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Original Research |
1 Sezione di Radiodiagnostica, Dipartimento di Fisiopatologia Clinica,
Università di Firenze, Viale Morgagni 85, 50134 Firenze, Italia.
2 Fisica Sanitaria, Azienda Ospedaliera Careggi, Firenze, Italia.
3 Centro di Studio e Prevenzione Oncologica, Firenze, Italia.
4 U.O. Radiologia Diagnostica, Azienda Ospedaliera Careggi, Firenze,
Italia.
5 U.O. Pneumologia, Azienda Ospedaliera Careggi, Firenze, Italia.
Received January 18, 2005;
accepted after revision June 24, 2005.
The Italung-CT Trial is supported by the Health Department of the Tuscany
Region, Italy; and the Ministry of Instruction, University and Scientific
Research of Italy (grant 2003068017).
Abstract
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MATERIALS AND METHODS. We determined the total-body effective dose of different acquisition techniques for one single-detector and one MDCT scanner and made projections about the cumulative radiation exposure to smokers undergoing four annual CT examinations on the same scanners in the Italung-CT Trial. Combining these data with estimates of radiation-induced fatal cancer and of the benefit of screening, we calculated the risk-benefit ratio for participants in the trial, ex-smokers, and never-smokers.
RESULTS. The cumulative effective doses per 1,000 subjects were 3.3 Sv using an MDCT scanner and 5.8 or 7.1 Sv using a single-detector scanner. Potential fatal cancers associated with radiation exposure were 0.11 per 1,000 subjects for MDCT scanners and 0.20 or 0.24 for single-detector scanners, which is about 10-100 times lower than the number of expected lives saved by screening assuming a 20-30% lung cancer-specific mortality reduction in current smokers. They were, however, of similar magnitude to the lives saved by screening in never-smokers and former smokers assuming a 10% efficacy of screening.
CONCLUSION. MDCT is associated with lower radiation doses than single-detector CT technology. The risk of radiation dose in the Italung-CT Trial is compensated for by the expected benefit. CT screening for lung cancer should not be offered to never-smokers, whereas its recommendation in former smokers is debatable.
Keywords: cancer screening • CT • lung cancer • MDCT • radiation exposure • single-detector CT
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The advent of MDCT scanners and updates to the protocol [15, 19] prompted us to investigate the cumulative dose currently delivered to the screened population. For this purpose, we calculated the radiation dose in a pilot study and made projections of the radiation exposure to smokers undergoing four annual CT examinations in a randomized clinical trial named Italung-CT [13], currently in progress. Moreover, we performed a risk-benefit analysis of radiation exposure associated with lung cancer screening for participants in the Italung-CT Trial and for ex-smokers and never-smokers.
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Italung-CT Trial
The Italung-CT Trial is a multicenter randomized controlled study, which
was approved by the local ethics committees of the participating centers,
aiming to evaluate reduction of mortality from lung cancer with CT screening
[13]. It started in 2004 and
will enroll 3,000 smokers 50-70 years old who will be randomized in an active
arm (1,500 subjects) undergoing annual low-dose CT for 4 years and a control
arm (1,500 subjects) who will receive usual care
[13].
Risk-Benefit Analysis
The risk-benefit analysis was performed by two epidemiologists after
approval of the local ethics committee.
Experimental Dose Measurements
Dose measurements were obtained on the single-detector and MDCT scanners
used in the pilot study and in the Italung-CT Trial. The dose at the isocenter
of the scanners was measured using a pencil ionization chamber (10 cm long)
and a read-out multimeter (NEROmAX, Victoreen), and the air CT dose index
(CTDI) was calculated. Several CTDIs at different beam collimations were
measured, and the dose-length product (DLP) involved in each acquisition
technique was obtained. Finally, the dose was computed based on the air CTDI
measured at the isocenter of the scanner using the software, CT-Dose, which
was developed by the Department of Biomedical Engineering, County of Aarhus
and the National Board of Health, Denmark
(www.mta.au.dk/dk/projekter/ctdose/index.htm).
