Radiation Dose Issues in Longitudinal Studies Involving
John R. Mayo1,2
Vancouver General Hospital, Vancouver, British Columbia, Canada; and 2University of British Columbia, Vancouver, British Columbia, Canada
Computed tomography (CT) examinations are increasingly used for These capacities have made CT an invaluable diagnostic and
clinical diagnostic and research purposes, as they provide in vivo research tool, accounting for the explosive growth of CT exami-
anatomic information similar to that provided by gross anatomy. In nations in the last 20 years. It is estimated that in 2006 more than
conjunction with physiologic maneuvers or contrast media, CT 62 million CT scans were obtained in the United States, as
may also provide in vivo physiologic information. Using calibrated compared with about 3 million in 1980 (1). Similar increased
acquisition protocols, accurate noninvasive measurements of tissue utilization has been reported in studies from the United Kingdom
density, air volume, blood volume, and capillary perfusion can be
(2) and Canada (3). Research studies are also increasingly using
performed. Serial CT scans can provide longitudinal measurements
serial CT examinations for the noninvasive evaluation of disease
indicative of disease progression or regression, allowing noninvasive
assessment of treatment effects. However, the X-ray radiation
progression and treatment effects.
associated with CT has been associated with a small but signiﬁcant However, the increased utilization of CT comes with a price:
increased risk of malignancy, which may be fatal. Large studies have increased population radiation exposure. In most cases, adding CT
detected this small risk, which appears to be related to the cumula- to diagnostic imaging algorithms substantially increases patient
tive radiation dose of all previous exposures in a linear fashion. It has X-ray radiation exposure. For example, a chest CT examination
been shown that the risk from a given radiation exposure is greater in (3–6 mSv) delivers 60 to 120 times more radiation dose compared
young people and females compared with older males. The combi- with a postero-anterior (PA) chest radiograph acquired using ﬁlm
nation of these two risk-enhancing factors, found in pregnant (z0.05 mSv) or 90 to 180 times that of the same view obtained
females, provides the greatest risk. Radiation risk decreases with using digital radiography (z0.03 mSv). In addition, since CT is so
increasing age for both men and women, asymptotically approach- available and easy to perform, it is liberally applied to exclude
ing zero. Radiation risk can be calculated using dose metrics pro- potentially serious but statistically unlikely diagnoses, often solely
vided on current CT scanners as outlined in this article. Ethically, to reassure anxious patients and clinicians. In the chest, serial CT
given that radiation is associated with measurable risk, clinically studies are widely employed to assess disease progression in
indicated and research CT examinations must provide an increase in
chronic obstructive pulmonary disease (COPD), interstitial lung
knowledge that has substantial beneﬁt to the subject. This beneﬁt
disease, and cystic ﬁbrosis. Repeated CT scans are often employed
should be related to the potential of saving of life or to the pre-
to follow suspicious lung nodules in patients at risk for lung cancer.
vention or mitigation of serious disease.
The net result of these actions is greatly increased CT utilization
Keywords: radiation dose; computed tomography; longitudinal studies; and population radiation dose. It is noted that in some cases CT
cancer risk replaces examinations with higher dose (e.g., bronchography for
bronchiectasis, nuclear medicine ventilation perfusion scintigra-
The invention and rapid development of computerized tomo- phy followed by pulmonary angiography for suspected pulmonary
graphy (CT) is one of the major medical advances of our time. embolism) while providing equivalent or superior diagnostic
Current multidetector CT scanners can image the entire chest in information, but these situations are in the minority.
