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Click here to read this article as a CME activity
a Division of Thoracic Surgery, New York Presbyterian Hospital, Weill Cornell Medical College, New York, New York
b Department of Surgery, New York Presbyterian Hospital, Weill Cornell Medical College, New York, New York
c Department of Radiology, Mount Sinai School of Medicine, New York, New York
Accepted for publication March 7, 2011.
* Address correspondence to Dr Stiles, Division of Thoracic Surgery, Department of Cardiothoracic Surgery, Ste M404, Weill Medical College of Cornell University, 525 E 68th St, New York, NY 10021 (Email: brs9035{at}med.cornell.edu).
Presented at the Forty-seventh Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2011.
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Abstract |
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Methods: We identified 94 consecutive patients undergoing resection for non-small cell lung cancer. Radiologic procedures performed from one year prior to resection until two years postresection were recorded. Estimates of effective doses (mSv) were obtained from published literature and institutional records. Predictors of dose greater than 50 mSv per year and greater than 100 mSv per three years were examined statistically.
Results: The majority of patients (median age = 67 years) had stage IA cancer (52%). In the three-year period, patients had 1,958 radiologic studies (20.8/patient) including 398 computed tomographic (CT) scans (4.23/patient) and 211 positron emission tomography (PET) scans (2.24 per patient). The three-year median estimated radiation dose was 84.0 mSv (interquartile range, 44.1 to 123.2 mSv). The highest dose was in the preoperative year. In any one year, 66% of patients received more than 50 mSv, while 19% received over 100 mSv. Over the three-year period, 43.6% of patients exceeded 100 mSv. The majority of the radiation (89.8%) was from CT or PET scans. On multivariate analysis, a history of previous malignancy (odds ratio [OR] 3.8; confidence interval [CI] 1.14 to 12.7), postoperative complications (OR 6.16; CI 1.42 to 26.6), and postoperative surveillance with PET-CT (OR 13.2; CI 4.34 to 40.3) predicted exposure greater than 100 mSv over the three-year period.
Conclusions: This study demonstrates that lung cancer patients often receive a higher dose of radiation than that considered safe for healthcare and radiation workers. The median cumulative dose reported in this study could potentially increase the individual estimated lifetime cancer risk by as much as 0.8%. Although risk-benefit considerations are clearly different between these groups, strategies should be in place to decrease radiation doses during the preoperative workup and postoperative period.
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| General Thoracic Surgery:
The Annals of Thoracic Surgery CME Program is located online at http://cme.ctsnetjournals.org. To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal.
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| Dr David Yankelevitz is a named inventor on a number of patents and patent applications relating to the evaluation of diseases of the chest including measurement of nodules. Some of these, which are owned by Cornell Research Foundation (CRF), are non-exclusively licensed to General Electric. As an inventor of these patents, Dr Yankelevitz is entitled to a share of any compensation which CRF may receive from its commercialization of these patents.
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Exposure to low-dose ionizing radiation from medical imaging procedures may be associated with the development of solid tumors and leukemia [1]. Although there is uncertainty in existing prediction models, the BEIR VII (seventh Biologic Effects of Ionizing Radiation) report predicts an average lifetime attributable risk of 1 radiation-induced cancer per 100 patients receiving a 100 millisievert (mSv) effective dose of radiation; a lifetime risk conversion factor for an individual of 0.0001 per mSv [1]. Therefore healthcare workers with repeated radiation exposure are typically monitored so that their cumulative effective radiation dose does not exceed 100 mSv over five years or a maximum dose of 50 mSv in any given year [2]. In contrast, monitoring of radiation exposure in individuals subjected to repeated medical imaging procedures is rarely done.
Patients undergoing surgery for newly diagnosed non-small cell lung cancer (NSCLC) usually undergo many diagnostic imaging procedures. Despite the potential risks, the radiation dose from such procedures is typically not monitored. Because most radiation-induced cancers develop many years after exposure, life expectancy must be considered when weighing the risk of radiation exposure against the substantial potential benefits derived from the imaging procedures required for diagnostic and surveillance purposes. However, certain groups of NSCLC patients, particularly younger patients with potentially curable early stage disease, may be at risk to suffer the detrimental effects of radiation exposure over time. The purpose of this study was to estimate the cumulative effective doses of radiation in patients undergoing lung cancer resection and to determine the predictors of increased exposure.
