INTRODUCTION. Jpn J Clin Oncol 2014;44(3) doi: /jjco/hyt224 Advance Access Publication 26 January 2014
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1 Jpn J Clin Oncol 2014;44(3) doi: /jjco/hyt224 Advance Access Publication 26 January 2014 The Dose and Risk Factors for Radiation Exposure to Medical Staff during Endobronchial Ultrasonography with a Guide Sheath for Peripheral Pulmonary Lesions under X-ray Fluoroscopy Masahiro Katsurada 1,2, Takehiro Izumo 1,*, Yuichi Nagai 3, Christine Chavez 1, Mayumi Kitagawa 3, Jun Torii 3, Takumi Iwase 3, Tomohiko Aso 3, Takaaki Tsuchida 1 and Shinji Sasada 1 1 Respiratory Endoscopy Division, Department of Endoscopy, National Cancer Center Hospital, Tokyo, 2 Department of Pulmonology, Kameda Medical Center, Chiba and 3 Department of Radiological Diagnosis, National Cancer Center Hospital, Tokyo, Japan *For reprints and all correspondence: Takehiro Izumo, Department of Endoscopy, Respiratory Endoscopy Division, National Cancer Center Hospital, Tsukiji Chuo-ku, Tokyo , Japan, tizumo@ncc.go.jp Received October 16, 2013; accepted December 12, 2013 Objective: Therapy for lung cancer has recently evolved to include molecular targeted therapy and adequate amounts of lung cancer tissue are needed to identify particular phenotypes. For this purpose, quite a number of investigations on diagnostic bronchoscopy have been undertaken. Corollary to the increasing number of transbronchial biopsies for peripheral pulmonary nodules is the increased chances of radiation exposure during fluoroscopy. Our aim was to determine the dose and risk factors of radiation exposure to medical staff. Methods: Endobronchial ultrasonography with a guide sheath under X-ray fluoroscopy was performed on 132 cases of peripheral pulmonary lesions. The radiation exposure dose to medical staff (operator physicians, assistant physicians, nurses and radiological technologists) was measured. Results: The median time of fluoroscopy was 7.6 min (range ). The median radiation exposure dose to operator physicians was 12 msv/exam (range 1 99), while that of the other medical staff was lower. In a multivariate analysis, body mass index and the location of the radial ultrasound probe had significantly higher odds ratios. Conclusions: The risk factors for an increased radiation exposure dose were patients BMI and the location of the radial ultrasound probe. But even then, the radiation exposure dose to medical staff during endobronchial ultrasonography with a guide sheath was very low, especially for nurses and radiological technologists in whom the exposure dose was negligible. Key words: body mass index bronchoscopy radial ebus fluoroscopy lung cancer EBUS-GS radiation INTRODUCTION Lung cancer is one of the most common causes of cancerrelateddeathsintheusa,europeandjapan(1 3). The outcome of the disease depends on the stage, with the earlier stages having the best survival rates. The National Lung Screening Trial demonstrated that early stage lung cancer can now be easily detected and mortality rates can be decreased by low-dose computed tomography (CT) scan screening (4). Dynamic changes concerning lung cancer treatment have come about as well. Much interest is now given to molecular markers that are targets of treatment. Examples of these targeted therapies are erlotinib for epidermal growth factor receptor mutation cancer (5), crizotinib for anaplastic lymphoma kinase fusion gene cancer (6) and pemetrexed for # The Author Published by Oxford University Press. All rights reserved. For Permissions, please journals.permissions@oup.com
2 258 Safety of using fluoroscopy during EBUS-GS adenocarcinoma (7). For efficient histological and molecular marker examination, procurement of adequate amounts of lung cancer tissues is necessary. Bronchoscopy is one of the most practical modalities for obtaining lung tissues but the diagnostic accuracy for peripheral pulmonary lesions (PPLs),20 mm was previously noted to be low (8). Improvements have been made and researches now show the benefits of radial type endobronchial ultrasound (R-EBUS), guide sheath (GS), combination of R-EBUS and GS (EBUS-GS) (9 11), virtual bronchoscopic navigation system (VBN) (12) and combination of R-EBUS and VBN (13,14). These procedures are augmented by the concomitant use of fluoroscopy. There is a vast availability of literature about the aforementioned diagnostic tools but reports on radiation exposure dose to medical staff and patients are few. Some researches indicate radiation exposure as a health hazard. Thus, it is