radiologists.
Yes
Yes Yes
Yes
Researcher present Yes Yes Yes Yes
Response rate (%)
Interviewed subjects
Country
Qualitya
? 42 80 64 96 76 ? ? 76 76 32 20 ? 31 40
117 102 161 240 124 137 45 39 120 68 313 147 130 153 220
Turkey Turkey England England Germany Germany USA USA England Israel USA USA England England Canada
3 3 1 2 1 1 2 2 2 3 1 1 3 2 1
Table 3 Ionizing radiation knowledge regarding doses and applications among physicians; percentage of correct answers per topic. First author
Arslanoglu [25] Gumus [20] Groves [17] Heyer [21] Heyer [18] Jacob [29] Leea [24] Leeb [24] Quinn [27] Rassin [16] Renston [28] Rice [19] Shiralkar [26]
Soye [22] Thomas [23]
Year Number interviewed Dose equivalent: CT vs. chest radiograph: % correct answers Dose equivalent: CT vs. chest radiograph: % underestimations Dose equivalent: ST vs. chest radiograph: % underestimations Dose relation: CT vs. chest radiograph: % correct answers Dose relation: CT vs. chest radiograph: % underestimations Dose relation: adult vs. child % correct answers Dose relation: adult vs. child % underestimations US and ionizing radiation, % false answers MRI and ionizing radiation, % false answers % confirming risk increase % correctly estimated risk increase % communicating risks and benefits Positive influence of course attendance on overall knowledge found
2007 117 8,2
2008 102 17
2008 153
83
73
2006 161
2006 124
2009 137
2003 240 18
2004 39 13
74
76
1997 120 9 60
2005 68
1996 313
2007 147 19
62
93
76
∼70
93.1
2008 130 6
2006 220 1-13 99-87
97
63-94
89 12
42 58 4
24
11
22
10 8.4
14
52 16
28 12.5
No
23
Yes
9
47
22
15
70
53 31
5
10
8
20
4
19
23 No
Yes
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2004 45 22
No
US, ultrasound; MRI, magnetic resonance imaging. a Emergency doctors. b Radiologists.
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resonance imaging (MRI) emits ionizing radiation, as reported by seven studies [18,20–22,25,26,29]. Again, the responses vary by year of publication, country, study design and study quality. In contrast to the higher proportion of correct dose estimations in the second of the two consecutive German studies, the proportion of correct responses concerning MRI as not involving ionizing radiation decreased from 2006 to 2009 [18,21]. 4.6. Risk awareness and risk communication In seven surveys, the physicians were asked if a single exposure to ionizing radiation due to a CT examination would increase the lifetime cancer risk. In one survey [16], 70% correctly confirmed that there is a small risk increase. In three other surveys [19,20,24], this figure was somewhat lower. A very low number of correct answers (2.5%) were reported from three further surveys [22,24,29]. Lee et al. [24] interviewed radiologists and emergency doctors. Of the radiologists, 47% confirmed a risk increase while only 9% of the emergency doctors did so. Two investigators also asked respondents to quantify the risk increase. While every second physician was aware of the risk increase in these studies, some 31% [19] and 16% [20] were able to give a correct approximation of the risk increase. In the study by Shiralkar et al. [26], 53% of participants were aware of a risk increase. However, only 23% of all doctors informed the patients about benefits and risks of the examination. Despite the fact that only 9% of the emergency physicians interviewed by Lee et al. were aware of a risk increase, 22% of them stated that they were speaking about CT risks and benefits with the patients [24]. The radiologists from the same survey, of whom 47% were aware of a risk increase, informed their patients less frequently (15%) [24]. 4.7. Influence of education and experience Nine surveys considered at least one possible influencing factor for knowledge. However, no significant influence was found concerning type of education [17,21,24] or speciality [21]. Neither the type of workplace [17] nor the duration of professional experience [18,19,21,24] was associated with reported knowledge. Attendance of a radiation protection course positively influenced overall knowledge in two [22,29] out of five [18,23,27] surveys. 5. Discussion We performed a broad systematic literature review in eight databases, resulting in 3091 articles. 14 primary research articles on physicians’ knowledge of radiation dose from computed tomography and other diagnostic procedures and associated risks were included in our final analysis. A common finding was a moderate, in some cases even low level of knowledge and radiation risk awareness. The included surveys varied markedly in design and study conduct. Four surveys were performed as face-to-face interviews. In such “direct” interviews, the answers reflect the current knowledge of the interviewees. Ten surveys used written questionnaires. This approach allows the respondents to gather some information before answering the survey questions. Finally, three investigations combined both methods. In several studies, the methods were not fully described. Furthermore, the detailed survey questions varied considerably. Most surveys concentrated on dose estimations, but used different approaches and focused on a varying range of procedures or patients. Comparisons are therefore hampered, and only broad conclusions can be drawn. Another limitation arises from the low numbers of interviewed persons in the single surveys.