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Patients and Methods |
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Procedures were categorized by year including the preoperative year (PRE), postoperative year one (PO1), and postoperative year two (PO2). Postoperative radiographic surveillance at our institution typically consists of a posteroanterior and lateral chest radiograph done at two weeks after discharge and at approximately 3, 9, and 18 months postoperatively [3]. Computed tomography (CT) of the chest without intravenous contrast is routinely performed at 6, 12, and 24 months postoperatively and yearly thereafter. In 2006, we initiated an Institutional Review Board approved prospective trial evaluating the role of fusion PET-CT scans (performed every 6 months for two years) in addition to standard CT scans in the postoperative surveillance of lung cancer patients. Forty-six patients (48.9%) from the current cohort had been enrolled in that study. This review was approved by the Institutional Review Board with a waiver for informed consent.
Effective Radiation Dose
Effective dose is a descriptor designed to reflect the overall detrimental biologic effect of radiation exposure [4]. It is calculated as the sum of each organ's radiation dose weighted to reflect the type of radiation and the relative risk of radiation-induced carcinogenesis in that organ. Effective dose calculations allow for comparisons across different types of imaging procedures. Estimates of effective doses in mSv were obtained from the published literature and institutional protocols and records [5]. Table 1
demonstrates the estimated effective dose values of the most common imaging procedures performed in this study. For individual patients, total effective dose was calculated yearly and for the three-year period based upon the imaging procedures each patient underwent.
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Comparison of continuous variables was conducted using the paired or unpaired Student t test or Wilcoxon rank sum, respectively. Standard deviations and interquartile ranges are presented with these values. Subgroup comparisons of categoric variables were performed using the ÷2 test or Fischer exact test. Adjusted odds ratios for clinical predictors were determined using multivariate logistic regression and are reported with 95% confidence intervals as a measure of the precision of these estimates. All p values are two-sided with statistical significance evaluated at the 0.05 alpha level. All analyses were performed in SPSS Version 18.0 (SPSS Inc, Chicago, IL).
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Finally, for PO2, adjuvant therapy and PET-CT surveillance were both predictors of exposure greater than 50 mSv. Of patients receiving adjuvant chemotherapy 42.3% (11 of 28) got greater than 50 mSv of radiation, versus 22.1% (15 of 68) of patients not receiving further therapy (p = 0.05). The median exposure of the two groups, however, was not statistically different (26.6 mSv vs 10.5 mSv, p = 0.309). For patients followed with PET-CT surveillance (n = 46), 45.7% received greater than 50 mSv radiation, compared with 10.4% of patients not on the PET-CT surveillance protocol (p < 0.001). Median doses in PO2 were 44.4 mSv versus 0 mSv, respectively (p < 0.001). The 0 mSv likely reflects poor capture of radiologic studies as noted above. Mean doses in PO2 were 42.5 mSv for the PET-CT surveillance group versus 13.9 mSv for the group not under surveillance (p < 0.001).
For the entire three-year period, the cumulative exposure exceeded 100 mSv for 43.6% of patients (n = 41). Factors temporally associated with increased exposure as described above were used to construct a multivariate logistic regression model for the endpoint of exceeding 100 mSV. History of a previous malignancy, postoperative complications, and PET-CT surveillance emerged as independent predictors; adjusted odds ratios and 95% CIs are presented in Table 6. For patients with another malignancy (n = 24), the median radiation dose for the three-year period was 127.4 mSv versus 77 mSv in those without (n = 70, p = 0.003). For patients with postoperative complications (n = 16), the median radiation exposure was 132.8 mSv versus 80.2 mSv in patients (n = 78) without postoperative complications (p = 0.037). Finally, as stated above, patients undergoing PET-CT surveillance (n = 46) got significantly more radiation exposure over the time period than patients (n = 48) not on the surveillance protocol (median of 124.3 mSv vs 63.3 mSv, respectively, p < 0.001).