2 to 5 seconds, producing up to 1,000 slices, each composed of The increased radiation dose of chest CT compared with the
sub-millimeter isometric voxels. These high signal to noise ratio, PA chest radiograph arises from two properties of the CT
large ﬁeld of view images provide noninvasive anatomic evalua- technique (4). First, unlike analog ﬁlm radiography, in which
tion of the chest with information content similar to that achiev- the image acquisition and display are both reliant on the ﬁlm, CT
able at autopsy. In vivo physiologic functional information is a digital technique in which image acquisition and display can
regarding pulmonary and systemic perfusion or gas transport be independently manipulated. Therefore, when CT dose is
can be obtained by acquiring CT images while administering excessive, the image does not become too dark (as it does in ﬁlm
intravenous contrast media or performing breathing maneuvers, radiography), but instead improves because of decreased image
respectively. Expert radiologic interpretation of these images can noise (5). Second, visualization of image noise is enhanced by the
differentiate diseases that are indistinguishable on history and ability to map the entire visible gray scale onto a selected segment
physical examination but demonstrate unique changes at the of the CT number scale. As a result, image degradation due to
gross anatomic level. Using standardized and calibrated acquisi- quantum noise (mottle) is easily visible and interferes with image
tion protocols; accurate noninvasive measurements of tissue interpretation. At high noise levels, images may be clearly non-
density, air volume, blood volume, and capillary perfusion can
diagnostic. However, at lower noise levels more subtle image
be performed. After validation of surrogate outcome measures,
degradation occurs which may lead to diagnostic inaccuracies or
serial CT scans can provide longitudinal measurements of disease
a lack of conﬁdence in image interpretation, effects that are
progression and treatment effects.
difﬁcult to detect and measure. Image noise also affects the
accuracy of measurements made on chest CT images (e.g.,
assessment of the extent of emphysema). Failure to standardize
(Received in original form August 4, 2008; accepted in ﬁnal form September 23, 2008)
acquisition protocols and account for equipment speciﬁc differ-
Correspondence and requests for reprints should be addressed to John R. Mayo, ences in noise levels can lead to systematic errors in measure-
M.D., Department of Radiology, Vancouver General Hospital, 899 West 12th
ments that may introduce errors in surrogate measures of disease
Avenue, Vancouver, BC, V5Z 1M9 Canada. E-mail: John.Mayo@vch.ca
activity and progression.
Proc Am Thorac Soc Vol 5. pp 934–939, 2008
DOI: 10.1513/pats.200808-079QC In the absence of standardized validated protocols, radiolog-
Internet address: www.atsjournals.org ists often obtain CT images using high radiation exposure levels to
Mayo: Radiation Dose in CT 935
minimize image noise and maximize image quality. Studies in stochastic risk (10). Stochastic risks are believed to be cumulative,
multiple jurisdictions have shown that the lack of standardization with increasing risk seen over successive exposures.
leads to wide variation in the level of radiation administered for Subjects exposed to the atomic bomb explosions in 1945 have
the same CT examination between institutions (2, 3), with no been extensively studied in the last 60 years. This group is unique
detectable difference in patient outcomes. In addition, studies since it is large, covers all ages, and was not selected on the basis of
have shown that radiologists, referring clinicians, and patients underlying disease. A substantial portion of the survivors re-
may be unaware of the high level of radiation exposure associated ceived less than 50 mSv, a low level of exposure that approximates
with CT examinations (6). This knowledge gap undoubtedly the dose range delivered by multiple chest CT exams. The major
contributes to the overuse of CT in low-yield diagnostic situations negative effect seen in this group is an increase in the number of
and its overuse in following disease progression or treatment cancers over that found in a nonexposed population. An earlier
effects. presentation of cancers has not been observed. However, to
In the early 1990s, concern was raised regarding radiation dose assess the risk from a single chest CT scan requires extrapolation
in chest CT (7–9). The authors of these early studies suggested of these results to even lower doses, and the nature of this
that greater consideration needed to be given to optimizing CT extrapolation has proven to be highly controversial.
