A literature review was conducted to determine norms for practice in neonatal intensive care units (NICU) around the world, given the harmful risks associated with radiation exposure at a very young age; risk of radiation-induced harm later in life increases with every X-ray image taken, more so for younger premature babies. Empirical studies including a measurement of radiation dose in a NICU, published after the year 2000 in a peer-reviewed journal, were collected. Measured doses to patients or X-ray phantoms, number of X-rays per stay and conclusions with recommendations made in response to these values were compared for 25 studies from around the world. The number of X-rays a patient underwent during a NICU stay ranged from 0 to 159. Younger, lower birth weight patients consistently had the greatest number of X-rays per stay. Recommended action based on measured dose ranged from extensive (to minimize risk to neonates) to minimal (to reduce risk) to none (because imaging benefits outweigh patient risk), with no consistent pattern linking recommended action with dose quantity. This demonstrates a broad range of interpretations of the As Low As Reasonably Achievable (ALARA) concept. These findings indicate a disparity in the response to neonatal X-ray dose concerns on a global scale, posing a public health risk to this particular neonatal population. More up-to-date imaging protocols and dose limits specifically for the NICU environment with standardized dose monitoring would help minimize this risk to achieve the public health goals of prevention and harm reduction.
Key Words
1. Introduction
The neonatal intensive care unit (NICU) hospitalises newborn babies with serious to life-threatening medical problems that demand close monitoring. X-ray imaging is crucial for diagnosis and evaluation of these ill neonates. Mobile X-ray imaging systems are positioned around the patient and the incubator as well as other life-saving equipment.
1
This positioning of imaging equipment around the patient is a unique NICU-specific challenge which is very different from traditional radiography.The number of chest and/or abdomen X-rays taken during a single NICU stay varies. The greater the number of X-rays taken, the greater the neonate's cumulative exposure to radiation from the NICU stay. Babies in particular are at risk of developing radiation-induced illness, such as cancer, later in life.
2
The younger the patient, the greater this X-ray risk is; therefore, babies born pre-term are at highest risk.3
One would expect a global response to this risk to neonates, with standardized, evidence-based X-ray imaging practice in NICUs world-wide. The aim of this study is to review published empirical studies on radiation dose from NICU X-ray imaging to gain insight into international norms for practice, mapping global patterns of radiological safety and As Low As Reasonably Achievable (ALARA) practices.
2. Multinational NICU dose measurements
Journal articles were found using PubMed and Google Scholar, with a range of search terms and phrases to assure all key studies were covered. Search terms were neonatal intensive care unit and special care baby unit (both as separate words, phrases and acronyms), radiation, dose, exposure, X-ray, pediatric and paediatric. This helped assure articles from countries with differing terminologies and spellings would be found. Articles meeting all of the following criteria were included:
- ✓peer-reviewed journal articles,
- ✓empirical research only (no editorials or reviews),
- ✓measured neonatal X-ray dose in the NICU,
- ✓published after 2000.
It is imperative that factors specific to the NICU environment such as incubators and mobile X-ray equipment were included in the dose measurement. This was the key quality assessment criteria for which all articles were checked.
There were 25 studies, with 17 measuring dose to neonatal patients
4
, 5
, 6
, 7
, 8
, 9
, 10
, 11
, 12
, 13
, 14
, 15
, 16
, 17
, 18
, 19
, 20
and 8 measuring dose to X-ray phantoms.21
, 22
, 23
, 24
, 25
, 26
, 27
, 28
The number of study patients ranged from 12 to 450, with median 129 and only 3 studies4
,6
,18
including under 60 patients. The design, type and thickness of tissue approximating materials varied between phantom studies. Image receptor technology, though mostly computed radiography cassettes, also varied between studies.For a single X-ray image of the chest, abdomen, or combined chest/abdomen, at least one of the two fundamental dose metrics was reported in each study:
- 1)Entrance surface (‘skin’) dose (ESD) [Gy], - quantifies radiation incident to the baby's skin,
- 2)Effective dose [Sv] - quantifies risk of long-term effects from radiation by estimating the whole body dose to all organs.