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Comment |
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In the current study, the data suggest that patients undergoing lung resection for NSCLC are subjected to variable cumulative radiation doses during the perioperative period, some upwards of 100 mSv. Our patients had a median exposure of 84.0 mSv over a three-year period. Using BIER VII estimates, this may increase the lifetime attributable risk of developing a radiation-induced cancer by as much as 0.84%. It is therefore important to understand the implications of exposure to low-dose ionizing radiation and to define factors associated with increased exposure in this patient population.
Although chest radiographs were by far the most commonly performed imaging procedure (60.6%) in our cohort, their contribution to total exposure was minimal (0.7%). Indeed, the overwhelming majority of exposure was from CT and PET-CT scans. While such imaging procedures have undoubtedly contributed to improvements in the diagnosis and staging of lung cancer, their utility in the follow-up of patients after resection of NSCLC is less well documented [11, 12]. It has been our practice to obtain chest CT scans every six months after resection in the first year and yearly thereafter. That is reflected by the data in the current study showing that patients received an average of 3.64 chest CT scans per patient. We do not routinely obtain PET-CT scans, though these are often performed in the setting of expected recurrence or in patients who are receiving adjuvant therapy. Due to what we perceived to be a potential benefit of PET-CT scans in the follow-up of NSCLC patients, we had begun a protocol in 2006 enrolling patients in a PET-CT surveillance program. In the current study, with 48.9% of patients enrolled in the PET-CT surveillance program, the entire cohort received an average of 2.24 PET-CT scans per patient.
In addition to diagnostic CT and PET-CT scans, CT-guided biopsies were also a potential significant source of radiation exposure [13]. In our cohort, 66 such procedures were performed. Due to variations in length of the procedure and in the number of images obtained, it is much more difficult to estimate the effective dose of biopsy procedures. However, based upon our own institutional data with a well-established biopsy program, we estimated it to be only 2 mSv. Other significant sources of radiation included nuclear cardiac studies, typically obtained in the preoperative period. Although only constituting 1.2% of the total studies, they contributed 8.4% of the total radiation exposure.
Although the current study has identified relatively high radiation exposure in NSCLC patients undergoing lung resection, clearly a risk-benefit consideration must be taken into account given the expected poor disease-specific survival in the patient cohort. Five-year overall survival can be estimated to be 73% for stage IA cancers, 58% for stage IB, 36% to 46% for stage II, and 9% to 24% for stage III [14]. Additionally, the excess relative risk of radiation-induced cancers is thought to decrease with advanced age [15]. Furthermore, although it is not well established how quickly radiation-induced cancers will arise, it is generally accepted that the occurrence of such cancers occurs after a long latency period. All of these factors would seem to suggest that perhaps radiation-induced cancers may not be a significant threat to this group of patients. In our cohort, the median age was 66.5 years. However, the majority of patients were stage IA (52.1%) or IB (23.4%), and so can have a reasonable expectation for long-term survival. Additionally, it is conceivable that the risk of radiation-induced cancer and the time to occurrence may be underestimated in this patient population with demonstrated genomic instability, and in many cases with a known field effect secondary to tobacco exposure. It is therefore important to identify patients at risk for high exposure, to improve documentation of exposure, and where possible, to identify means to limit further exposure.
Several factors were apparent which appeared to identify patients at risk for exposure greater than 50 mSv per year or greater than 100 mSv for the three-year period. Patients with a history of an additional malignancy other than NSCLC can be expected to undergo more imaging procedures throughout their life. These patients had a significantly higher likelihood of receiving radiation greater than 50 mSv in the PRE and were more likely to receive greater than 100 mSv throughout the study. Given their demonstrated predisposition to cancer, these patients should be considered as particularly high risk for radiation-induced tumors. Patients undergoing extensive cardiac imaging procedures were also more likely to have doses exceeding the threshold we described. Such procedures have previously been documented to lead to high radiation exposure in the general population [16]. Given the tendency to repeat many of these studies in at-risk patients, this cohort should also be considered to be at higher risk for radiation-induced malignancies, although the cardiac comorbidities may limit long-term survival. In the year immediately after surgery (PO1), it was not surprising that patients suffering from complications were more likely to undergo more imaging procedures and be exposed to more radiation. Potential postoperative complications are often evaluated by CT scans. They may also lead to interventional radiologic procedures. In PO2, adjuvant chemotherapy also predicted exposure greater than 50 mSv. This is expected as these patients typically are followed more closely for recurrence and generally receive more postoperative CT and PET-CT scans.
