Unintentional Exposure of Neonates to Conventional Radiography in the Neonatal Intensive Care Units

Journal of Perinatology (2007) 27, 579–585 r 2007 Nature Publishing Group All rights reserved. 0743-8346/07 $30 www.nature.com/jp ORIGINAL ARTICLE Unintentional exposure of neonates to conventional radiography in the Neonatal Intensive Care Units

D Bader1,2, H Datz3,4, G Bartal5,6, AA Juster7,8, K Marks9,10, T Smolkin11,2, S Zangen12,10, A Kugelman1,2, C Hoffmann6,13, G Shani4, A Ben–Shlomo3, M Margaliot3 and S Sadetzki6,14 1Department of Neonatology, Bnai-Zion Medical Center, Haifa, Israel; 2B. Rappaport Faculty of Medicine, Technion, Israel Institute of Technology, Haifa, Israel; 3Radiation Safety Division, Soreq Nuclear Research Center, Yavne, Israel; 4Faculty of Bio-Engineering, Ben-Gurion University, Beer Sheva, Israel; 5Department of Radiology, Meir Medical Center, Kfar Saba, Israel; 6Sackler School of Medicine, Tel- Aviv, Israel; 7Department of Neonatology, Kaplan Medical Center, Rehovot, Israel; 8Hadassah Medical School, Hebrew University, Jerusalem, Israel; 9Department of Neonatology, Soroka Medical Center, Beer Sheva, Israel; 10Faculty of Medicine, Ben- Gurion University, Beer Sheva, Israel; 11Department of Neonatology, Rambam Medical Center, Haifa, Israel; 12Department of Neonatology, Barzilay Medical Center, Ashkelon, Israel; 13Department of Radiology, Chaim Sheba Medical Center, Tel Hashomer, Israel and 14Cancer & Radiation Epidemiology Unit, Gertner Institute, Chaim Sheba Medical Center, Tel Hashomer, Israel