Dosimetry methods included mathematical calculations using X-ray settings and direct measurements using thermo-luminescent dosimetry (TLD) chips or ionization chambers. Various commercial software programs, published conversion factors, and other calculations were utilized to estimate effective dose.
The key findings are summarized in Table 1a, where an empty field indicates that data were not reported. Some studies reported mean values, some medians, and others only the minimum and maximum values. Two phantom studies reported the number of patient X-rays per stay in the NICU where the phantom study was completed.
Table 1aSummary of Literature. Patient entrance surface dose (ESD) and effective dose (E) are per X-ray image, with mean or median and/or range [min,max] as reported by the authors.
| First Author | Country | Year | # X-rays/stay | ESD [μGy] | E [μSv] |
|---|---|---|---|---|---|
| Patient Studies | |||||
| Armpilia | UK | 2002 | 3 | 36 [28,58] | 8 |
| Donadieu | France | 2006 | 11 [0,95] | 13 | |
| Makri | Greece | 2006 | 6 [1,27] | 43 | [10,17] |
| Dougeni | Greece | 2007 | 3 [0,26] | 38 [16,77] | |
| Datz | Israel | 2008 | 8 | 430 | |
| Smans | Belgium | 2008 | 10 [0,78] | 34 | |
| Olgar | Turkey | 2008 | 10 | 70 | [16,27] |
| Puch-Kapst | Germany | 2009 | 4 | [12,15] | 16 |
| Frayre | Mexico | 2010 | >50 | ||
| Toossi | Iran | 2012 | [62,76] | ||
| Iyer | USA | 2013 | 32 [1,159] | 46 | |
| Baird | Canada | 2013 | 17 [0,72] | 53 | 17 |
| Alzimami | Saudi Arabia/Sudan | 2014 | 1 [1,3] | 80 [40,110] | 20 [10,300] |
| Dabin | Belgium | 2014 | 8 | [8,172] | |
| Fernandez | Spain | 2015 | 60 | ||
| Aramesh | Iran | 2017 | 2 [1,3] | [50,80] | |
| Park | Korea | 2018 | 26 | [49,69] | |
| Phantom Studies | |||||
| Jones | UK | 2001 | [56,74] | 36 | |
| Ono | Japan | 2003 | 26 [0,47] | [17,34] | |
| Duggan | Australia | 2003 | [28,46] | ||
| Brindhaban | Kuwait | 2004 | [51,102] | [20,46] | |
| Lacerda | Brazil | 2008 | 4 [0,50] | 75 | |
| Emadelden | Sudan | 2016 | 18 | ||
| Hinojos-Armendariz | Mexico | 2018 | 40 | ||
| Longo | Italy | 2018 | <40 | ||
∗ Dose to neonate in neighboring incubator.
Medians for the reported average ESD and effective doses were 46 μGy and 19 μSv, respectively. In studies where the patients were categorized by birth weight, the smaller the birth weight and lower the age, the longer the NICU stay and the more X-ray images taken,
5
,11
,12
,26
and in some cases the higher per X-ray image dose.11
Conclusions and recommendations from these studies varied greatly, with no consistent patterns in terms of geography or matching level of recommendations with (higher or lower) dose values, as shown in Table 1b. Authors' demonstrated a wide range of interpretations of the ALARA concept and of neonatal risk from X-rays. In order to illustrate these findings, a continuous scale is proposed, with two opposite ends, and middle notch, of the scale defined below. Each of the 25 studies’ set of conclusions and recommendations is represented by one or more different point along the scale, some consecutive and others separate.