exposures and ensuring appropriate clinical use guidelines on the Disagreement regarding the extrapolation of nuclear explo-
single detector row CT scanners in use at that time. These early sion data is based on three nonresolvable issues: uncertainty in
warnings were not heeded, and the last 15 years have been char- the actual radiation exposure received, since on-site radiation
acterized by ever-increasing CT utilization. The increased utili- dose measurements were not obtained; differences in the natural
zation of CT has been hastened by the development of multi- cancer risk of the Japanese population compared with other
detector row CT scanners, leading to expanded clinical indications populations; and the different quality of the radiation imparted by
for CT examinations (e.g., pulmonary embolism, cardiac gated atomic bombs compared with X-ray–based medical imaging. As
CT angiograms [CCTA], trauma CT). This has fueled an increase a result of differences in interpretation, learned societies have
in both the number of installed scanners and the number of come to varying conclusions on the risk attributable to radiation
patients scanned per shift. These advances have served to further exposure at the levels found in chest CT. The International
increase population CT radiation exposure. The development of Commission on Radiological Protection, or ICRP, used a linear
evidence-based guidelines governing the use and technical no-threshold extrapolation of nuclear explosion data and esti-
parameters for CT is required to responsibly use this valuable mated 50 additional fatal cancers induced per million people
diagnostic test. exposed to 1 mSv of medical radiation (11). In contrast, the
The purpose of this review is to outline (1) evidence indicating French Academy of Science concluded that there was not
the detrimental effect of radiation dose at the level administered sufﬁcient evidence to support an increased cancer risk associated
in chest CT examinations, (2) parameters that affect CT radiation with radiation exposures less than 20 mSv (12), a level above that
dose, (3) advances in dose reduction in the chest CT, and (4) the delivered in chest CT examinations (, 6–11 mSv). Further con-
interaction between CT radiation dose and diagnostic accuracy. ﬂicting evidence on the impact of low-level radiation exposure is
A complete review of radiation dosimetry and bioeffects is found in tissue culture experimental studies that have shown
beyond the scope of this review. induction of free radical detoxiﬁcation mechanisms with low-
level radiation exposure (13). This has led some to suggest that
low-level radiation exposure may be beneﬁcial, an effect known
as radiation hermesis. Finally, the long-term study of the mortal-
ity of British radiologists showed lower cancer mortality than
There has been considerable debate within the medical commu- predicted by the atomic bomb data (14). It is postulated that this
nity regarding the risk of low-level radiation exposure from CT. may be accounted for by the healthy worker effect, the beneﬁcial
The reason for this debate arises from an incomplete knowledge effects of dose fractionation, or overestimation of the dose
of the complex link between ionizing radiation and future neg- received by these physicians.
ative outcomes in humans. In broad overview, the negative In 2007, additional important data were added to this debate
outcomes of ionizing radiation in humans can be divided into (15) when the 15-country study reported the cancer induction
two major categories that can be separated on the basis of time effect of low-level radiation exposure studied in 407,000 radi-
and exposure: deterministic effects seen immediately after large ation workers followed for over 20 years providing 5.2 million
exposures, and stochastic effects seen after a long latent period person-years of follow-up. This study is unique as it reports on
(6–25 yr) and associated with low exposures. the largest cohort to date, has accurate dosimetry, and in-
Deterministic effects, skin erythema, skin necrosis, and hair vestigated multiethnic workers. Ninety percent of the subjects
loss only occur above a threshold dose that lies well above those received a dose less than 50 mSv and on average each worker
administered in diagnostic chest CT examinations. In medical received a dose of 19 mSv. Therefore this study is focused on
imaging, deterministic dose levels are only seen in complex low-level doses, close to that received during a single chest CT
interventional cases using large quantities of ﬂuoroscopy time. examination (6–11 mSv). The authors reported an excess rela-
These effects will not be discussed further in this review. tive risk (ERR) for all-cause mortality of 0.42 per Sievert
By comparison, stochastic effects are believed to have no (0.00042 per mSv), with a statistically signiﬁcant increasing
radiation dose threshold, and therefore are associated with the excess relative risk with increasing radiation dose (P , 0.02)
low radiation doses delivered during chest CT. Mechanistically, indicating a dose–response effect. The increased risk in all-
stochastic effects are believed to be mediated by chemical dam- cause mortality was mainly due to an increase in mortality from
age to the DNA molecule and clinically manifest as an increased all cancers.