Perhaps the most notable risk factor for increased radiation exposure in our study was enrollment in a PET-CT surveillance program. We had initiated this program at our institution in response to a perception on our part that patients with NSCLC were being increasingly followed with PET-CT imaging, both internally and by outside referring physicians. The study was designed to determine the incidence and characteristics of abnormalities on postoperative PET-CT surveillance studies and to prospectively determine the incidence of recurrent or new primary lung cancer diagnosed by PET-CT. At present we have not analyzed the data with respect to the long-term aims of that proposal. In the current study, however, we documented an almost twofold increase in radiation exposure in these patients followed liberally with PET-CT. Although PET-CT scanning is frequently practiced in the postoperative surveillance of NSCLC patients, to our knowledge there is no evidence that it has any benefit over other imaging strategies. Given the high radiation doses apparent in our patient population in which 89% of PET-CT surveillance patients exceeded 50 mSv in a 12 month period and 69.6% exceeded 100 mSv for the three-year period, we believe that there needs to be evidence that performing this test provides a sufficient benefit to justify the additional risk before it can be made part of routine surveillance.
While half of our cohort was enrolled in a PET-CT surveillance protocol, the other half, who were followed with a more standard surveillance protocol, still had substantial radiation exposure. This protocol relies predominantly on plain chest radiographs and noncontrast chest CT. Such a CT-based surveillance protocol is relatively standard practice in the care of most NSCLC patients. Of these patients in our study, 43.8% still exceeded 50 mSv in a given 12-month period while a remarkable 18.8% exceeded 100 mSv for the entire study period. Their median dose of exposure (63.3 mSv) could increase their lifetime risk of cancer by as much as 0.63%. If anything, radiation exposure was underestimated in this population as many were lost to documented radiographic follow-up after one year.
An improved understanding of the risks of radiation is needed among healthcare providers [17]. Patients with any of the risk factors suggested in our study should be identified as having the potential for higher radiation exposure and subsequently as being at higher risk for the development of radiation-induced malignancies. In some patients the risk-to-benefit profile may justify the potential risks of no imaging or of imaging with a potentially less accurate technique delivering less radiation. With technological advances, it may become possible to delineate patient-specific doses for each imaging study performed and to include them in an electronic medical record, facilitating identification of patients with large cumulative doses.
Methods should also be considered to curtail radiation exposure. Attempts should be made to limit the number of preoperative CT and PET-CT scans and in particular to avoid repeat studies at different imaging centers. There are now also technical improvements in CT scanners allowing for dose reduction. Such techniques should be applied whenever possible. Low-dose scans, such as those performed in CT screening studies which have doses in the range of 1 mSv, may also be considered as alternatives to the standard dose scans typically used for surveillance. In addition, preoperative lung and cardiac nuclear imaging procedures should not be performed on a routine basis and should only be obtained when deemed a clinical necessity. Care should be taken in the performance of preoperative CT-guided biopsies [13]. Opportunities also exist in the postoperative time period for limiting radiation exposure. It is our practice to obtain chest radiographs every third month and chest CT scans every sixth month. This practice would typically generate an exposure of 28.4 mSv. The addition of yearly PET-CT scans would give a further estimated dose of 50 mSv over the time period of the study. Although surveillance CT scans, recommended by both National Comprehensive Cancer Network and American College of Chest Physicians guidelines, arguably may help to identify recurrent disease and second primary tumors, neither postoperative surveillance CT scans nor PET-CT scans have been shown to improve survival after resection of NSCLC.