This software provides Monte Carlo simulation based on an anthropomorphic
(Adam and Eve) phantom. The effective (whole-body) dose, as defined by the
International Commission on Radiological Protection (ICRP) 60
[20], and the lung dose were
determined. Three basic CT techniques were assessed: first, low-dose at thick
and thin collimations; second, full-dose at a thin collimation; and, third,
full-dose at a thick collimation. In addition, we estimated the dose of the
preliminary scout anteroposterior view with 120 kVp, 40 mAs, and 2-mm beam
collimation, which can be considered computed projection radiography.
Dose Estimates
Dose in the pilot study—Using the previously described
measurements of the dose associated with the single-detector and MDCT
acquisition techniques, we retrospectively estimated the dose radiation that
was actually delivered to the 60 subjects participating in the pilot
study.
Dose projections in the screened arm of the Italung-CT Trial—The dose projections in subjects undergoing screening for lung cancer in the active arm of the Italung-CT Trial were computed by, first, considering the dose associated with the MDCT and single-detector scanners and protocols used in the Italung-CT Trial [13]; and, second, summing up the dose to subjects with negative tests, the dose to subjects requiring additional follow-up CT examinations, and the dose to subjects requiring intervention. The acquisition techniques for single-detector and MDCT scanners in the Italung-CT Trial are essentially the same as those recommended in the last available ELCAP protocol (icscreen.med.cornell.edu) with some minor differences. In particular, the ELCAP protocol recommends supplemental acquisition of a package of thin-collimation slices at full dose centered on indeterminate nodules when these are found using low-dose, thick-collimation acquisition on a single-detector scanner. Actually, we observed that even low-dose 3-mm-collimation acquisitions obtained on a single-detector scanner with 1.5-step reconstructions provide images with sufficient spatial resolution, and we adopted this technique for lung cancer screening with a single-detector scanner. Nonetheless, for the single-detector scanner, we computed also the dose associated with the previously mentioned ELCAP recommendation. For that purpose, we considered the dose associated with one 20-mm-thick package of thin-collimation slices at full dose centered on a nodule 8 mm in diameter. Additional follow-up CT examinations are recommended in subjects with noncalcified nodules at baseline screening test that are 5 mm or more in mean diameter and new nodules at annual repeat test of 3 mm or more in diameter. The number and the time schedule of such follow-up examinations vary according to the size and the intervening size change of the nodule. We assumed one follow-up examination at 3 months after the initial examination for an indeterminate nodule at baseline and two follow-up examinations at 1, 3, or 6 months for an indeterminate nodule at annual repeat screening examinations.
The frequency of noncalcified nodules at baseline and hence the proportions of subjects with a negative screening test and of subjects requiring follow-up reflect the selection criteria of the screened population and can vary as a function of several factors, including race, age, smoking habits, incidence of granulomatous diseases, and so on [21]. In the CT series reported to date, the frequency of noncalcified nodules at baseline ranged from 5.1% in a Japanese study including nonsmokers [2] to 51% in a Mayo Clinic study [6]. More importantly, this frequency is reduced up to more than one half if a cutoff of 5 mm in mean diameter is used for the baseline screening examination [4, 6, 9, 13, 22]. The incidence of new nodules at annual repeat examinations (all sizes) ranged from 5% in the ELCAP study [3] to 13% in a Mayo Clinic study [6].
For computation of the dose projections in the active arm of the Italung-CT Trial, we used arbitrary values of 10% frequency of subjects showing indeterminate nodules requiring follow-up at baseline and annual repeat screening rounds. Also, the percentage of subjects enrolled in CT screening for lung cancer requiring intervention varies [12, 21]. In the studies of heavy smokers in Western countries, the percentage is consistently below 3% at baseline and repeat screening rounds and is usually lower in the latter [1, 3, 8, 13]. We used an arbitrary value of 1% for the baseline test and 0.5% for the annual repeat test. Before intervention, these subjects usually undergo examinations with additional radiation exposure, including full-dose chest CT before and after IV contrast administration, CT-guided biopsy, and 18F-FDG PET. Although the dose associated with those examinations differs from center to center and from subject to subject, we considered an average effective dose of 15 mSv for subjects examined with MDCT and 20 mSv for subjects examined with single-detector CT, including 7 mSv for the chest PET examination [23]. Computation of the dose in this small fraction of subjects is justified by the fact that benign lesions are definitely found in up to 25% of the subjects undergoing intervention in the context of CT lung cancer screening [8].
