HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Swensen, S. J. Search for Related Content PubMed PubMed Citation Articles by Swensen, S. J. Social Bookmarking                      What's this?

CT Screening for Lung Cancer

¹ Department of Radiology, Mayo Clinic, 200 First St. S.W., Rochester, MN 55905.

Received February 18, 2002; accepted after revision March 14, 2002.

 
Supported by the National Cancer Institute (NCI R01 CA 79935-03) and the Mayo Clinic.

Address correspondence to S. J. Swensen.

Introduction

Top Introduction CT Screening: Mayo Clinic... Biomarkers Reasons for Optimism Reasons for Doubt References

 
When epidemiologists, ethicists, radiologists, smokers, venture capitalists, entrepreneurs, lung cancer advocates, the tobacco industry, CT manufacturers, and insurance companies look at the possibilities for CT screening, all have different images, visions, and visceral reactions. The use of CT screening has clearly caught the attention of America. I would like to present one perspective based on several years of study.

I will briefly review results from my institution from more than 4500 patient-years of scanning in a hypothesis-driven scientific setting at our institution. I will look at reasons for optimism and reasons for doubt that CT screening for lung cancer will ultimately save lives (i.e., reduce disease-specific mortality). I will also touch briefly on the ancillary findings among our participants and explore the concept of comprehensive, full-body CT screening.

In the early 1900s, lung cancer was a rare occurrence. It was not until the 1930s and 1940s that it showed up on the radar screen, so to speak, and today it is unfortunately the most common cause of cancer deaths among both men and women. We cannot lose sight of the fact that smoking causes lung cancer, and the best cure for lung cancer is prevention.

In fact, smoking causes more deaths than AIDS, alcohol, drug abuse, car crashes, murders, suicides, and fires combined. It accounts for one of every five deaths in the United States—430,700 deaths per year.

CT Screening: Mayo Clinic Experience

Top Introduction CT Screening: Mayo Clinic... Biomarkers Reasons for Optimism Reasons for Doubt References

 
At my institution, we have several years of experience in performing low-dose helical CT screening of the chest and abdomen. CT screening is performed in a scientific format—that is, it is hypothesis-driven. Our phase II study (non-randomized) comprises 1520 participants who, at enrollment, were at least 50 years old, had at least 20 pack-years of smoking, and, if they were no longer smokers, had quit within the previous decade. All participants were asymptomatic with regard to lung cancer [1].

In our first prevalence year, 51% of participants had one or more uncalcified radiologically indeterminate nodules. Forty percent of these nodules were smaller than 4 mm in diameter, and 50% measured from 4 to 7 mm. In the two subsequent incidence years, our participants had return rates of 98% and 96%. In the first incidence year, 14% of our participants had new lung nodules that were not present at admittance in retrospect. In the second incidence year, 9% had new nodules that were not present, in retrospect, in either of the two previous years.

At the end of 3 years of scanning, we are following up more than 2800 uncalcified, radiologically indeterminate lung nodules. Nearly 70% of our participants have one or more uncalcified lung nodules. We have identified 41 lung cancers, 59% of which are stage IA. The mean size of the cancers was 17 mm in diameter; four were smaller than 7 mm in diameter at the time of discovery. The smallest cancer at the time of discovery was 3 mm.

A total of 1.4% of all lung nodules in our study are now known to be malignant. We expect that nearly 99% of all the lung nodules we identified were benign and therefore were false-positive findings.

More than 90 million current and past smokers exist in the United States [2]. If you were to extrapolate our findings to just this high-risk population, you would expect to find more than 150 million uncalcified radiologically indeterminate nodules in the adult population. That is the "fly in the ointment" that concerns all of us involved with screening. One important feature of a useful screening test is a low false-positive rate. CT apparently will not meet this criterion.

Unfortunately, it is difficult to distinguish benign from malignant nodules. The most appropriate means of treating most small lung nodules is with radiologic follow-up. Three-dimensional analysis with segmentation may be the most accurate, sensitive, and reproducible tool for follow-up of small nodules [3]. For nodules that are at least approximately 7-8 mm, a positron emission tomography or CT nodule enhancement study may be helpful in the treatment.

To date, eight of our participants have had surgery for removal of a benign nodule, approximately 20% of the operations that were performed. The most recent data from multi-center studies in both the United States and Europe show that approximately 50% of lung nodules removed at surgery are benign [4]. That rate of resection of benign nodules would be clearly unacceptable for a mass screening endeavor, given the number of false-positive findings. Even if the cost were the only consideration, $20,000-25,000 per operation would be unacceptable. A much greater concern, however, is the morbidity and the 3.8% mortality seen with wedge resections of lung nodules in community hospitals in the United States [5]. As we seriously study this test, we should not do more harm than good to patients.