important to know the radiation exposure dose during bronchoscopy. In this study, our aim was to find out the dose and the risk factors of radiation exposure to medical staff when performing diagnostic bronchoscopy. PATIENTS AND METHODS MEASUREMENT OF THE RADIATION EXPOSURE DOSE TO MEDICAL STAFF The radiation exposure dose to medical staff of the Respiratory Endoscopy Division of the National Cancer Center Hospital in Tokyo, Japan was measured from 1 October 2012 to 28 December The medical staff consisted of the operator physicians, assistant physicians, nurses and radiological technologists. Radiation protectors (lead gowns) were worn every time fluoroscopy was used. To measure the radiation dose, radiation analyzers (MYDOSE mini x, PDM-117, ALOKA, Japan) were placed in pockets outside the radiation protectors (Fig. 1) at the beginning of each procedure. These analyzers can record X-ray energies from 1 to 9999 msv. Readings were recorded immediately after each procedure. This study was approved by the National Cancer Center Institutional Review Board. VISTA, Hitachi, Japan) was used to guide the insertion of the R-EBUS probe with GS through the working channel of the bronchoscope until the target site is reached. After confirming the location of the R-EBUS probe and GS within a target lesion, transbronchial and brush biopsies for cytology were carried out for specimen collection. When the R-EBUS probe was adjacent to or outside the target lesion, the bronchus closest to the PPL was first meticulously searched under fluoroscopy prior to specimen collection. Each biopsy and brush sampling procedure, as well as the removal of the GS after sampling, was done likewise under fluoroscopy guidance. STATISTICAL ANALYSIS We investigated the risk factors for radiation exposure dose and the variables affecting fluoroscopy time using the Fisher exact test. Variables under the P-values of 0.2 were analyzed using logistic regression. All P-values were two sided and levels 0.05 were considered statistically significant. Statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University; ac.jp/saitama-sct/saitamahp.files/statmed.html; Kanda), a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria, Ver ) and a modified version of R commander (Ver ). RESULTS There were a total of 151 diagnostic bronchoscopy procedures during the study period. The study included 132 procedures wherein EBUS-GS for PPLs was used. Nineteen tests were excluded (7 did not use R-EBUS, 5 had no measurement of radiation dose to operator physicians, 4 did not use GS, 3 were tests for diffuse lung diseases). The medical staff consisted of BIOPSY PROCEDURE BY GUIDED BRONCHOSCOPY For all patients, flexible bronchoscopy was done using a fiberoptic bronchoscope (BF-1T260 or BF-P260F, Olympus, Japan) in combination with the R-EBUS probe (20 MHz mechanical-radial type; UM-S20-20R or UM-S20-17S, Olympus, Japan) and GS (K-201 or K-203, Olympus, Japan). The location of the bronchus leading to the lesion was planned in advance by using high-resolution chest CT (HRCT) or VBN (Ziostation2, Ziosoft, Japan or LungPoint, Broncus, USA). Each procedure was done under local anesthesia with conscious sedation; the scope was inserted through the oral route. Oxygen saturation and blood pressure were monitored during the entire procedure. X-ray fluoroscopy (VersiFlex Figure 1. (A) The members of the medical staff as they perform bronchoscopy. Note that they are wearing lead gowns for radiation protection. (B)The radiation analyzer is placed in a pocket near the anterior chest outside the radiation protector. The part of measurement is indicated with an arrow.
3 Jpn J Clin Oncol 2014;44(3) 259 nine doctors (regular staff and rotating trainees), four nurses and four radiological technicians. Table 1 shows the baseline characteristics of the patients and target lesions. All examinations were completed as planned. The median examination time of bronchoscopy was 20 min (range 5 45). VBN was used for 50 cases wherein the target bronchi were small and difficult to trace. The number of the within location of the R-EBUS probe was 75 (56.8%), adjacent to was 36 (27.3%) and outside was 21 (15.9%). Table 1. Characteristics of patients and target lesions No. or median (range) Patients n ¼ 132 Age (years) 69 (32 89) Gender Male 77 (58.3%) Female 55 (41.7%) BMI (kg/m 2 ) ( ) Target lesions Size of long axis (mm) 24.5 (8 107),20 44 (33.3%) (66.7%) Solid 102 (77.3%) GGO 24 (18.2%) Pure GGO 6 (4.5%) Mixed GGO 18 (13.6%) Consolidation 6 (4.5%) Lobe affected Right upper lobe 