The Risk
The radiation-induced risk associated with the CT screening procedure was
assessed combining the experimental dose measurements, the theoretic dose
projections, and the estimates of the radiation-induced cancer deaths
calculated from the English National Radiological Protection Board (NRPB) data
for different age groups [24].
In the same report, sex differences were minor and were neglected here.
Estimate of the Benefit from CT Screening for Lung Cancer
The estimate of the benefit from screening was derived from the expected
incidence of lung cancer in the absence of screening and from the available
predictions of lung cancer-specific reduction of mortality associated with CT
screening [25,
26].
The following assumptions were made. First, we considered a population of 100,000 subjects with one third ranging in age from 55 to 59 years; one third, 60-64 years; and one third, 65-69 years. Second, we performed separate analyses for men and women. Third, we considered a screening program of 4 years with four rounds (one CT screening examination per year), as in the Italung-CT Trial. Fourth, we assumed that the benefit of early diagnosis was limited to all the cancers that would have developed during the years of the screening tests and over the ensuing 4 years, whereas no benefit is assumed after that period. Fifth, we estimated the incidence in our population by smoking attitude (current smokers, ex-smokers, and never-smokers) taking into account the following: first, the age and sex incidence rate of lung cancer in the general population as derived from the local tumor registry for the 1998-2000 period [27] (Table 1); second, the proportion of smokers, ex-smokers, and never-smokers in the Tuscany population (Table 2) [28]; and third, the relative risk for lung cancer of smokers and former smokers in comparison with never-smokers [29] (Table 3). Former smokers were defined as individuals who smoked at least 100 cigarettes over their lives and who now never smoke at all [29].
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To minimize the healthy screening effect for which people undergoing screening have a lower risk in the first years, we assumed that in the first year the expected incidence is one third of that in the general population and in the second year, two thirds. We considered that, without screening, the patients with lung cancer diagnosed in the 8-year period since the beginning of the screening program would have died according to the observed relative survival at 15 years. In this way, we estimated the cumulative number of deaths in the population cohort. We arbitrarily applied to the cumulative number of deaths expected in the population cohort (in the absence of screening) a reduction of mortality of 30%, 20%, 10%, and 0% associated with early diagnosis due to active screening with CT.
Our predictions extend the most favorable and unfavorable sets assumed in a cost-effective analysis by Mahadevia et al. [25]. Those researchers hypothesized a 50% stage shift associated with lung cancer screening and, by weighting the possible influence of confounding factors such as variable adherence to the annual screening regimen and the degree of length bias and overdiagnosis bias, constructed three fundamental scenarios—namely, a base case scenario implying a 13% reduction of mortality, a favorable estimate scenario with a 16% reduction, and an unfavorable estimate scenario with a 4% reduction. Otherwise, based on an analysis of the stages of all cancers detected in the ELCAP and Mayo Clinic observational studies, Patz et al. [26] anticipated that no lung cancer-specific mortality change with screening is expected. It is noteworthy that if CT screening does not modify mortality, the specific lung cancer mortality reduction is 0%.
The number of deaths potentially prevented by screening was estimated taking into account patient sex and smoking habits.
The net benefit of screening was computed as the difference of the number of lives saved minus the number of estimated radiation-induced fatal cancers. This was expressed as a risk-benefit ratio, where a value of 1 implies that the number of lives saved with screening is equal to the number of radiation-induced deaths; a value of 0.1, that the number of lives saved exceeds 10 times the number of radiation-induced deaths; and so on.
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Dose Delivered in the Pilot Study
Two hundred ten CT examinations were performed in the pilot study over 3
years and the low-dose 3-mm-collimation technique was used in 14 examinations
performed on a single-detector scanner.
The cumulative 3-year doses were 53.9 mSv in the 36 subjects screened with the MDCT system (mean exposure per subject, 1.49 mSv/3 y and 0.49 mSv/y) and 141.6 mSv in the 24 subjects screened with the single-detector system (mean exposure per subject, 5.9 mSv/3 y and 1.9 mSv/y).
Dose Projections in the Active Arm of the Italung-CT Trial
The dose projections are detailed in
Table 5. The cumulative
effective dose to the active arm of the Italung-CT Trial was 3.35 Sv per 1,000
subjects over 4 years (0.83 mSv per subject/y) using the MDCT scanner
(low-dose 4-mm collimation, yielding four 1-mm-thick sections) and 5.87 Sv
(1.46 mSv/y) (low-dose 3-mm collimation only) or 7.12 Sv (1.78 mSv/y)
(low-dose 10-mm collimation and one full-dose thin-collimation package) per
1,000 subjects over 4 years using the single-detector scanner.