Table 1bSummary of Literature. Conclusions and Recommendations reported by the authors as listed in Table 1a.
| First Author | Conclusions | Recommendations |
|---|---|---|
| Patient Studies | ||
| Armpilia | Doses compared favourably with 80 μGy ESD 30 and 50 μGy.31 Risk substantially outweighed. | Take only essential X-rays, collimate carefully. Only have adequately trained staff take X-rays to reduce repeats. Continually assess, review and optimize doses and develop DRLs. |
| Donadieu | Dose was low with regard to environmental exposure and international recommendations. | Assure collimation is used, as it seems difficult to minimize the number of radiographs in this setting. Additional studies are needed to evaluate the possibly lifetime consequences of exposure at this age. |
| Makri | Doses were below 80 μGy, 30 however patient risk increases significantly when number of X-rays are considered. | Avoid unnecessary X-rays and assure exposure per X-ray is minimized. |
| Dougeni | Doses showed good compliance with 50 μGy 31 | Standardise imaging protocols (per weight group) and train specialized staff. |
| Datz | Techniques used and correspondingly doses varied widely across centres. | Optimize techniques and improve collimation to reduce dose. Write national guidelines.Train specialized staff. |
| Smans | Dose is low (below 80 mGy ESD 30 ), however increases quickly if a large number of X-rays are taken. Risk from this is low compared with their other medical risks. | Investigate whether this dose is ALARA? Since techniques are not necessarily optimized for the given equipment type. Teach staff theoretical and practical knowledge to aid improving collimation. |
| Olgar | Doses were acceptable. | Increase distance of infants from each other although scatter contribution is low. |
| Puch-Kapst | Doses were low compared to natural background radiation. | none. |
| Frayre | Doses were higher than 50 μGy 31 | Assess image noise to reduce dose (optimize). Develop reference levels for neonates. |
| Toossi | Doses were slightly higher than others reported. 30 ,31 | Establish local DRLs to help optimize dose and involve medical physicists. Re-train specialized staff. Define national guidelines for neonates. |
| Iyer | Data showed a significant number of X-rays taken during a stay. | Monitor number of X-rays taken to avoid unnecessary exposure. Establish DRLs for this patient population. Determine impact of low dose radiation on this population. |
| Baird | Significant exposure seen in patients with necrotizing enterocolitis during their stay. | Reduce number of X-rays taken by exercising prudence. |
| Alzimami | Doses varied, were higher than other studies due to unsuitable equipment. | Use dedicated imaging equipment with beam filtration for these patients. |
| Dabin | Doses varied between centres; they were usually low (lower than Refs 30 ,31 ), though cumulative dose per stay could be high. Risks were still outweight by medical benefits. | Use suggested DRL of 41 μGy ESD to help reduce dose, harmonize and optimize practice. |
| Fernandez | Doses were well below published recommendations. No apparent risk to staff or adjacent patients. | none. |
| Aramesh | Doses were all below the international standards. | Use proper filtration, kilovoltage, time and collimation to prevent genetic damage. |
| Park | Doses were higher for lower birthweight patients. | Perform additional studies to minimize cumulative dose and achieve optimal image quality, as it is difficult to reduce the number of X-rays taken. |
| Phantom Studies | ||
| Jones | Changing radiographic technique did not lower effective dose. | Use good standards of practice ie collimation, as this is more important than radiographic technique. |
| Ono | Individual dose varied widely among neonates | none. |
| Duggan | Doses can be reduced by following suggested protocols. These may reduce image quality, which is yet to be investigated using clinical images. | Use 0.05 mm hafnium filter at 66 kVp to achieve dose much lower than 80 μGy 30. Take X-ray of chest and abdomen together when both are required, in order to reduce dose. |
| Brindhaban | Patient benefits outweigh the risks of these doses. | Use 60 kV or above, with a minimum filtration of 2.5 mm Al equivalence to minimize patient dose. Explore use of additional collimation (lead sheets on top of incubator) to achieve non-regular field shapes and further reduce dose, |
| Lacerda | Doses were below the 80 μGy 30 and above those from many studies in the literature. | Investigate suitability of X-ray equipment for optimal neonatal X-ray imaging. |
| Emadelden | No excessive doses since they were below 80 μGy 30 ; risk is outweighed by the clinical benefit. | Use 0.5 mm lead rubber to protect brain and gonads of neonates. |