risk of cancer and genetic defects. Stochastic effects occur A subanalysis stratiﬁed by dose categories (less than: 400,
randomly and the risk of their occurrence depends on the type 200, 150, and 100 mSv) showed that cancers in the highest dose
of ionizing radiation administered, the tissue receiving the categories did not drive the risk estimates. Therefore, this study
radiation, and the age of the subject. It is believed that dose supports the concept that there is a small cancer risk from low-
fractionation, a substantial modiﬁer of detrimental effect for dose radiation delivered in CT examinations. These new data
deterministic radiation doses, does not substantially modify the add supportive evidence to the concern over radiation dose
936 PROCEEDINGS OF THE AMERICAN THORACIC SOCIETY VOL 5 2008
delivered in chest CT examinations and support the use of the TABLE 1. METHODS OF QUANTIFYING IONIZING RADIATION
ALARA principle (As Low As Reasonably Achievable) for
these exams. Method Conventional Units of Units, or SI
However, there are limitations to these new data. Because
workers were studied, there is no information on the effect in Radiation exposure Roentgens (R) Coulombs per kilogram (C/kg)
Absorbed dose Rads (rad) Grays (Gy)†
children; and since 90% of the workers were men who received
Equivalent dose Rems Sieverts (Sv)‡
over 98% of the cumulative dose, minimal information is avail- Effective dose Effective dose
able on the effect in women. The largest excess mortality from all equivalent (Sv)*
contributing countries is found in the data from Canada, and
statistical signiﬁcance is lost if this cohort is not included. Finally, Abbreviations of the units of measure are in parentheses.
* 1977 tissue-weighting factors.
the largest discrepancy between this study and the atomic bomb †
D multiplied by ICRP radiation weighting factor WR. The WR for x rays is 1.
cohort arises in the lung cancer mortality, suggesting that the ‡
1990 tissue-weighting factors.
confounding effects of smoking may have been inadequately Reprinted by permission from Reference 37.
The inﬂuence of age at exposure and of sex has been studied body risk estimate or be used to facilitate comparisons between
in the nuclear explosion cohort, showing that radiation risk is examinations in different parts of the body. Equivalent dose is
substantially modiﬁed by these subject factors (16, 17). The a modiﬁcation of absorbed dose that incorporates weighting
increased radiation sensitivity of children is felt to arise from factors to account for the different biologic effect of various
two biological facts: they have more time to express the cancer- sources of radiation. For X-rays, the radiation weighting factor
inducing effect of radiation and they have more rapidly dividing is 1 and the equivalent dose has the same numerical value as
cells than adults which are inherently more radiation sensitive. absorbed dose.
It has been found that women have approximately twice the Effective dose is a further reﬁnement of radiation dose
risk compared with males for the same level of radiation ex- measurement that estimates the whole body dose that would be
posure. Increased female risk is heightened in chest CT by the required to produce the same stochastic risk as the partial body
presence of radiosensitive breast tissue in the radiated ﬁeld. dose that was actually delivered in a localized CT scan. It is useful
Radiation dose to breast tissue in chest CT examinations has because it allows comparison of CT dose to that delivered in other
been calculated (18) and directly measured (19, 20), with reports medical examinations. Effective dose is calculated by summing
showing wide variation in average values, ranging from 10 to the absorbed doses to individual organs weighted for their ra-
70 mGy. The variation in values is related to CT parameter diation sensitivity (11). The measurement unit is the sievert (Sv)
settings, differences in size and conﬁguration of breast tissue, and or milli-sievert (mSv). Since effective dose requires determina-
methods to calculate or directly measure radiation dose. There is tion of absorbed dose to each body organ multiplied by their
no debate that all CT-associated breast radiation dose values are radiation sensitivity, the distribution of radiation dose in the body
substantially greater than the average glandular dose of 3 mGy for must be determined. Chest CT has a markedly asymmetric dose
standard two-view screening mammography. It is important to distribution, with higher dose found peripherally and lower dose
note there is a strong age at exposure effect for breast tissue, with centrally due to the shielding effects of body tissue. This makes it
lower risk for subjects above the age of 40 (21). These factors must difﬁcult to calculate the exact effective dose for each patient.
be taken into account in setting chest CT radiation dose param- Instead, a simpler calculation is performed (Figure 1). Scanner
eters in CT chest examinations for women. Breast shields, thyroid
shields (22, 23), and X-ray tube current modulation techniques
have been employed to decrease radiation dose to these super-
ﬁcial and radiosensitive tissues within the chest. These techniques
have been shown to decrease breast radiation exposure delivered
in chest CT scans. However, these dose-modifying techniques
must be used with consideration of their impact on image quality.