Higher awareness and training of the medical teams and radiographers Objective: To evaluate the extent of unintentional exposure to X-rays are required to minimize unnecessary exposure of newborns to ionizing performed during routine diagnostic procedures in the Neonatal Intensive radiation. Care Units (NICUs). Journal of Perinatology (2007) 27, 579–585; doi:10.1038/sj.jp.7211792; Study Design: During a 1-month period, 157 consecutive neonates from published online 12 July 2007 five level-III NICUs were recruited for this study. The mean birth weight was 1747±911 g (range: 564–4080 g), and gestational age was 31.6±3.6 Keywords: X-ray radiation; neonate; overexposure weeks (range: 24–41 weeks). A total of 500 radiographs were performed including chest (68%), abdomen (17%) and combined chest and abdomen (15%). The average number of radiographs taken per infant was 4.2±3.6 (range: 1–21). Unintentional inclusion of body regions Introduction other than those ordered was determined by comparing the areas that Nearly 12% of all births in Western countries are premature, with should be included in the radiation field according to International about 2% of infants born less than 32 weeks of gestation.1–3 recommendations, to those that appeared in the actual radiograph. In the last decade, the survival of preterm infants has risen to Result: A comparison of the recommended borders to the actual nearly 90%, especially of those with a very low birth weight of less boundaries of the radiographs taken show an additional exposure to than 1500 g. Even infants with a birth weight of less than 750 g 1–3 radiation in all three procedures: 85% of chest radiographs also included the have a survival rate of 55%. Advanced neonatal care has also whole abdomen, 64% of abdomen radiographs included both thigh and increase the survival of term infants with serious diseases caused by upper chest and 62% of chest and abdomen radiograph included the thigh. either congenital anomalies or a complicated neonatal course. (The range in all procedures was from ankle to upper head.) Between 2 and These high-risk infants are prone to a variety of diseases and 20% of the relevant targeted body tissues were not included in the exposed morbidities such as respiratory distress syndrome, fields resulting in missing data. The gonads of both sexes were exposed in bronchopulmonary dysplasia, patent ductus arteriosus and 1–3 7% in all chest X-rays. Among male infants, the testes were exposed in 31% necrotizing enterocolitis. of plain abdomen radiographs and 34% of chest and abdomen radiographs. During their prolonged and complicated medical course in the Neonatal Intensive Care Units (NICUs), these neonates are exposed Conclusion: In the NICUs participating in the study, neonates are to repeated diagnostic procedures that involve X-ray radiation.4–6 currently being exposed to X-ray radiation in nonrelevant body regions. Owing to the high frequency of respiratory disease and other morbidities, these infants continue to require additional X-ray Correspondence: Dr D Bader, Department of Neonatology, Bnai-Zion Medical Center, evaluations through early childhood and over time could receive 40 Golomb Street, Haifa 31048, Israel. substantial accumulating doses of radiation.4 E-mail: [email protected] Received 2 February 2007; revised 22 May 2007; accepted 19 June 2007; published online 12 Gonadal exposure to ionizing radiation of the neonate, July 2007 particularly preterm infants, is another important issue since Radiography in the Neonatal Intensive Care Unit D Bader et al 580 irradiation before adulthood may have long-term harmful effects The study population was stratified according to the infant’s on the size and function of the gonads.7–9 birth weight. Length of hospitalization (in days) and the number Detailed studies on the field size and body tissues included in of X-ray radiographs taken per infant during their particular initial each X-ray taken on these infants are scarce.10 Considering the hospital admission, was recorded. health hazards of ionizing radiation, the objective of this study was to evaluate unnecessary radiation exposure to body tissues outside Imaging technique the anatomical region of interest in five NICUs in Israel. The three most commonly performed diagnostic plain X-ray These data could be used as a first step in minimizing the risk examinations undertaken in the NICUs were investigated: chest, of radiographic examinations in infants. abdomen, and chest and abdomen (babygram). For each type of radiograph, the exposure fields were defined, and compared to those recommended by the International Methods guidelines.11–13 The acceptable minimal field size was set by Patients recognizable anatomical landmarks for specific examination. In The Institutional and Ministry of Health approvals for this study our population (during the neonatal period), the tolerance level were obtained for all NICUs and informed consent was obtained was reduced to 2.0 cm at each edge on the measured film. For from the parents of each infant. None of the parents refused to example, an ideal chest radiograph would include the lower participate in this study. Level III NICUs located in five general cervical area at the top of the radiograph and the upper edge of the hospitals participated in the study (Bnai-Zion, Barzilay, Kaplan, abdominal area at the bottom (T12\L1), while the skull, upper Soroka and Rambam Medical Centers). These NICUs are a limbs and the middle-upper abdominal area should not be representative sample, caring for 22% of all infants born each year included. The ideal abdominal radiograph would include the in Israel (144 000 deliveries in 2003). All infants admitted to the diaphragms at the top and stop just inferior to the symphysis pubis NICUs during January 2003 were eligible to participate. This (Figure 1). Violation of the International recommendation was prospective study is part of a larger study designed to evaluate defined as 2.0 cm beyond the recommended boundaries. All the dosimetry of X-rays performed in NICUs. departments participating in this study adopt the guidelines on A total of 100 plain X-ray radiographs were obtained from each Quality Criteria for Diagnostic Radiograph in Pediatrics.13 center during January 2003. The three most commonly performed Unintentional inclusion of body tissues was determined by radiographs (abdomen, chest, and chest and abdomen comparing the body tissues that should have been exposed in the (babygram)) were ordered consecutively by the NICU teams, based type of radiograph ordered, to those that appeared in the actual on the medical condition of each infant (chest radiograph for radiograph taken. Each radiograph was determined to be either in Respiratory Distress Syndrome and so on). There were no inclusion accordance or in violation of the international guidelines by the or exclusion criteria for each type of radiograph. Radiographs were principal investigator in each center. preformed by certified radiographers, day and night, as requested by the medical teams of each NICUs. The study was completed at Analysis each center during the month of the study after 100 consecutive For analysis, we derived the percent of exposure for each body plain X-ray images were taken. region by dividing the number of times a certain region was

Chest X ray Abdominal X Ray

Int. recommendation

Figure 1 International recommendation for a typical chest and abdomen X-rays.