| Hinojos-Armendariz | Dose can be lowered without impacting on image quality. | Optimize by adding 2 mm Al filtration and increasing the tube potential. |
| Longo | For >1 m distance, doses (due to scatter) to adjacent patients is <1 mSv (public annual exposure limit). | Do not using mobile lead shielding to protect adjacent neonates as it may interfere with patient monitoring equipment. |
2.1 End of scale: extensive action recommended – minimize risk to patients
A stringent justification system is already in place to minimize the number of X-rays taken per patient during a NICU stay. Recommendations are to measure, continually assess and review X-ray dose, and optimize equipment accordingly, assuring doses are ALARA. There is a strong demand for a) national imaging protocol for radiographers and other staff who capture NICU X-ray images and/or b) local, national or international diagnostic reference levels (DRLS) for radiation dose per weight group for this unique patient population. This is the most risk-averse interpretation whereby, although doses are reportedly low, the recommendation is for them to be even lower. The increased risk to younger patients is recognized, as is the uncertainty surrounding the extent of the risk to preterm infants specifically. Efforts are being made for radiological safety; however, peace of mind regarding the relative effectiveness of hospital procedures could be provided via evidence-based standards documents.
2.2 Opposite end of scale: take no action – the benefits outweigh the risks
Given the life-threatening complications which these neonates endure and the benefits delivered by X-ray images in the NICU, the risk to the patient is concluded as being low. Risks to staff and adjacent (neighboring) patients are also seen as low. Recommendations for improvements in radiological practice are lacking; however, the need for additional (dose, epidemiological follow-up) studies is recognized by some to evaluate the possible lifetime consequences of exposure to ionizing radiation at this age.
2.3 Middle of the scale: minimal action recommended - reduce risk to patients
For a given NICU patient, a relatively large number of X-rays are taken per day for both routine monitoring and spontaneous checks. Future aims stated for improved radiological safety practice are based around reducing this number of images. Other recommendations include NICU-specific radiographer/technician training, more appropriate X-ray beam collimation and shielding, and keeping neighboring neonates at a distance to avoid scattered radiation to neighbors.
3. No NICU diagnostic reference levels (DRL)
It is only possible to speculate reasons for the varied interpretations of the risks associated with radiation doses to neonates. However, the overarching cause for any reasons will be associated with the lack of evidence-based standardization in clinical practice specifically for neonates. DRLs exist for a range of X-ray procedures for adult sizes, with limited paediatric data,
29
and no NICU data.The NICU has inherent, unique challenges with fitting mobile equipment around life-saving equipment. Setting up for a chest X-ray using static equipment in a general radiography room, even for a newborn patient, does not come with the same challenges.
There are reference dose limits based on general radiography of newborns which do not take into consideration the unique NICU imaging environment or the increased radiosensitivity of premature newborns. The 1996 European Guidelines on Quality Criteria for Diagnostic Radiographic Images in Paediatrics show the criteria for ESD to a newborn as 80 μGy for anterior-posterior (AP) chest X-ray.
30
In 2000 the National Radiological Protection Board published a median chest X-ray ESD for newborns of 50 μGy in Doses to Patients from Medical X-ray Examinations in the UK – 2000 Review.31
Neither of these publications include mobile X-ray imaging of newborns in the NICU. Nevertheless, this review showed that in the last 2 decades, even in recent NICU dosimetry studies, either or both of these dose limits were used as a reference for comparison. In that respect these values are acting as surrogates for NICU DRLS, considered as current standards for NICU doses. The development of NICU-specific DRLs with patients grouped by NICU-specific birthweights is long overdue.A common difficulty with developing paediatric DRLs is the grouping of the children and deciding which metric to use for grouping (weight, height, body mass index, anatomical thickness, etc.). For example, in hospitals where the patient weight is not recorded when the image is taken there are no useful grouping data for DRLs. Average size of patient as a function of age has been experimentally determined to get around this difficulty for paediatrics.
