Published online March 1, 2006
PEDIATRICS Vol. 117 No. 3 March 2006, pp. 882-888 (doi:10.1542/peds.2005-0817)
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SPECIAL ARTICLE

Cumulative Effective Doses Delivered by Radiographs to Preterm Infants in a Neonatal Intensive Care Unit

Jean Donadieu, MD, PhDa, Abdelkrim Zeghnoun, PhDa, Candice Roudier, MSca, Carlo Maccia, PhDb, Phillipe Pirard, MDa, Christine André, MDc,d, Catherine Adamsbaum, MDc,d, Gabriel Kalifa, MDc,d, Paul Legmann, MDc,e and Pierre-Henri Jarreau, MD, PhDc,,f

a Département Santé et Environnement, Institut de Veille Sanitaire, St Maurice, France
b Centre d'Assurance de Qualité ds Applications Technologiques dans le Domaine de la Santé (CAATS), Bourg la Reine, France
c Université Paris-Descartes, Faculté de Médecine, Assistance Publique-Hôpitaux de Paris, Paris, France
d Service de Radiologie Pédiatrique, Hôpital Saint-Vincent-de-Paul, Université Paris-Descartes, Paris, France
e Service de Radiologie A, Hôpital Cochin, Paris, France
f Service de Médecine Néonatale de Port-Royal, Hôpital Cochin, Paris, France


   ABSTRACT
TOP
 ABSTRACT
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. We sought to determine the number and distribution of radiographs and the cumulative effective radiograph doses (cED) received by a population of preterm infants (PIs) hospitalized in an NICU.

STUDY DESIGN. We reviewed the files of all preterm infants (gestational age: <34 weeks) who were admitted to an NICU during an 18-month period and were discharged alive. A generalized additive model was used to study the relationship between cED and patient characteristics.

RESULTS. Four hundred fifty files were analyzed. The median gestational age was 30.1 weeks (range: 24.1–33.9 weeks), and the median birth weight was 1250 g (range: 520–2760 g). The median number of radiographs per infant was 10.6 (range: 0–95), and the median cED was 138 µSv (range: 0–1450 µSv). The cumulative dose exceeded 500 µSv in 7.6% of the cases. Factors that influenced the cumulative effective dose were gestational age, birth weight, care procedures, and clinical adverse events.

CONCLUSIONS. Given the potentially life-threatening complications of PIs, cumulative radiograph doses received in the ICU seem low with regard to environmental exposure and international recommendations. Additional studies are needed to evaluate the possible lifetime consequences of exposure to ionizing radiation at this age.

Key Words: ionizing radiation • preterm infants • exposure • intensive care

Abbreviations: ED—effective dose • cED—cumulative effective dose • RDS—respiratory distress syndrome • BPD—bronchopulmonary dysplasia • CPAP—continuous positive airway pressure • CT—computed tomography • CI—confidence interval

Recent articles mention growing concerns about the long-term effects of radiation exposure during infancy and childhood.1,2 Over the last 20 years the vital prognosis of preterm infants, and particularly those born before 34 weeks' gestation, has improved dramatically,3 mainly thanks to treatment in specialized units, respiratory support, and parenteral nutrition. Approximately 1.5% of live births in Western countries occur before 34 weeks' gestation. Diagnostic radiology plays an important role in the intensive care setting, raising questions as to the potential impact of radiograph exposure at this age and particularly the risk of oncogenicity.

The small size of premature infants brings more organs into the radiograph field, potentially resulting in a higher effective dose (ED) than in adults.

Only a few studies published since 1990 have examined the distribution of the number and doses of radiographs in neonates,4–10 and only 3 have provided information on preterm infants.11–13 This prompted us to study the number of radiographs performed in an NICU together with the cumulative ED (cED) received. We then correlated this information with clinical characteristics that commonly depict stays in the NICU.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Population
The NICU of Port-Royal (Cochin Hospital, Paris, France) is a level III NICU located in a tertiary perinatal center including an 80-bed maternity unit that specializes in high-risk pregnancies. Between January 1, 2002, and June 30, 2003, 821 infants were admitted to the NICU. The medical charts of 485 infants born before 34 weeks' gestation were retrieved for this study. The files of patients who died in the ICU (n = 28) and those with missing radiograph films (n = 7) were excluded from the analysis.

Data Collection
The following information was collected from each chart: gestational age, birth weight, early-onset infections, late-onset infections, main pulmonary disorders (eg, respiratory distress syndrome [RDS] and bronchopulmonary dysplasia [BPD]), gastrointestinal complications such as feeding intolerance and necrotizing enterocolitis, and persistent ductus arteriosus. The distribution and duration of the following major medical interventions were recorded also: mechanical ventilation, nasal continuous positive airway pressure (CPAP), oxygen supplementation via a nasal cannula, and central venous catheter implantation.