Journal of Perinatology Radiography in the Neonatal Intensive Care Unit D Bader et al 581

96% 98% 100

80% 80 74%

64% 64%

45% 38% 40

22% 20 10%

Percentage Frequencies of Organs at Examinations 0% 0 A K T G P Ab L.C U.C N L.H U.H Exposed organs

Violation of International recommendations International recommendations

A-Ankle; K-Knee; T -Thigh; G-Gonads; P-Pelvis; Ab-Abdomen; L.C-Lower Chest; U.C-Upper Chest; N-Neck; L.H-Lower Head; U.H-Upper Head Figure 2 Abdomen X-ray examination, necessary and unnecessary exposure of body organs.

99% 100% 95% 100

85%

41% 40

20 13% 7% 4% 1% 2%

Percentage Frequencies of Organs at Examinations 0% 0 A K T G P Ab L.C U.C N L.H U.H Exposed organs

Journal of Perinatology Radiography in the Neonatal Intensive Care Unit D Bader et al 582

100% 97% 95% 100 94% 88%

80% 80

62% 60

37% 40

26%

20 Percentage Frequencies of Organs at Examinations

1% 2% 0 A K T G P Ab L.C U.C N L.H U.H Exposed organs

Violation of International recommendations International recommendations A-Ankle; K-Knee; T-Thigh; G-Gonads; P-Pelvis; Ab-Abdomen; L.C-Lower Chest; U.C-Upper Chest; N-Neck; L.H-Lower Head; U.H-Upper Head Figure 4 Chest and abdomen X-ray examination, necessary and unnecessary exposure of body organs. clinical characteristic of the study population is shown in Table 1. (Figure 4). Of the abdomen radiographs taken, 45% unnecessarily The major diagnoses of the infants were: (a) respiratory distress exposed the neck and 64% exposed the upper chest (Figure 2). (varying from mild conditions requiring only observation with a Of the three targeted areas of abdomen X-rays, the abdomen was single chest radiograph being taken (such as transient tachypnea not in the field of the radiograph 2% of the time, the pelvis was not of the newborn) to a full blown disease such as respiratory distress in the field 4% and the lower chest was omitted in 20% of the syndrome of the extreme preterm infant, for which up to 21 abdomen X-rays taken. Chest and abdomen X-rays omitted the radiographs were taken), (b) necrotizing enterocolitis and (c) lower and upper chest 3–5%, the pelvis 6% and the neck 12% of patent ductus arteriosus. The mean number of radiographs taken the time. Of the chest radiographs taken, 5% omitted the neck and per infant is shown in Table 1. 1% did not have the lower chest in the field (Figures 2–4). Of the 500 radiographs, 68% were chest, 17% abdomen and 15% The gonads of both sexes were unintentionally exposed in 7% in combined chest and abdomen (Table 2a). all chest X-rays. Among male infants, the testes were exposed in The distribution according to the type of radiograph and birth 31% of plain abdomen and 34% in chest and abdomen radiographs weight is also shown in Table 2a. The largest group had a birth (Figures 2 and 4 are related to both sexes since the ovaries cannot weight of less than 1500 g (n ¼ 96, 61%) and, thus, received about be shielded during plain abdomen and chest and abdomen 65% of all radiographs taken. In all birth weight groups, the chest radiographs). The testes were not shielded in any of the abdomen X-ray was the most common procedure. or chest and abdomen radiographs performed. Table 2b describes the number of radiographs ordered per infant during the study. The majority of infants (75%) received only 1–2 radiographs per type (chest, abdominal, and/or chest and Discussion abdominal) in all birth weight groups. Our results demonstrate that in the NICUs which participated in the study, a wide range of neonatal body areas (from the ankle to Unintentional exposure the upper head) are being unnecessarily exposed to X-rays during The actual X-ray images show exposure of larger areas than those the performance of standard diagnostic radiology procedures in the ordered and discordance with International recommendations NICUs. We have also noticed that up to 20% of all radiographs need (Figures 2–4). Unnecessarily exposed body tissues ranged from to be repeated because the targeted body tissues did not appear in ankle to upper head. The thigh and upper chest were exposed in the radiographs, leading to insufficient data and increasing the 64% of all plain abdomen X-ray (Figure 2). The whole abdomen infant’s overall exposure to radiation. Additionally, the gonads were was exposed in 85% of all chest radiograph (Figure 3). The thigh not shielded in the majority of the radiographs taken, increasing was exposed in 62% of all chest and abdomen radiographs the possible risks of damage to future reproduction and fertility.