32
However NICU patients are routinely weighed to determine progress in growth; therefore, this grouping metric issue does not apply to the NICU patient group and NICU-specific DRLs could be developed.A special interest project for Paediatric Imaging DRLs (PiDRL) set out to develop paediatric specific DRLs; however, only a draft document was published in 2015.
33
The work package aimed at neonatal examinations with mobile equipment was said in the follow-up (2018) publication to have been completed “as far as possible.”29
The 2018 European recommendations specifically state that the first weight group, <5 kg or neonates, applies to newborn babies but not to those in incubators.29
Therefore, this does not include NICU patients, whose birthweights are generally significantly less than 5 kg. These most recent 2018 European recommendations again quote the same value, 80 μGy for newborn AP chest X-ray. They also suggest it may not be appropriate to establish DRLs for NICU imaging due to the differing types of incubators affecting dose differently.29
4. Technological advancement
With advances in medical technology more neonates are surviving; however, there has been a lack of progress with NICU dose optimization over the last few decades.
34
Twenty years of studies were included in this review in order to highlight improvements made in NICU radiation protection practices over time. Lower doses would be expected in more recent years given the technical improvements in imaging equipment and safety standards over the reported span of time. However, this is not the case as there is no apparent improvement in practice over time. The placement of each study's recommendations for ALARA action on the continuous scale of NICU action recommended does not correspond with its year of publication.Radiographic settings do not reflect changes in image detection technology,
1
and new imaging equipment is not by default optimized for its intended clinical use or particular patient group.35
There has been a change from screen film systems to computed radiography (CR), and since CR is more tolerant of over- or under exposure than screen film systems, unnecessarily high radiation doses can occur with CR compared with screen film.36
Most of the studies included here used CR, with a few screen film systems. Modern NICUs are moving towards cutting edge digital radiography (DR) systems with wireless image receptors, where image quality is inherently different to CR.35
Radiographic settings should have been adapted from screen film to CR, and they should be adapted again when DR becomes the third generation of imaging equipment used in the NICU. Not only does the equipment need to be optimized for its particular generation of image receptor and other technological advances, the X-ray settings must also be optimized for neonatal patient sizes. Future work should take into consideration changes in image receptor technology for future proofing of NICU DRLs.5. Literature review limitations
The purpose of this study was to compare norms for practice around the world with respect to the ALARA concept in neonatal X-ray imaging within the NICU environment. It was not undertaken to compare and contrast X-ray settings or to examine statistical relationships between dose measurements. No meaningful in-depth statistical analysis could be made of the dose measurements given the differences in the reported values and in the dosimetry methods. Entrance air kerma and ESD are combined in Table 1a; the backscatter from such small patients would not be expected to make a significant difference. Average, mean and median values of doses and number of X-rays are also combined in Table 1a. Three studies reported cumulative doses with no per image dose
5
,15
,19
; for these studies, the per image dose was calculated using the average number of images per stay from that study. Some studies separated chest, abdomen and chest/abdomen X-ray images whereas others combined them into a single group; therefore, they are combined in Table 1a. Some studies included measurements such as dose area product (DAP) and energy imparted to the patient; however, these are not included in Table 1a. Overall comparisons between studies for the purpose of this review were only made possible by these simplifications.A comparison of X-ray settings and measured doses in NICU was previously made in a review article by Yu.