This study has two major limitations. The first is in regard to effective dose estimation. It is derived from a sum of the equivalent doses to tissues and organs that are considered to be radiosensitive. However, several uncertainties exist in the conversion from a radiologic dose to an effective dose based upon differences in tissue densities, compositions, and radiation attenuations. These differences are further amplified by differences in patient sex, age, and size. Therefore it is thought that risk estimate models may either underestimate or overestimate effective dose by a factor of 2 or 3 [1]. Doses may also differ based upon the type of imaging equipment or upon institutional imaging protocols. In our estimates we sought to produce conservative estimates of effective dose based upon those reported in the literature and upon our own institutional data, with a goal of avoiding overestimation. It is also possible that current risk-estimation models overestimate the risk associated with low-dose radiation. Limits placed upon healthcare and radiation workers are highly conservative by nature, made in a population without a chance of benefit from the radiation they receive, as opposed to those receiving the potential benefit from a medical procedure.
In our study, it is also certain that we failed to capture numerous imaging procedures performed on the cohort of patients. Although every attempt was made to collect all imaging procedure reports, both from our own institution and from outside facilities, we undoubtedly missed procedures that were not entered into the electronic medical record. As a tertiary referral center, many of our patients obtain their imaging studies at outside imaging facilities or institutions. Additionally, although we selected a cohort of patients from 2006, our follow-up was still incomplete with the median radiologic follow-up of 571 days. Although alive at 24 months, 41% of patients had no documented radiologic studies in PO2. Most of these patients undoubtedly had some sort of imaging procedures during this period, results of which were not documented in our institutional electronic medical record. This therefore led to an underestimation of the number of studies and of the radiation exposure in the current cohort.
In conclusion, this study demonstrates that lung cancer patients often receive a higher dose of radiation than that considered safe for healthcare and radiation workers. The median cumulative dose reported in this study could potentially increase the individual estimated lifetime cancer risk by as much as 0.8%. Although risk-benefit considerations are clearly different between these groups, strategies should be in place to decrease radiation doses during the preoperative workup and postoperative period. It is critical to document and tally cumulative radiation exposure in patients expected to be cured of their NSCLC so that the risk of radiation-induced malignancies can be calculated and taken into clinical consideration.
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Discussion |
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The subject of appropriate and judicious use of radiologic studies impacts the manner in which we will detect, diagnose, stage, treat, and follow-up patients with lung cancer. It is increasingly becoming a subject of discussion with our patients when they raise this issue, and it is the genesis for a new initiative being undertaken by the American College of Radiology entitled "Image Wisely."
So my question is largely based on the use of the CT [computed tomographic] and, particularly, the PET [positron emission tomographic]-CT scans for the follow-up of patients who have had a favorable early stage lung cancer resected. You pointed out that a standard X-ray is a tenth of a millisievert. You receive about half of that dose from cosmic radiation if you go across the country. You could have 400 or 500 chest X-rays a year and barely reach the limit of 50 mSv, the maximum dose for a worker in the radiation field. But a PET-CT scan, as you pointed out, is 25 mSv, a relatively huge dose. So my question for you: Do you think that early detection of a recurrent lung cancer carries the same implication for the long-term outcome in that patient that early detection of a primary lung cancer does? I must confess that I have thought not and therefore have not used CAT [computed axial tomographic] scans or PET scans for routine follow-up other than to confirm a suspected recurrence. Also I would like to know how this study of yours has affected you and your colleagues in terms of how you are now following your early stage lung cancer patients?
DR STILES: Well, thank you very much, Dr Cooper. I also really appreciated discussing the paper with you yesterday. I think you make some timely and important points.
To me, the true value of surveying or following these patients is in detecting second primary lung cancers. Unlike many oncologists, I really don't believe that we derive a big benefit by detecting recurrent disease. So then the question really becomes, as you say, do you believe in screening? I come from an institution that has a bias towards screening and I believe in it. I think that you have to assume these patients are going to have a rate of second primary lung cancers of approximately 1 to 2% per year. At five years that is 5 to 10%, which is probably higher than any risk associated with radiation-induced malignancy over that time period. That doesn't mean that we shouldn't follow those patients or that we should not think about the radiation for the patients.
To me, particularly with the results from the National Lung Screening Trial, people are going to be interested in screening and people are going to continue to do further imaging studies on these patients. We wanted to get the message out there that we just need to do that with a note of caution.