RADIATION DOSE MEASUREMENT
There are many methods currently in use for quantifying ionizing
radiations (Table 1) (24). The fact that several methods exist
attests to the complexity of this issue. The simplest parameter,
radiation exposure, is determined by measuring ionization in air
caused by the X-ray beam. The measurement unit is coulombs per
kilogram (abbreviation, C/kg). It has limited clinical value, as it
does not take into account the area irradiated, the penetrating
power of the radiation, or the radiation sensitivity of the irra-
diated organs. From radiation exposure we can calculate the skin
entrance dose, which is important when examining deterministic
effects such as skin erythema. Although deterministic effects are
not encountered in routine CT, they are of potential concern in
CT ﬂuoroscopy. A more reﬁned measurement is absorbed dose,
determined by measuring the energy absorbed per unit mass
within an object. The measurement unit is the gray (abbreviation,
Gy). Unlike radiation exposure, the gray is dependent on the
composition of the object or subject placed in the radiation beam. Figure 1. Diagram shows algorithm for the estimation of radiation
However, absorbed dose does not account for the differing exposure risk from computed tomography (CT) using the metric of
radiation sensitivity of organs, and it cannot provide a whole- effective dose.
Mayo: Radiation Dose in CT 937
manufacturers use dose data derived from measurements made in These serve as a guide to those planning or evaluating research
head and body phantoms to determine a weighted CT dose index (e.g., ethics committees). Research radiation exposure is divided
(CTDI) for each CT scanner model at all available selections of into four categories (I, IIA, IIB, and III) corresponding to
tube voltage (kVp), tube current (mA), and rotation time. The effective dose limits of less than 0.1 mSv, 0.1 to 1mSv, 1 to
selected pitch value is then incorporated to produce a CT dose 10 mSv, and over 10 mSv. The increasing dose limits in the four
index called the CTDIVOL. Once the scan length is determined categories are related to increasing potential beneﬁt from the
from the topogram, the appropriate CTDIVOL is combined with research as indicated by the category guidance notes: I, expected
the actual length scanned in the patient to calculate the dose to only increase knowledge; IIA, increase in knowledge leading to
length product (DLP). Since the administered radiation dose is a health beneﬁt; IIB, increase in knowledge aimed directly at the
linearly related to the length scanned in the patient, technologists diagnosis, cure, or prevention of disease; III, increase in knowl-
should ensure that the scanned volume is conﬁned to the region of edge to have substantial beneﬁt and usually directly related to the
interest to avoid excessive radiation dose. saving of life or the prevention or mitigation of serious disease. In
The DLP is a measure of the radiation dose delivered to that addition, these research guidelines account for the substantial age
patient during the scan. An estimated effective dose for the variation in radiation sensitivity allowing an increase by a factor
speciﬁed CT scan can be calculated by multiplying the DLP of 5 to 10 for subjects over 50 years old and decreasing the limits
value by the normalized effective dose coefﬁcients (Table 2) for by a factor of 2 to 3 for children. It is noted that research that
the scanned body part. This normalized effective dose coefﬁ- involves serial radiologic investigations must calculate the cumu-
cient accounts for the radiation sensitivity of the body region lative radiation dose over the course of the study to determine the
scanned based on exposed organ radiosensitivities. The DLP exposure category.