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The Risk
With the previously described cumulative doses and the estimate of 0.035
fatal cancers for each Sievert for subjects ranging in age from 50 to 70 years
(men and women altogether)
[24], the numbers of lifetime
fatal cancers associated with 4 years of CT screening programs for lung cancer
for subjects 50-70 years old were 11.7 per 100,000 (0.11 per 1,000) for the
MDCT scanner and 20.5 or 24.9 per 100,000 (0.20 or 0.24 per 1,000) for the
single-detector scanner.
The Benefit
Table 6 details the lung
cancer incidence rates in our area estimated for current smokers, ex-smokers,
and never-smokers and different age groups and sex.
Table 7 reports the expected
number of lung cancers in 8 years in a cohort of 100,000 subjects. Based on a
probability of dying within 15 years after the diagnosis of lung cancer equal
to 91% in men and 90% in women
[27],
Table 8 reports the number of
expected deaths from lung cancer in the same area and the same period in the
absence of screening. Table 9
shows the estimates of deaths from lung cancer saved assuming a 10%, 20%, and
30% reduction of specific lung cancer mortality with CT screening according to
sex and smoking habits.
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The Risk-to-Benefit Ratio
Different scenarios may be drawn according to efficacy of screening,
smoking habits, sex of the screened subject, use of single-detector or MDCT
technology, and patient age at the commencement of screening.
In Figures 1A and 1B, the risk-benefit ratios associated with undergoing four annual screening examinations with the MDCT and single-detector scanners (low-dose plus full-dose high-resolution CT) used in the Italung-CT Trial assuming 10%, 20%, and 30% lung cancer mortality reduction are reported for male and female never-smokers, ex-smokers, and current smokers. Assuming a 10% reduction of mortality, the risk-benefit ratio is higher than 1 for male and female never-smokers examined with a single-detector scanner. At the same level of efficacy, the ratio is between 1 and 0.1 for male and female never-smokers examined with MDCT and for male or female former smokers examined with a single-detector or MDCT scanner. The risk-to-benefit ratio for current smokers, assuming a 10% screening efficacy, ranges between 0.32 (females examined on a single-detector scanner) and 0.02 (males examined on an MDCT scanner). Assuming 20% or 30% screening efficacy, the ratio is around or below 0.1 for male and female current smokers examined with either a single-detector or an MDCT scanner.
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The estimation of this radiation-induced cancer risk is difficult. In fact, it is fundamentally based on observational studies of the atomic bomb survivors and radiation workers chronically exposed to low radiation doses and implies several assumptions. In particular, the cancer risk from low-level radiation such as that used for diagnostic radiology procedures has been extrapolated by observations obtained at moderate and high doses using a linear no-threshold relation between the radiation dose and the risk of cancer [31]. However, other scenarios—including the possibility that the linear no-threshold relation underestimates or overestimates the cancer risk from a low radiation dose, the presence of a dose threshold below which the risk is 0, and the possible protective effect of low-radiation dose against cancer (so-called hormetic response)—can be hypothesized based on observational, experimental, and radiobiologic data.
Even adopting a linear no-threshold dose-risk relation, which appears to be the most reasonable and prudent assumption, other variables that can modify the dose-risk relation, such as a theoretic relationship, need to be considered. First is the age of the patient at exposure. In fact, the low-dose radiation-induced cancer incidence generally decreases with advancing age. It is noteworthy, however, that the risk of radiation-induced lung cancer does not seem to show this pattern and peaks at the age of 50-60 years [18]. Second is the temporal profile of the dose exposure. In fact, protracted exposures are associated with lower risks of cancer than those of an acute exposure to the same total dose [18]. This is particularly relevant, but to date unsettled, in the context of screening procedures using X-rays in which a series of low-dose examinations is performed over many years. Third is that the latent period between radiation exposure and cancer death increases with decreasing exposure, and it is possible that for low doses the latent period exceeds the normal life span [31].
To perform a balanced analysis of the harm and gain of diagnostic radiology-related radiation exposure, studies evaluating also the benefit in terms of reduced mortality are needed [32, 33].