Journal of Perinatology Radiography in the Neonatal Intensive Care Unit D Bader et al 583

Table 1 Description of clinical characteristic of the study population (n ¼ 156 Table 2 Description of the X-ray procedures by birth weight and type of infants) radiographs

Gestational age (weeks) (a) Distribution of all X-ray radiographs by birth weight and type of procedure, Mean±s.d. 31.6±3.6 n ¼ 499 radiographs Range 24–41 Birth weight (g)

Birth weight (g) <1500 1500–2000 >2000 Total Mean±s.d. 1747±911 n(%)n(%)n(%)n(%) Range 564–4080 Chest 220 (44) 75 (15) 44 (9) 339 (68) Abdomen 55 (11) 8 (1.6) 21 (4) 84 (17) Categories (n, %) Chest and abdomen 51 (10) 7 (1.4) 19 (4) 77 (15) <1500 g 96, 61% Total 326 (65) 90 (18) 84 (17) 500 (100) >1500– <2000 g 13, 8% >2000 g 48, 31% (b) Distribution of X-ray radiographs by number of procedures performed for each neonate, birth weight and type of procedure Gender (%) Birth weight (g) Male 45.9 Female 54.1 <1500 1500–2000 >2000 Total

Major diagnosis (n, %) No. of chest radiographs RDS, TTN, BPD 132, 84% 1–2 36 20 35 91 NEC 5, 3% 3–4 11 4 4 19 PDA 13, 10% 5–9 9 4 4 17 IVH 5, 3% 10–21 3 F 14

Length of hospitalization (days) No. of abdominal radiographs Mean±s.d. 55.2±46.0 1–2 16 6 11 33 Range 4–120 3–4 5 F 16 5–9 1 F 12 Number of X-ray radiographs per infant 10–21 1 FF1 Total Mean±s.d. 4.2±3.6 No. of abdomen and chest radiographs Range 1–21 1–2 25 6 11 42 3–4 5 F 16 By birth weight 5–9 1 FF1 <1500 g 10–21 FFFF Mean±s.d. 5.1±4.3 Range 1–21 Total 113 40 69 222 >1500 g Mean±s.d. 3.6±2.6 Range 1–13 today. Despite the low risks associated with each radiograph, Sutton Abbreviations: BPD, bronchopulmonary dysplasia; IVH, intraventricular hemorrhage; et al.4 concluded that overall radiation doses in the NICUs may NEC, necrotizing enterocolitis; PDA, patent ductus arteriosus; RDS, respiratory distress syndrome; TTN, transient tachypnea of the neonate. have been underestimated in earlier studies for several reasons. First, infants may be referred to other hospitals, where additional examinations may be ordered. Second, preterm infants with Our results are concordant with those of Soboleski et al.,10 who chronic lung disease and other complications related to concluded that in their medical center the present techniques in prematurity are expected to have more radiographs throughout neonatal and pediatric radiography, result in unnecessary radiation their childhood. Finally, at least 5% of all radiographs have to be exposure to nonrelevant structures. repeated due to technical errors. Inappropriate ﬁeld size is the most critical fault in the pediatric The Committee on Environmental Health at the American radiographic technique.13 Alice Stewart14 was one of the pioneers in Academy of Pediatrics reviewed the risks associated with ionizing research of the possible risk of ionizing radiation to the fetus. The radiation exposure in most procedures and concluded that the fetuses of her time are our preterm infants of modern Neonatology danger is low. However, the Committee emphasized that radiation