39 (29.5%) Right middle lobe 21 (15.9%) Right lower lobe 27 (20.5%) Left upper lobe 13 (9.8%) Left middle lobe 10 (7.6%) Left lower lobe 22 (16.7%) Location Mediastinum 33 (25.0%) Center 60 (45.5%) Mesothelium 37 (28.0%) All 2 (1.5%) Visible on chest X-ray Yes 111 (84.1%) No 21 (15.9%) Bronchus sign Yes 108 (81.8%) No 24 (18.2%) BMI, body mass index; GGO, ground glass opacity. The predominant type of histology was adenocarcinoma (41.7%) followed by squamous cell carcinoma, NSCLC and small cell carcinoma (Table 2). The median radiation exposure dose was 12 (1 99) msv/ exam to operator physicians, 3 (0 7) msv/exam to assistant physicians (vs. operator: P, 0.01), 0 (0 9) msv/exam to nurses (vs. operator: P, 0.01) and 0 (0 1) msv/exam to radiological technologists (vs. operator: P, 0.01). We investigated the risk factors of radiation exposure to operator physicians with the Fisher exact test. BMI, bronchus sign and R-EBUS probe location had P, 0.2 (BMI: P ¼ 0.04, bronchus sign: P ¼ 0.18, R-EBUS probe location: P ¼ 0.04). Logistic regression analysis indicated that BMI [odds ratio; 3.51 ( ): P ¼ 0.03] and R-EBUS probe location [odds ratio; 1.84 ( ): P ¼ 0.02] were significant risk factors (Tables 3 and 4). The median duration of fluoroscopy was 7.6 ( ) min. By Fisher exact test, visible on chest radiograph, diameter of GS, size of PPL, location of PPL and location of R-EBUS probe all had P values of,0.2 (visible on chest radiograph: P, 0.01, diameter of GS: P ¼ 0.04, size: P, 0.01, location: P ¼ 0.14 and location of R-EBUS probe: P, 0.01). Logistic regression analysis indicated that size Table 2. Outcomes of EBUS-GS No. or median (range) Time of bronchoscopic examination (min) 20 (5 45) Use of VBN Yes 50 (37.9%) No 82 (62.1%) Diameter of GS (mm) (31.1%) (68.9%) Use of needle Yes 23 (17.4%) No 109 (82.6%) Location of R-EBUS probe Within 75 (56.8%) Adjacent to 36 (27.3%) Outside 21 (15.9%) Histology Adenocarcinoma 55 (41.7%) Squamous cell carcinoma 12 (9.1%) NSCLC 3 (2.3%) Small cell carcinoma 2 (1.5%) Other 2 (1.5%) EBUS-GS, endobronchial ultrasonography with a guide sheath; VBN, virtual bronchoscopic navigation; GS, guide sheath; R-EBUS, radial type endobronchial ultrasound; NSCLC, non-small cell lung cancer.
4 260 Safety of using fluoroscopy during EBUS-GS Table 3. The radiation exposure dose from fluoroscopy during bronchoscopy Table 4. Risk factors of dose of radiation exposure of the operator physicians [odds ratio: 0.33 ( ): P ¼ 0.02] and location of the R-EBUS probe [odds ratio: 3.66 ( ): P, 0.01] were the variables that significantly affected the duration of fluoroscopy (Table 5). DISCUSSION Median (range) Time of fluoroscopy (min) 7.6 ( ) Operator physician (msv/exam) 12 (1 99) Assistant physician (msv/exam) 3 (0 7),0.01 Nurse (msv/exam) 0 (0 9),0.01 Radiation technician (msv/exam) 0 (0 1),0.01 P value (vs. operator physician) Our study aimed to determine the radiation exposure dose and the risk factors of medical staff. The radiation exposure dose to medical staff was low, especially to assistant physicians, nurses and radiological technologists. Meanwhile, our data showed that operator physicians were exposed to a median of 12 (1 99) msv/exam of radiation. This is similar to that reported by Steinfort et al. (15). Our fluoroscopy time was 7.6 ( ) min. Fujita et al. (16) reported that the fluoroscopy time was min with GS. Some health hazards arising from radiation exposure have been reported, among which are cancer and cataract formation. In 2007, Cardis et al. (17) reported that workers in the nuclear industry of 15 different countries had an excess relative risk (ERR) of 0.97 per Sv of radiation [95% confidence interval (CI): ] for cancers other than leukemia. Ozasa et al. (18) reported that atomic bomb survivors had an ERR of 0.47 per Sv (95% CI: ) for all solid cancers. Sigurdson et al. (19) investigated radiologic technicians in the USA from 1983 to They reported that the standardized incidence ratio (SIR) was 1.04 [95% CI: ) for all cancers, that female technologists had an elevated risk for all solid cancers (SIR ¼ 1.16; 95% CI: ) and that male technologists experienced a decreased risk for solid tumors (SIR ¼ 0.92; 95% CI, ). Berrington et al. (20) investigated radiologists and radiotherapists in the UK from 1897 to 1997 and observed that the number of cancer deaths in those who registered after 1920 was similar to that expected from death rates for all medical practitioners combined [standardized mortality ratio (SMR) 1.04; 95% CI: ]. Chodick et al. reported in 2008 that