value is displayed on the scanner console once the topogram has
been obtained and the scan prescribed. In chest CT, multiplying RADIATION DOSE REDUCTION
the DLP by 0.017 allows the radiologist or technologist to
calculate the estimated effective dose of the examination before Reduction in CT radiation exposure results in increased image
scan acquisition. The DLP value can be archived in the picture noise and decreased image quality. Studies assessing the sub-
archiving and communication system (PACS) by storing the jective evaluation of chest CT scans have demonstrated that
protocol page. Newer DICOM standards for CT enable the radiologists consistently gave higher image-quality scores to
storage of dose data in the DICOM header of each examination. images obtained with a higher radiation dose (30, 31). Image
It is noted that effective dose, while easy to calculate and noise can be measured by placing a region of interest (. 100 pixels)
convenient, is also an imperfect dose descriptor. Since tissue- in an area of uniform density (e.g., the thoracic aorta). The
weighting factors are averaged over sex and age, effective dose standard deviation of the pixel values represents image noise and
risk assessment is appropriate to a 30-year-old hermaphrodite. is a measure of the uncertainty of quantitative CT measures. It is
An alternate approach has been described (25) that uses mea- noted that the choice of reconstruction algorithm affects image
sured or calculated organ radiation doses, applies them to age- noise, with higher noise associated with high-spatial-frequency
and sex-speciﬁc organ risk estimates (from the BEIR 7 report) reconstruction algorithms (e.g., bone or lung algorithms) com-
and calculates an effective risk from the examination. Effective pared with low-spatial-frequency algorithms (e.g., standard, soft-
risk would attempt to estimate the risk of developing cancer from tissue algorithm). Since high-spatial-frequency reconstruction
the partial body irradiation of the examination. It would not algorithms are most commonly used to assess bones or lung
consider hereditary effects that are currently embodied in the parenchyma, tissues with high radiographic contrast, increased
effective dose calculation. Effective risk could be adjusted for age noise is usually not a diagnostic problem. However, increased
and sex. Although this is a new approach requiring further noise may interfere with quantitative measures of disease such
evaluation, it has the potential to improve communication of as computer-calculated emphysema scores. New adaptive re-
the risk from CT radiation exposure to patients and physicians. construction algorithms are being developed that can decrease
Radiation dose surveys have noted wide variations in DLP image noise, providing improved image quality at lower radiation
settings for identical examinations between institutions (2, 3, 26, dose. These advanced algorithms should facilitate radiation dose
27). To decrease this variation and protect the public from in- reduction.
advertent overexposure, the European communities have pub- Radiation dose can be adjusted at the time of image acquisi-
lished suggested reference dose values (28) for chest CT exami- tion by changing the X-ray tube current or voltage and the scan
nations, with a DLP value of 650 mGy cm. This reference dose time. In practice, the tube current is most frequently adjusted to
value was obtained by surveying a large number of institutions in change the radiation dose and image noise. In most CT scanners,
Europe and adopting the 75th percentile of responses as the the tube current is adjustable in steps from 20 mA to approxi-
reference dose values. This value serves as a guide to acceptable mately 400 mA. Decreasing the tube voltage also decreases the
practice. radiation dose, but also affects subject contrast and can impact CT
The European Commission has also provided guidelines for number measurements. Finally, radiation dose is linearly related
radiation exposure in medical and biomedical research (29). to the scan time. However, in most cases scan time is minimized to
reduce motion artifact. It is noted that the radiation exposure
delivered at a given tube voltage and current setting will vary
TABLE 2. DOSE LENGTH PRODUCT TO EFFECTIVE DOSE greatly between CT scanners of different models and manufac-
CONVERSION COEFFICIENTS turers because of differences in scanner geometry (X-ray tube-to-
patient separation) and X-ray tube ﬁltration.
Study E/DLP (mSv/mGy cm)
In the past, the tube current of CT scanners was uniform at all
Head 0.0023 angles around the patient and for the full longitudinal (cranial
Chest 0.017 caudal) extent of the scan. However, the chest is an elliptical
Abdomen 0.015 object that has higher attenuation from left to right than from
anterior to posterior. Attenuation also varies as the chest is
scanned cranial to caudal because of the shoulders. CT image
Deﬁnition of abbreviations: DLP 5 dose length product; E 5 effective dose. quality is disproportionately degraded by views with few photons
938 PROCEEDINGS OF THE AMERICAN THORACIC SOCIETY VOL 5 2008
(photon starvation) compared with the image quality improve- Since children, young adults, women, and pregnancy have been
ment associated with views with high photon counts. To address shown to increase radiation sensitivity, the most strident dose
this issue, manufacturers have introduced programs that adjust reduction efforts should be focused on these groups. Finally, it is
the tube current depending on the attenuation of the object in noted that the complexity of CT requires a close collaboration
both the transverse (x, y) and longitudinal (z) directions to between radiologists and medical physicists to successfully re-
minimize either photon-starved or photon-rich projections, max- duce radiation dose while maintaining diagnostic accuracy.
imizing image quality while minimizing radiation dose. This tube
Conﬂict of Interest Statement: J.R.M. does not have a ﬁnancial relationship with
current modulation technique has been shown to produce a sub- a commercial entity that has an interest in the subject of this manuscript.
stantial reduction in radiation dose (32–34) with minimal degra-
dation of image quality. Routine use of dose modulation systems
is recommended, as they compensate for asymmetry in the size
and density of the body section being scanned, resulting in
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