Journal of Perinatology Radiography in the Neonatal Intensive Care Unit D Bader et al 584 exposure should be restricted only to those infants requiring X-ray It is clear from our work and the work of Barcham et al.7 that a procedures for good medical care.15 lack of proper guidance for professionals working with preterm Frush et al.16 emphasized that certain tissues are more infants, combined with a heavy work load and unintentional radiosensitive than others, and can be up to 10 times more oversight of existing guidelines, may lead to radiographers failing radiosensitive in infancy and childhood than in adulthood. This to use gonadal shielding and to utilize the collimation to ensure a means that a similar radiation dose per gram of tissue possibly has maximum quality radiograph. a more harmful effect in neonates. It is imperative that all neonatal teams, including physicians, Our study shows that a wide range of neonatal body tissues are nurses, radiographers and radiologists, acknowledge the existence being unnecessarily exposed to X-ray radiation, with a general and emphasize the valuable concept and criteria of ‘As Low As failure to protect the gonads. We must emphasize that our Reasonably Achievable (ALARA)’. These teams should work together data were obtained only during a limited time of study, and to find the most effective way to reduce this potential hazard. It is not during the entire hospitalization of the infants involved important to try to minimize the number of radiation-producing in this study. Furthermore, since our data relate only to tests, to examine the exposure dose and regularly review and common procedures, such as chest and abdomen X-rays, one implement dose reduction methods.11–13,17–19 A dedicated should keep in mind that there are also some infants who receive professional team should be established in every NICU to monitor much higher doses of radiation, as in computed tomography or quality control of X-ray radiology and to educate the NICU and fluoroscopy.3,5 radiology teams. Although all the radiology departments who participated in our Although this study was conducted on film-based conventional study had adopted the recommendations of the International radiography, our results and suggestions can clearly apply to Commission on Radiological Protection from 1990,11–13 we still computerized radiography, as well as digital radiography, as they see some serious difficulties in their implementation. regard the universal standards of radiography. There are no simple answers to why body tissues, other than A better awareness without causing an irrational fear is the key those originally intended, are exposed to radiation in the infants of for improving this issue. All caregivers are strongly advised to our study, or why the gonads are not routinely shielded. acquire better quality radiographs using adequate collimation and First, radiographers are eager to create the highest quality gonadal shielding. image and avoid repeated radiographs, but as a result they widen the fields of the radiograph, causing more extensive exposure of other radiosensitive body tissues. Acknowledgments Second, some extreme preterm infants are not many centimeters long and a 1–2 cm violation could include a large percentage of We thank Ms Maya Bader and Ms Samara Brown for their help in editing this paper. their body tissue. There is no easy way to get an ideal radiograph among this population. Third, gonadal shielding in abdominal radiographs in boys would be extremely difficult. In some tiny preterm infants, the References gonads will be closed up to the symphisis pubis and cannot be 1 Lee KG, Cloherty JP. Identifying the high risk newborn and evaluating gestational age, completely excluded from the film. Among extreme preterm female prematurity, postmaturity, large for gestational age and small for gestational age infants, it is difficult to shield the ovaries without shielding out infants. In: Cloherty JP, Eichenwald EC and Stark AR (eds). Manual of Neonatal Care, 5th edn. Lippincott Williams and Wilkins: Baltimore, MD, 2004, pp 42–56. almost the entire pelvis. 2 Martin JA, Kochanek KD, Strobino DM, Guyer B, MacDorman MF. Annual summary of 7 Addressing this issue, Barcham et al. concluded that the failure vital statistics. Pediatrics 2005; 115: 619–634. to follow these recommendations can be traced to a ‘philosophical 3 Vohr RB, Allen M. 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A good radiographic technique should 7 Barcham N, Egan I, Dowd S. Gonadal protection methods in neonatal chest radiography. Radiol Technol 1997; 69(2): 157–161. involve minimal radiation and proper collimation to avoid 8 de Rooij DG, van de Kant HJ, Dol R, Wagemaker G, van Buul PP, irrelevant organ exposure in the production of an image with all van Duijn-Goedhart A et al. Long-term effects of irradiation before adulthood on 17 the necessary information. reproductive function in the male rhesus monkey. Biol Reprod 2002; 66(2): 486–494.

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