The results may be confounded as all published studies tend to use different questions and different bench-marks. Considerable differences in medical and educational practices as well as health systems issues exist between the various countries. In addition, average effective doses for different examinations may vary between countries, which makes overall judgements using a common standard difficult. Interestingly, the publications covered the years 1996 and 2004–2009 only, with a gap between 1997 and 2004. Possibly, the article by Brenner et al. in 2001 [5] stimulated the discussion on health risks due to computed tomography. The surveys after 2004 focused on CT and radiation dosage and might be motivated by the increased scientific interest. The two surveys before 1997 addressed computed tomographies only among other radiological examinations. In Germany, an increase in awareness was noted in the two consecutive studies in the same study region. Overall, the reports from Germany showed higher proportions of correct answers compared to those from the other countries. However, only a few questions are directly comparable with other surveys (Table 3). The awareness of the ongoing survey among the target population (hospital physicians) may have contributed to these results. The second German survey was performed in the same geographical region, and aimed at paediatricians outside and inside hospitals, who may have been informed about the earlier investigation. Additionally one may assume a priori higher awareness among paediatricians concerning radiation risks of children. The overall relatively poor results concerning knowledge of radiation exposure and risk awareness are difficult to interpret. No trends over time were discernible in any country but Germany. All other successive surveys were not conducted in the same region, and differed in terms of methodology, limiting comparability. The findings must therefore be interpreted with caution and may only be seen as rough indicators for medical CT related practice. Our study questions focussed on physicians’ knowledge of radiation doses and related risks. Most of the identified surveys evaluated knowledge on doses in quantitative numerical terms. From the perspective of radiation protection, the underlying rationale would be to assume that good knowledge about medical radiation risks leads to fewer CT indications and reduced radiation exposure in children. However, this assumption can be questioned. The review has shown that a better knowledge about the radiation doses does not necessarily imply a reduced CT use in the diagnostic process. Additionally, knowledge evaluation by asking for quantitative numerical terms may be criticised. Accordingly it might be more appropriate to obtain information on issues such as the knowledge of recommended primary examinations, given a specified case scenario. We are currently conducting a survey among physicians which includes such an approach.
6. Conclusions We conducted a systematic literature review to include all available information on physicians’ knowledge about CT radiation doses and associated health risks. Only a minority of physicians were well informed about these topics in almost all studies we found. However the different methodologies of the 14 included studies render an interpretation difficult. Nevertheless, this systematic review implies that radiation protection awareness among physicians particularly for CT could be improved.
Competing interests The authors declare no competing interest.