radiologic technologists had an adjusted hazard ratio of 1.25 (95% CI; ) for cataract for workers in the highest category (mean, 60 msv) vs. lowest category (mean, 5 msv). The lowest cumulative ionizing radiation exposure dose that could result in Univariate analysis 12 m Sv/exam.12 msv/exam Fisher, P value BMI (kg/m 2 ), Bronchus sign Yes No 9 15 Visible on chest X-ray Yes No 9 12 Diameter of GS (mm) Size (mm) Lung field Right upper field Right middle field 15 6 Right lower field Left upper field 7 6 Left middle field 5 5 Left lower field Location Mediastinum Center Mesothelium All 0 2 Characteristics of target lesion Solid Pure GGO 3 3 Mixed GGO 7 11 Consolidation 4 2 Use of VBN Yes No Location of R-EBUS probe Within Adjacent to Outside 8 13 Multivariate analysis Odds ratio 95% CI P value Bronchus sign BMI Location of R-EBUS probe
5 Jpn J Clin Oncol 2014;44(3) 261 Table 5. Factors affecting fluoroscopy time Univariate analysis,7.6 min/exam 7.6 min/exam Fisher, P value BMI (kg/m 2 ), Bronchus sign Yes No Visible on chest X-ray Yes 61 50,0.01 No 4 17 Diameter of GS (mm) Size (mm) , Lung field Right upper field Right middle field 13 8 Right lower field Left upper field 6 7 Left middle field 4 6 Left lower field Location Mediastinum Center Mesothelium All 2 0 Characteristics of target lesion Solid Pure GGO 3 3 Mixed GGO 5 13 Consolidation 3 3 Use of VBN Yes No Location of R-EBUS probe Within 53 22,0.01 Adjacent to 8 28 Outside 4 17 Multivariate analysis Odds ratio 95% CI P value Bronchus sign Size (mm) Location of R-EBUS probe ,0.01 progressive cataract was 2 Sv(21). However, there have been recent reports about changes occurring in the posterior subcapsular lens with lower cumulative radiation exposure dose. Vano et al. researched 54 interventional cardiologists, 69 nurses and technicians from hemodynamic rooms and 4 endovascular surgeons in Buenos Aires. They showed that posterior subcapsular lens changes were found in 50% of interventional cardiologists and in 41% of nurses and technicians, and that the estimated cumulative eye doses raged from 0.1 to 18.9 Sv (22). For interventional radiology procedures, Chida et al. reported that the annual mean + SD radiation exposure dose to operator physicians, assistant physicians, nurses and radiological technologists was ( ), ( ) and ( ) msv/year, respectively (23). Our study showed that the radiation exposure dose to medical staff was very low. The median radiation exposure dose (range) to medical staff was at most 12 (1 99) msv/ exam. In our hospital, each member of the medical staff performs an average of 360 bronchoscopies per year. We estimate that the average annual dose to operator physicians, assistant physicians, nurses and radiological technologists is 4.3, 1.08, almost 0 msv and almost 0 msv, respectively. These values could be less because of the additional protection from wearing lead gowns. Furthermore, the radiation exposure dose to nurses and radiological technologists is extremely low. We realized that the risk factors with significant odds of higher radiation exposure dose were the patient s BMI and the location of the R-EBUS probe. The relatively high exposure dose when dealing with patients with greater BMI could be explained by a larger surface area that needs fluoroscopy and also by the fact that the operator and assistant physicians are strategically closer to the fluoroscopy gantry in such situations. Meanwhile, when a PPL does not have a bronchus directly leading to it, the location of the R-EBUS probe when inserted initially through the GS is usually not seen within the target site. To search for an optimal location for sampling, the probe had to be repositioned for as many times possible while expending intermittent, albeit more frequent, use of fluoroscopy. Thus, adjacent to or within location of the R-EBUS probe has a higher probability of increased radiation exposure. Interestingly, the variables affecting the fluoroscopy time were different from those of radiation exposure. This suggests that duration of fluoroscopy may not be the only factor correlated with risk of radiation exposure. Our data show that as the BMI of the patient increases, the radiation exposure dose to the operator increases regardless of fluoroscopy duration. The limitations of this study are first, this is a single-center study in an academic hospital. Secondly, all procedures for PPLs at our institution were carried out using both R-EBUS and GS. Our results may not be applicable to conventional diagnostic bronchoscopies that use fluoroscopy alone.