Radiographs
All radiograph films, including those of inadequate quality, were stored in the patients' medical charts. Only a few single radiographs could have been lost from a given patient's file, thus only slightly underestimating the doses for these individuals. Each radiograph film was reviewed by 2 experienced investigators who classified them into 1 of the following 6 categories: babygrams (radiograph field including at least both chest and abdomen); chest radiographs (radiograph field limited or slightly exceeding the chest region); abdominal radiographs (radiograph field centered to the abdominal region including or not the gonads); and head and limb radiographs.

Radiograph Dose Evaluation
In the NICU, radiographs were taken with a mobile radiograph device, the settings of which (kilovolts and milliamperes) are determined by the radiographer according to the infant's weight. The mobile radiograph device used during the study period was a Mobilett Plus EH Siemens (Munich, Germany) single-phase generator. Agfa (Mortsel, Belgium) medium-sensitivity screen film was used. The doses received by the infants (entrance surface dose and ED) were calculated by the PCXMC software program (STUK-Radiation and Nuclear Safety Authority, Helsinki, Finland), which simulates energy deposition (Monte Carlo calculation) in different organs depending on the morphologic characteristics of the patient (weight and size).14–16

For each premature infant, the overall cumulative dose was calculated by taking into account the number and types of examinations performed during the NICU stay. Because most of the radiographs were performed during the initial days of hospitalization and the variation in the absorption coefficient was moderate with regard to the infant's weight, all radiograph doses were calculated by using the birth weight. The ED was expressed in microsieverts (µSv). Initially, the individual ED was assessed for each radiograph, then the total cED was calculated by summing up the number of radiographs taken for each patient.

Very few patients had computed tomography (CT) scans (n = 3 [0.6% of patients]). Head CT scans were performed in 2 patients, and head and abdomen CT scans were performed in 1 patient. The ED of each CT scan was assessed, taking into account all the physical parameters (kilovolts, milliamperes, rotation time, number of slices, and slice thickness). Impactscan 0.99W software (www.impactscan.org) was used to asses the ED received during these examinations.

Statistical Methods
In addition to standard descriptive statistics, a generalized additive model with penalized regression splines17 was used to investigate determinants of the cED. This approach permits adjustments for possible nonlinear effects of continuous variables. Potential variables were tested with Akaike's information criterion. The final model was adjusted for the variables found to influence the goodness of fit, that is, continuous variables (birth weight, gestational age, duration of central venous catheter use and of mechanical ventilation, length of stay in the NICU) and binary (yes/no) variables (feeding intolerance, necrotizing enterocolitis, mechanical ventilation, nasal CPAP, oxygen supplementation). To normalize the distribution of the residuals, the cED was first log-transformed. All analyses were performed by using the mgcv library implemented in R software.18


   RESULTS
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 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Demographic and Medical Data
During the study period, 450 newborns meeting the inclusion criteria were admitted to the NICU. The gender ratio was 1. Median gestational age was 30.1 weeks (range: 24.1–33.9 weeks). Median birth weight was 1250 g (range: 520–2760 g). The median length of NICU stay was 16 days (range: 1–246 days). RDS was diagnosed in 41% of the cases and always treated with surfactant. Early-onset infections occurred in 17% of the cases. Ventilatory support was provided in 80% of the cases, initially with mechanical ventilation (53%; median duration: 3 days; range: 0.04–58 days) or nasal CPAP (27%; median duration: 5 days; range: 0.01–246 days). Most patients who received mechanical ventilation subsequently received nasal CPAP. Overall, a central venous line was used in 72% of the cases, for a median of 18 days (range: 0.1–120 days). Ninety infants were discharged directly from the hospital, whereas 390 infants were first transferred to a secondary care unit. All infants were free of respiratory support at hospital discharge, but most still required nutritional support (parenteral or enteral). The main medical characteristics of the patients from admission to discharge are shown in Table 1.


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  		TABLE 1 Characteristics and Major Morbid Events of the 450 Premature Infants (<34 Weeks' Gestation) Who Were Admitted to the NICU During an 18-Month Period

 
Distribution of Radiographs and ED Per Patient and Distribution of the Radiograph Fields
The median number of radiographs per patient was 10.6 (range: 0–95). The median cED equivalent was 138 µSv (range: 0–1450 µSv). The distribution of radiographs and of the cED (Fig 1) was highly asymmetrical. Only 7.3% of the patients had >30 radiographs, and only 7.6% received a cED >500 µSv. Table 2 shows the frequency of the different types of radiographs according to term and the corresponding EDs. Babygrams represented approximately half of all radiographs overall and a higher proportion in highly preterm infants. A large proportion of chest radiographs included additional organs (mainly part of the abdomen). Overall, the field of the radiographs appeared to be more precise as birth weight and gestational age increased. Table 3 shows the calculated radiation doses received by various organs, according to gestational age. The most exposed organs were the thyroid, the liver, the breast, the lung, and the gonads. The bone marrow received, on average, a dose 5 times lower than the other organs, and brain exposure was very low.