Regarding how it has affected us practically, we are trying to do low-dose CT scans whenever we can. That carries a dose of about 2 mSv compared to a dose of 7 mSv for a regular CT scan without contrast, as high as 15 mSv if you get CT scans with contrast. We are trying to spread out surveillance scans. And we certainly learned that PET-CT surveillance increases the dose. To my knowledge, there is no evidence that PET-CT surveillance carries any benefit over CT alone for screening or for following these patients. We certainly don't get routine PETs anymore outside of that protocol that we had running then. To us, the only time to get a PET is when we want to further investigate morphologic changes on the CT scan.
DR COOPER: Thank you. And my last combination question is sort of rhetorical. Have you discussed this with your medical oncologists, who seem to want a PET-CT scan every three or four or five months? If you had some funds to invest, would you invest in biomarkers to detect early recurrence or in technology to lower the radiation dose for radiologic detection of recurrent lung cancer?
Thank you again, and I would say that the manuscript reads very well and I would strongly recommend it.
DR STILES: Well, thank you, Dr Cooper. We have not discussed it further with our medical oncologists. It is amazing that we have actually gotten a fair amount of resistance from radiologists, who frequently claim that these are not big risks. They in fact could be frequently overestimated; even the BEIR VII [seventh Biologic Effects of Ionizing Radiation] report admits that the estimated chances of malignancy could vary by as much as two to threefold. Another argument is also made that these are old patients who are less likely to develop malignancy. To us, these patients have demonstrated genomic instability, they may have field effects from smoking, and they likely have defects in DNA repair pathways. So I could make just as much of an argument that these patients are at an even higher risk of radiation-induced malignancy.
I think right now we have to focus on lowering the dose. In the big picture, as you say, the real message and the real thing that we need to move forward and invest in is really developing either blood-based or bodily fluid-based biomarkers to at least further define who needs treatment, or at least who needs more intensive imaging.
DR PAUL H. SCHIPPER (Portland, OR): My question has to do with risk tolerance. I think if you are a healthcare worker and you are paid a salary, you may be willing to tolerate a certain risk of cancer, and you certainly don't want to risk death, and your risk tolerance if you are a lung cancer patient might be quite a bit higher. And, Dr Cooper brought up some of this; if you walk across the United States, there is some risk of radiation exposure there. So what is your risk tolerance for being out in the sun?
The numbers that you used, the 50 and 100, do you think that ought to be adjusted up depending on the diagnosis that we are making or the risk that we think that this cancer is going to recur, and what might that number be? Is maybe 50 too low and 100 appropriate?
DR STILES: I don't know that there is an appropriate level that we can set for cancer patients. A lot of these imaging procedures are necessities. I think it is more important to identify how much they are getting and to keep track of individual patient's records. So the set yearly limit to me matters less than the total exposure.
DR CARLOS DEL CAMPO (Fullerton, CA): I have a brief comment and a quick question. The comment is I want to congratulate you for bringing this to the attention of the Society. This is a major problem we have been trying to deal with for a long time, and I will give you a brief example, and this happens very often in our hospital.
A patient comes into the ER, gets a chest X-ray and is found to have a pleural effusion. Before the pleural effusion is being drained, somebody decides to do a CT. Of course, the result is you cannot tell the underlying pathology. So they get a chest tube and then they repeat the CT. Now, it may be done without contrast. Then you find a lung tumor as the underlying pathology. So somebody orders a CT with contrast, and then we have to stage the patient and then he gets a PET-CT scan. That patient got a tan without going to Hawaii just from radiation. So we have to bring this to the attention to all these societies, and we have a committee in our hospital to do this.
Now, my question to you is this. Should we or the Society decide as a part of the record of every patient, we should have a form, either an electronic charting or the regular chart, where the dose that these patients are receiving is calculated as well as the risk?
DR STILES: Well, thank you for your comments. I think that is a great idea. One of the things that we learned in the study is that we actually probably weren't capturing all the imaging procedures being done. In addition to our hospital, there were numerous imaging procedures performed at other hospitals, too. There are national efforts to organize methods to track cumulative doses for individual patients. I do think that is the way to go in the future.
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= median dose; 
= mean dose). (B) Percent of cohort exceeding 50 mSv of effective radiation dose per year of the study (