6 262 Safety of using fluoroscopy during EBUS-GS CONCLUSIONS We demonstrated the dose and risk factors of radiation exposure to medical staff during EBUS-GS under X-ray fluoroscopy. The risk factors for a relatively higher radiation exposure dose were patients BMI and the location of the R-EBUS probe but, the dose of radiation exposure to medical staff was very low, especially to nurses and radiological technologists. Funding This work was supported by The National Cancer Center Research and Development Fund (25-A-12). Conflict of interest The authors have reported no conflicts of interest to Japanese Journal of Clinical Oncology. References 1. Matsuda T, Marugame T, Kamo K, Katanoda K, Ajiki W, Sobue T. Cancer incidence and incidence rates in Japan in 2006: based on data from 15 population-based cancer registries in the monitoring of cancer incidence in Japan (MCIJ) project. Jpn J Clin Oncol 2012;42: Siegel R, Naishadham D, Jemal A. Cancer statistics, CA Cancer J Clin 2013;63: Gatta G, Zigon G, Capocaccia R, et al. Survival of European children and young adults with cancer diagnosed Eur J Cancer 2009;45: Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. New Engl J Med 2011;365: Tsao MS, Sakurada A, Cutz JC, et al. Erlotinib in lung cancer molecular and clinical predictors of outcome. New Engl J Med 2005;353: Shaw AT, Kim DW, Nakagawa K, et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. New Engl J Med 2013; 368: Scagliotti GV, Parikh P, von Pawel J, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol 2008;26: Rivera MP, Mehta AC, Wahidi MM. Establishing the diagnosis of lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143(Suppl):e142S 65S. 9. Kurimoto N, Miyazawa T, Okimasa S, et al. Endobronchial ultrasonography using a guide sheath increases the ability to diagnose peripheral pulmonary lesions endoscopically. Chest 2004;126: Shirakawa T, Imamura F, Hamamoto J, et al. Usefulness of endobronchial ultrasonography for transbronchial lung biopsies of peripheral lung lesions. Respiration 2004;71: Herth FJ, Eberhardt R, Becker HD, Ernst A. Endobronchial ultrasound-guided transbronchial lung biopsy in fluoroscopically invisible solitary pulmonary nodules: a prospective trial. Chest 2006;129: Tachihara M, Ishida T, Kanazawa K, et al. A virtual bronchoscopic navigation system under X-ray fluoroscopy for transbronchial diagnosis of small peripheral pulmonary lesions. Lung Cancer 2007;57: Ishida T, Asano F, Yamazaki K, et al. Virtual bronchoscopic navigation combined with endobronchial ultrasound to diagnose small peripheral pulmonary lesions: a randomised trial. Thorax 2011;66: Asano F, Shinagawa N, Ishida T, et al. Virtual bronchoscopic navigation combined with ultrathin bronchoscopy. A randomized clinical trial. Am J Respir Crit Care Med 2013;188: Steinfort DP, Einsiedel P, Irving LB. Radiation dose to patients and clinicians during fluoroscopically-guided biopsy of peripheral pulmonary lesions. Respir Care 2010;55: Fujita Y, Seki N, Kurimoto N, et al. Introduction of endobronchial ultrasonography (EBUS) in bronchoscopy clearly reduces fluoroscopy time: comparison of 147 cases in groups before and after EBUS introduction. Jpn J Clin Oncol 2011;41: Cardis E, Vrijheid M, Blettner M, et al. Risk of cancer after low doses of ionising radiation: retrospective cohort study in 15 countries. BMJ 2005;331: Ozasa K, Shimizu Y, Suyama A, et al. Studies of the mortality of atomic bomb survivors, Report 14, : an overview of cancer and noncancer diseases. Radiat Res 2012;177: Sigurdson AJ, Doody MM, Rao RS, et al. Cancer incidence in the US radiologic technologists health study, Cancer 2003;97: Berrington A, Darby SC, Weiss HA, Doll R. 100 years of observation on British radiologists: mortality from cancer and other causes Br J Radiol 2001;74: Chodick G, Bekiroglu N, Hauptmann M, 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: Vano E, Kleiman NJ, Duran A, Romano-Miller M, Rehani MM. Radiation-associated lens opacities in catheterization personnel: results of a survey and direct assessments. J Vasc Interv Radiol 2013;24: Chida K, Kaga Y, Haga Y, et al. Occupational dose in interventional radiology procedures. AJR Am J Roentgenol2013;200:
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