Figure 1
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  		FIGURE 1 Distribution of EDs among all patients (n = 450) below 34 weeks' gestational age (median: 138 µSv).

 

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  		TABLE 2 Distribution of Radiograph Type According to Gestational Age and Dose per Radiograph

 

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  		TABLE 3 Median Organ Dose (µSv) According to Gestational Age

 
Clinical Determinants of the cED
Schematically, the lower the birth weight and gestational age, the more severe the clinical situation, as reflected by more frequent use of respiratory support and parenteral nutrition and longer hospital stays. A regression model was used to take all these parameters into account. The main statistical difficulty in designing the model was the very close relation between birth weight and term: the 2 variables provided almost the same information (correlation coefficient: 0.8; degrees of freedom: 449; P < .001). The final model included 445 subjects (data were missing for 5 patients), and excluded gestational age, based on the Akaike's information criterion scores.

The following variables were not significantly associated with the cED: gender, RDS, BPD, persistent ductus arteriosus, early-onset infection, and late-onset infection. In contrast, the cumulative dose was 29% higher (95% confidence interval [CI]: 15–45%) in infants with feeding intolerance and 62% higher (95% CI: 18–123%) in those with necrotizing enterocolitis. Table 4 lists the variables that are significantly associated with the cED.


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  		TABLE 4 Determinants of the cED (n = 445)

 
This model showed that the cED was relatively high in infants who weighed <1200 g and fell rapidly as birth weight rose (Fig 2 A). As expected, the dose increased with the length of stay (Fig 2 B), although it tended to plateau after ~90 days.


Figure 2
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  		FIGURE 2 Variation of the cED, with regard to birth weight (A) and duration of NICU stay (B) plotted following the penalized regression spline function. The central line is the mean value, and the 95% confidence interval is depicted by the lower and upper lines.

 
The dose also increased with the number of medical procedures, especially central catheter insertion (152%; 95% CI: 118–193%), nasal CPAP (36%; 95% CI: 21–53%), mechanical ventilation (32%; 95% CI: 18–48%), and oxygen supplementation (14%; 95% CI: 1–29%). Finally, the dose rose significantly with the duration (per day) of catheter use (0.6%; 95% CI: 0.0–1.2%) and mechanical ventilation (2.1%; 95% CI: 1.3–2.9%).

Respiratory disorders (RDS and BPD) did not seem to influence the cumulative radiograph dose, but the information carried by these diagnoses is probably included in the notion of respiratory support and its duration. In contrast, the cumulative dose was 29% higher (95% CI: 15–45%) in infants with enteropathies and 62% higher (95% CI: 18–123%) in those with enterocolitis.


   DISCUSSION
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The main objective of this study was to obtain information on the radiation dose received by premature newborns who undergo radiographs in an NICU.

Although the methods used to estimate the cED did not include "in vivo" measurements, all the relevant physical parameters such as the standard radiographic settings of the machine, the actual size and weight of the newborns, and the radiograph field size were considered.19 It should be noted that the ED was calculated on the basis of birth weight and not body weight at the time of radiograph exposure. However, this approximation has a limited impact on the cED equivalent, a previous study having shown that most radiographs received by newborns are delivered during the first days after admission to the ICU.13 In the worst-case scenario, this bias would tend to overestimate the dose received by newborns with the lowest birth weight. A second limitation is that most of these infants were subsequently transferred to a secondary care unit, where they may have undergone other radiographs. However, as stated above, the need for radiographs is maximal during the first days of the NICU stay, and the clinical stability of the infants who were transferred would have limited the need for new radiographs.

We found that median cumulative dose was moderate (138 µSv). The dose distribution was highly asymmetric: only 34 patients (7%) received a dose >500 µSv, and only 4 patients (0.8%) received a dose >1000 µSv; the maximum dose received was 1450 µSv. In the 3 patients who underwent CT scans, the cEDs resulting from conventional radiographs were 528, 378, and 359 µSv, whereas the EDs resulting from the CT scans were 16000 (head and abdomen), 2880 (head), and 2400 (head) µSv, respectively.