There is no proof that CT screening is effective in reducing mortality of lung cancer, but there is consensus that randomized clinical trials should be performed to evaluate this possibility [15]. Because there is no indication supporting the extension of CT screening examinations for life, even for heavy smokers [15, 26], we focused on the risk-to-benefit ratio of radiation exposure in the active arm of the Italung-CT Trial, which is a 4-year clinical trial and is currently in progress [13]. Accordingly, on the scanners used for the CT screening program, we experimentally measured the radiation dose related to the CT acquisition techniques and protocols currently used in this trial. The cumulative dose delivered to subjects undergoing lung cancer screening was calculated in retrospect for a pilot study and as projections for the Italung-CT Trial. For the calculation of the risk of fatal cancer, we used the effective dose [20] and NRPB data [24], whereas for the estimation of the benefit we assessed the number of expected cancers in our area based on the data from the local tumor registry [27]. A range of efficacy of the screening procedure in reducing the mortality of lung cancer of between 0% and 30% was assumed.
For the basic low-dose CT technique, we measured a dose of 0.36 mSv on the MDCT scanner using a 1-mm slice collimation, 120 kVp, and 20 mAs and a dose of 1.1 or 1.2 mSv on the single-detector scanner using a 3- or 10-mm collimation, 140 kVp, and 43 mA. Although a small increase in the peak kilovoltage—for instance, from 120 to 140 kVp—implies an increase in the dose of about 30% on the single-detector scanner we used, this change was necessary to improve the image quality, taking into consideration the characteristics of the detectors and time of rotation of the single-detector scanner of our study. Nishizawa et al. [17] experimentally calculated an effective dose of 3.6 mSv for the basic CT examination technique. However, they used a single-detector mobile scanner with 100 mAs and a table speed of 10 mm—that is, pitch of 1 and 10-mm-collimation slices. Diederich and Lenzen [14] reported an effective dose of 0.3 mSv for men and 0.55 mSv for women on a single-detector scanner (10- or 5-mm collimation, pitch of 2, 25 mAs).
Our data indicate that MDCT technology enables considerable dose savings as compared with single-detector CT technology. This is especially true if one considers that low-dose thin-collimation acquisitions with 1- to 1.5-mm reconstruction can obviate supplemental full-dose thin-collimation packages. A similar dose saving can be obtained in the case of a single-detector scanner if low-dose 3-mm-collimation acquisitions are used.
At variance with prior studies [14, 17, 18] in the calculation of the radiation dose associated with lung cancer screening, we included the additional exposure related to follow-up and interventional CT examinations required in the management of suspected nodules. The considerable dose associated with such additional examinations was previously emphasized [26, 34]. To calculate dose projections for participants in the Italung-CT Trial, we considered the dose exposures with current single-detector and multidetector technology, the percentages of nodules requiring follow-up and intervention reported in the literature, and the last ELCAP protocol and management recommendations. In particular, we adopted a cutoff value of 5 mm in mean diameter for an indeterminate nodule at baseline requiring follow-up and a restricted number of follow-up CT examinations—namely, one examination for nodules detected at baseline screening and two examinations for nodules initially detected at annual repeat screening rounds. The mean cumulative 4-year doses for 1,000 screened subjects examined on an MDCT scanner were 3.3 Sv (0.83 mSv/y per subject) and 5.8 Sv (1.46 mSv per subject); the dose was 7.1 Sv (1.78 mSv per subject) for those examined on a single-detector scanner.
The lower dose exposure associated with the adoption of MDCT technology for lung cancer screening programs was confirmed in the pilot study, in which the mean annual dose per subject was 0.49 mSv for MDCT and 1.9 mSv for single-detector CT. Although no definite studies are yet available, preliminary data (personal unpublished observation) indicate that with the newer MDCT scanners (12, 16, > 16 detector rows) low-dose thin-collimation acquisition techniques recommended for lung cancer screening will provide dose exposures similar to those of the 4-MDCT scanner of our study.
To calculate the risk of radiation associated with lung cancer screening with CT, we used the total-body (effective) dose and adopted the estimates of lifetime radiation-induced fatal cancer from English NRPB publications, in which data are stratified according to age at exposure and in which the effect of sex is minor [24].