37
Although Yu's review was published 10 years ago, studies from the past 20 years (as opposed to 10 years) were included in this review to determine the progress made over 20 years. Only four of the studies herein were included in the review by Yu and are therefore repeated. Half the studies herein are from the first decade and half from the second. Together, they indicate that the recommendations made by Yu 10 years ago have not been addressed, with all studies referencing dose limits from either or both the above-mentioned 199630
and 200031
publications. There are still no NICU DRL's.One effective dose measurement stood out from the others
14
; this is likely because the entrance surface air kerma input into PCXMC to estimate effective dose was 1 mGy; Table 1a shows this is higher than the average ESD value.Other X-ray imaging techniques such as fluoroscopy and computed tomography (CT) are not discussed here; only imaging within the NICU was included. These findings are based on published studies only and therefore may not capture regional nuances within a given country. In any case, these nuances are not required to define broad global patterns. Regional differences
8
,14
,22
in practice stem from national differences, which stem from international differences – hence the concern presented here. Conclusions were drawn from a group of 25 published studies with differing scientific methodologies for a given measurement. Despite these differences, the ESD results from both patient and phantom studies were all within an order of magnitude. Therefore, the methodological differences did not detract from the ability to draw conclusions. On the contrary, these differences instilled greater confidence in the conclusions drawn by offering consistent findings despite the diversity of research design.6. Suggested future work
For each individual chest/abdomen X-ray taken, cancer risk for NICU patients has been shown to increase by 2.5 (male) and 2.9 (female) per million neonates
20
; for 10 X-rays this number increases tenfold. Therefore some of these patients will develop cancer later in life. Given this, risk should be minimized to achieve the public health goals of prevention and harm reduction. The following can help achieve these goals, with greater consistency worldwide in NICU X-ray imaging.Establishing a consistent, user-friendly and accurate method of quantifying radiation dose per image in the NICU would allow for routine measurements and monitoring. This in turn would allow for three outcomes: developing NICU-specific DRLs and performing dose optimization experiments to find a safer dose of X-rays to use and corresponding standardized imaging protocol.
A collaborative working effort between the manufacturers of mobile X-ray systems and incubators, along with medical physics experts, radiographers/X-ray technicians and neonatologists and other relevant clinical staff would allow for the above-mentioned future work to be achieved. A recent example of collaboration between clinicians and manufacturers is the Medical Imaging and Technology Alliance developing improved methods of quality assurance testing of the relatively high radiation dose interventional X-ray equipment used for life-saving clinical procedures.
38
Indications for any X-ray imaging modality must always be considered by the clinician making the request, particularly for neonatal patients. Clinicians should consider why the image is needed and if a different imaging method, such as ultrasound, could be used in its place.
A longitudinal follow-up study of NICU patients would provide statistical evidence of the long-term effects of radiation from medical procedures specifically, rather than using extrapolated atomic bomb survivor data.
2
Similar epidemiology studies have been completed for other high-risk paediatric patient groups include cardiac catheterization39
,40
and CT41
patients.7. Conclusions
This literature review showed that there is no standardized practice at a global level. Interpretations of neonatal cancer risk and corresponding ALARA actions recommended vary from country to country based on local clinical and radiation protection protocols. International recommendations, though published for newborn babies, remain absent for NICU patients, leaving no standard practice or dose measurement for reference. To minimize risk to neonates and achieve greater consistency worldwide in NICU X-ray imaging, the following are proposed: NICU-specific DRLs, standardized dosimetry methods, optimization of settings for equipment and patient size, and standardized imaging protocol.
Declaration of competing interest
The author has no conflicts of interest relevant to this article.
Acknowledgements
Thank you to the NICU staff at Winnipeg Children's Hospital, Canada and Leeds General Infirmary, UK for inspiring this work, and to Professor Allan Kellehear for his support of this article.
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Article info
Publication history
Published online: November 18, 2020
Accepted:
October 30,
2020
Received in revised form:
August 3,
2020
Received:
December 13,
2019
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© 2020 Taiwan Pediatric Association. Published by Elsevier Taiwan LLC.
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