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Appendix A. Fifth and final query for medline (“radiation”[TI] OR “Radiation Dosage”[Mesh Terms] OR “Radiation, Ionizing”[Mesh Terms] OR “Tomography, X-Ray Computed”[Mesh Terms] OR “Diagnostic Imaging”[Mesh Terms]) AND (“awareness”[TI] OR “knowledge”[TI] OR “knowledge”[Mesh Terms] OR “Awareness”[Mesh Terms] OR “Health Knowledge, Attitudes, Practice”[Mesh Terms] OR “Clinical Competence”[Mesh Terms]) AND (“physicians”’[TIAB] OR “physicians”[TIAB] OR “physician”[TIAB] OR “radiologists”’[TIAB] OR “radiologists”[TIAB] OR “radiologist”[TIAB] OR “doctors”’[TIAB] OR “doctors”[TIAB] OR “doctor”[TIAB] OR “paediatricians”’[TIAB] OR “paediatricians”[TIAB] OR “paediatrician”[TIAB] OR “pediatricians”’[TIAB] OR “pediatricians”[TIAB] OR “pediatrician”[TIAB] OR “Physicians”[MeSH Terms]) NOT (“Case Study”[TI] OR “Case Report”[TI] OR “Case Studies”[TI] OR “Case Histories”[TI] OR “case reports” [Publication Type] OR “News” [Publication Type] OR “Review”[PT]) NOT (“animals”[mh] NOT (“humans”[mh] and “animals”[mh])) NOT mammogra*[TI] References [1] Mettler FA, Wiest PW, Locken JA, Kelsey CA. CT scanning: patterns of use and dose. J Radiol Prot 2000;20:353–9. [2] Shrimpton PC, Hillier MC, Lewis MA, Dunn M. National survey of doses from CT in the UK: 2003. Br J Radiol 2006;79:968–80. [3] Monson RR, Cleaver JE, Abrams HL, et al. Health risks from exposure to low levels of ionizing radiation (BEIR VII-Phase 2). Washington, DC: The National Academies Press; 2006. [4] UNSCEAR (United Nations Scientific Committee on the Effects of Atomic Radiation). Sources and effects of ionizing radiation (volume II: effects). Vienna: United Nations; 2000. [5] Brenner DJ, Elliston CD, Hall EJ, Berdon WE. Estimated risks of radiation-induced fatal cancer from pediatric CT. Am J Roentgenol 2001;176:289–96. [6] Rehani MM, Berry M. Radiation doses in computed tomography. The increasing doses of radiation need to be controlled. Br Med J 2000;320:593–4. [7] Heyer CM, Peters S, Lemburg S. Structure of the meeting of the German radiological society and scientific discourse pertaining to radiation dose and dose reduction: an analysis of 1998–2008. Rofo 2009;181:1065–72. [8] Berdon EW, Brenner DJ, Brody AJ, et al. The ALARA (as low as reasonably achievable) concept in pediatric CT intelligent dose reduction. Pediatr Radiol 2002;32:217–313. [9] Shah NB, Platt SL. ALARA: is there a cause for alarm? Reducing radiation risks from computed tomography scanning in children. Curr Opin Pediatr 2008;20:243–7. [10] Bundesministerium für Umwelt, Naturschutz, Reaktorsicherheit. Umweltradioaktivität und Strahlenbelastung im Jahr 2007. Berlin: Bundesregierung Deutschland; 2008. [11] Aldrich J, Hufton A, Kalra MK, et al. Dose reduction in CT while maintaining diagnostic confidence: a feasibility/demonstration study. Vienna: International Atomic Energy Agency; 2009. [12] Galanski M, Nagel H, Stamm G. Paediatrische CT-Expositionspraxis in der BRD: Ergebnisse 2005/06. Hannover: Medizinische Hochschule Hannover; 2006. [13] Galanski M, Nagel HD, Stamm G. CT-Expositionspraxis in der Bundesrepublik Deutschland: Ergebnisse 1999. Frankfurt: Zentralverband Elektrotechnik und Elektroindustrie (ZVEI); 2000. [14] Higgins J, Green S. Cochrane handbook for systematic reviews of intervention (version 5.0.1.). Oxford: The Cochrane Collaboration; 2008. [15] Moher D, Liberati A, Tetzlaff J, Altman DG, for the PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009;62:1006–12. [16] Rassin M, Granat P, Berger M, Silner D. Attitude and knowledge of physicians and nurses about ionizing radiation. J Rad Nur 2005;24:26–30.
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