Pending results of randomized trials, the estimate of the potential benefit of lung cancer screening with CT in reducing the specific mortality rate is speculative and controversial [1-3, 9, 19, 26]. In our analysis of the benefit of screening in terms of reduction of specific lung cancer mortality, we covered a range of between 30% and 0% screening efficacy [25, 26], the most favorable estimate being similar to that of mammographic screening for breast cancer [35]. The additional assumption was made that the 4-year mortality rate of lung cancer outside a screening program is so high that it can be considered equivalent to the incidence.
In the present analysis, we applied the assumptions discussed earlier to the expected number of lung cancers based on current incidence rates in our area provided by the local tumor registry and on the Italian estimate on relative risk of current smokers in comparison to ex-smokers and nonsmokers.
In calculating the risk-benefit ratio related to the radiation exposure in lung cancer screening with CT, besides the estimated efficacy of the screening procedure in reducing lung cancer-specific mortality, the interaction of several variables related to risk and benefit must be taken into account. In particular, because the incidence of lung cancer and the potential benefit of screening differ according to smoking habits, age, and sex, the risk-to-benefit ratio of radiation exposure related to lung cancer screening with CT varies accordingly.
For male and female current smokers participating in a 4-year program, such as the Italung-CT Trial, our data indicate that assuming lung cancer-specific mortality reduction of 10-30% with CT screening, the benefit of screening overcomes the risk associated with the radiation exposure. Our data also indicate that this favorable ratio, ranging from 0.32 (in women examined on a single-detector scanner with a 10% screening efficacy) to 0.007 (in men examined on an MDCT scanner with a 30% screening efficacy), is more pronounced in elderly smokers who show the highest incidence of lung cancer.
Conversely, our data indicate that even a 4-year screening program with CT is not indicated for subjects with a low risk of lung cancer such as never-smokers, with a risk-benefit ratio ranging from 1.66 (women examined on a single-detector scanner with a 10% screening efficacy) to 0.08 (men examined on an MDCT scanner with a 30% screening efficacy).
In former smokers, the situation is intermediate, but it is noteworthy that for a screening efficacy of 10% the ratio is between 0.25 and 0.87 with either CT technology for women and men. The estimate of lung cancer risk in former smokers is difficult to calculate owing to the controversial definition of this category and its presumable heterogeneity and to the uncertainties about the change over time of the lung cancer risk in subjects who quit smoking. Our data seem to indicate that some caution should be exercised in initiating lung cancer screening programs in former smokers, and that in such a case a keen understanding of the individual risk and of the specific risk categories is necessary.
Although it is possible that extension of CT screening to more than 4 years will increase the benefit more than the risk in heavy smokers, we did apply our analysis to the typical regimen of screening used in ongoing randomized clinical trials—namely, annual CT examination for a few years [11].
If CT screening does not affect mortality, subjects participating in CT screening programs have no benefit of radiation exposure and only a possible detrimental effect due to radiation-induced cancers. This assumption enables us to assess the risk associated with lung cancer screening in a simpler way than when some degree of efficacy is assumed. Several considerations are needed to properly weigh the risk of radiation-induced cancers in subjects participating in annual CT screening programs for lung cancer. In fact, one has to consider the interaction between radiation exposure for the lung and other factors in modifying the risk of lung cancer. In particular, it was reported that the interaction between X-ray radiation and smoking could imply a multiplicative effect [18]. Moreover, recent data showed that the risk of radiation-induced lung cancer does not decrease with increasing age at exposure [18]. On the other hand, there is considerable uncertainty about the time needed for development of radiation-induced cancer after X-ray exposure for lung cancer screening, but it can reasonably be estimated in terms of many years. It is conceivable that most subjects will receive in the meantime considerably higher doses of radiation for diagnostic or therapeutic procedures due to current diseases [30].
In conclusion, MDCT technology is associated with lower radiation doses than single-detector technology and is recommended for lung cancer screening with CT. However, even a 4-year annual screening with an MDCT scanner implies a nonnegligible dose exposure and a risk of radiation-induced fatal cancer. The amount of this risk—in consideration of the uncertainties of the benefit of screening in terms of reduction in specific lung cancer mortality—can equal or even dominate the spontaneous lung cancer incidence and mortality in nonsmokers in Western countries. Studies of lung cancer screening with CT should be restricted to current smokers, and their extension to former smokers is debatable.
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