Published data on radiographs in neonates are scarce and mainly deal with dosimetric issues.4–7,9,20,21 To date, only 3 studies have evaluated the frequency distribution of radiographs in this setting together with a measure or calculation of the dose. The largest study evaluated the frequency of radiographs in 2408 infants admitted to a Japanese NICU.12 The median number of radiographs per patient was related to the birth weight and term. The EDs were not calculated. The frequency of CT examinations was quite high, with 940 infants receiving 1012 scans. In a United Kingdom study,11 the distribution of radiographs was analyzed in 55 neonates born before 34 weeks' gestation. An asymmetric distribution was observed, with a median number of 5 radiographs per patient (compared with 10.6 in our study). The median cED (40 µSv) was also lower than in our study (138 µSv). Such differences might be explained by differences in clinical severity, medical management, or sampling. A US study13 involved 25 surviving neonates with birth weight <750 g who were admitted to an NICU over a 1-year period. The median number of radiographs per child was 31, and the mean cumulative dose was 720 µSv; these values are slightly higher than among the 35 corresponding neonates in our study (median: 26 radiographs per patient; mean cED: 497 µSv).

Despite the differences among published studies, our results confirm that the cumulative effective radiograph dose received by NICU patients seems moderate and is within the range of doses of environmental ionizing radiation received over a similar period.22

It is noteworthy that a single CT scan of the head delivers >10 times the median ED resulting from all standard radiographs in a given infant, whereas combined CT scans of the head and abdomen deliver ~30 times this dose. However, CT scans were rare in our study (<1% of patients), as they were in the United Kingdom study. In contrast, in the US and Japanese studies, 12% and 40% of the infants, respectively, had CT scans.

Despite these reassuring results for the dose delivered by radiographs, other aspects of neonatal exposure to ionizing radiation should also be considered. The ED relies on individual organ-absorption coefficients, which depend on morphologic parameters. Each organ, therefore, has a specific coefficient of radiosensitivity. For a given energy, the absorption coefficient depends not on age but solely on body size. Animal studies have suggested that premature newborns have increased radiosensitivity,23 but few data on premature infants are available. The Oxford Survey Children Cancer case-control study of risk factors for cancer in childhood showed that obstetric radiographs increased the risk of malignancies, including leukemia.24 However, despite an increased risk of cancer according to the number of radiographs received in utero, these studies failed to show that human newborns were particularly radiosensitive, at least at doses <5 mGy. The cohort study of newborns of mothers irradiated at Hiroshima is also inconclusive in this respect.25–27 Epidemiologic studies of perinatal risk factors for leukemia and other cancers have yielded contradictory information on the association between prematurity (or low birth weight) and malignancies. Most failed to show an association,28,29 but some showed a positive correlation.30,31

The risk of exposure should be interpreted with regard to the uncertain vital prognosis of highly premature neonates. As expected, higher ED equivalents were associated with major outcomes and medical interventions. We focused on morbid events, the clinical consequences of which (mainly respiratory or digestive) potentially indicated radiograph examination. Infections and persistent ductus arteriosus were not associated with the cumulative dose. It is more surprising that major respiratory disorders (RDS and BPD) did not seem to influence the cumulative dose, but the association between the received dose and nasal CPAP or oxygen supplementation, which themselves do not require radiograph monitoring, tends to confirm this finding. In contrast, gastrointestinal disorders were strongly associated with the cumulative radiograph dose. We also observed a continuum of variations between birth weight and the ED equivalent, although the relationship was not linear: around a threshold weight of 1200 g, the cED started to diminish as birth weight increased (Fig 2 A). Finally, as expected, factors that reflect the intensity of medical management and its monitoring (mechanical ventilation and central catheter use) strongly determined the dose of the radiographs.


   CONCLUSIONS
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
The more severe the neonatal morbidity of premature infants (which is tightly correlated with gestational age and birth weight), the higher the radiograph dose received in the NICU. Considering that the prognosis of highly premature infants has improved dramatically thanks to progress in intensive care, it seems difficult to minimize the number of radiographs in this setting. However, given the uncertainties surrounding the precise radiosensitivity of extremely premature newborns, it seems logical to try to minimize radiograph exposure, notably by limiting the radiograph field or by using shielding techniques. Indeed, a large proportion of the radiographs analyzed here included both the thorax and the abdomen and sometimes were more extensive. Finally, it is also important to recall that the use of CT scans should be minimized in this population.


   ACKNOWLEDGMENTS
 
This work was supported by a grant from the Direction Générale de la Sûreté Nucléaire et de la Radioprotection.

We thank David Young for editorial assistance.


   FOOTNOTES
 
Accepted Jul 25, 2005.

Address correspondence to Jean Donadieu, Département Santé et Environnement, Institut de Veille Sanitaire, 12 Rue du Val d'Osne, 94415 Saint Maurice Cedex, France. E-mail: j.donadieu{at}invs.sante.fr

The authors have indicated they have no financial relationships relevant to this article to disclose.


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 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics



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