Biomarkers

Top Introduction CT Screening: Mayo Clinic... Biomarkers Reasons for Optimism Reasons for Doubt References

 
In our studies, we are retaining sputum samples for both cytologic and biomarker analysis. In addition, we have blood samples from all patients for comparison DNA. The ultimate answer to screening for lung cancer and for many other diseases may come down to a genetic biomarker. The answer may lie in a blood or sputum sample, which could allow enrichment of the screened population, targeted imaging, and intervention for the most appropriate patients.

Our protocol included a low-dose helical CT scan of the chest and upper abdomen through the level of the kidneys. Nearly 700 of our 1520 participants had a significant ancillary finding. The findings included four renal cancers, three breast cancers, one atrial myxoma, two gastric tumors, and 114 abdominal aortic aneurysms. However, we also found 147 indeterminate renal, adrenal, or breast masses that needed further evaluation. When one combines the findings of benign lung nodules with nonpulmonary ancillary findings after only 3 years of scanning, nearly 80% of our participants have had one or more positive findings that will need further diagnostic testing.

These ancillary findings, coupled with the 41 lung cancers that we found, certainly raise the possibility that total-body screening is not only lifesaving but also cost-effective. However, scientifically such a conclusion is absolutely unproven at this point, and the matter needs to be throughly studied in a responsible manner.

Serious ethical questions have been raised about advertising directly to the general public in the United States. A primary concern is that of informed consent [6]. If the claim is that lung cancer can be found early, the inference may well be that "we can save your life." A person reading such an advertisement could reasonably presume that the necessary scientific studies have been performed, and that the recommendation in the advertisement is from evidence-based medicine. This presumption is particularly true if physicians are involved in the promotion. Our profession must be seriously concerned about such a practice.

Reasons for Optimism

Top Introduction CT Screening: Mayo Clinic... Biomarkers Reasons for Optimism Reasons for Doubt References

 
Many reasons explain why so many in the scientific community are optimistic that CT screening offers the answer to the scourge of lung cancer. Low-dose helical CT is much more sensitive for detection of lung cancer than chest radiography [7,8,9]. We fail to detect most lung cancers smaller than 2 cm in diameter with chest radiography [10,11,12]. CT will detect most lung cancers smaller than 2 cm. In practice today, only 15-20% of lung cancers are stage IA at presentation. Survival of patients with stage I lung cancers is 60-70%. There is reason for hope.

Another reason for optimism is the success that medicine has had with improving the survival of patients with colorectal, breast, and prostate cancers, all of which have had statistically significant improvements in survival rates since the 1970s [13]. However, no progress has been made with lung cancer, and no test has been shown to be effective for reducing mortality. Could CT screening be the test that will be effective for reducing mortality? More Americans die of lung cancer than colorectal, breast, and prostate cancers combined.

Why should screening for lung cancer fail? The experience with lung cancer is that it is most often fatal, with a 5-year survival rate of only 13-14%. In fact, when one looks at the outcome of patients who decline treatment for stage I cancer, the disease is almost universally fatal [14]. The proponents of screening strongly assert that tens of thousands of lives per year could be saved with mass screening in the United States alone. They contend that the identification of ancillary findings will save additional lives and that screening will be clearly cost-effective [15].

Reasons for Doubt

Top Introduction CT Screening: Mayo Clinic... Biomarkers Reasons for Optimism Reasons for Doubt References

 
Much is known, but much still needs to be learned, about the natural history of lung cancer. Experts now understand that a 5-mm lung cancer is actually late in the natural history of the disease, probably in the last third of the timeline of a lung cancer. In fact, at 5 mm, a lung cancer has undergone approximately 20 doublings and contains about 100 million cells [16].

When does lung cancer metastasize? Is it when it is undergoing angiogenesis? Angiogenesis occurs at 1-2 mm for most tumors [17,18,19,20].

When does lung cancer become a systemic disease? Human tumor grown in nude mouse models sheds between 3 and 6 million cells per gram of tissue every 24 hr [21]. Even though most of these cells are not viable, all it takes is one viable metastatic cell to lead to the death of a patient.

CT for lung cancer is directed at non—small cell lung cancer. It is not anticipated that earlier detection of small cell lung cancer will result in a significant reduction in mortality. This observation will mitigate any positive effect that CT has on overall lung cancer mortality rates.

Although intuitively it may make sense to some that earlier detection will result in decreased mortality, this assumption has not been proven. In fact, questions have been raised regarding whether there is any correlation at all. Patz et al. [22] reviewed a series of 510 patients and found no relationship between tumors smaller than or equal to 3 cm in diameter and survival (i.e., patients who had a 3-cm mass had the same survival rate as those with a 1-cm nodule). In a related study [23], no relationship was seen between stage at presentation and size of tumor (i.e., 1-cm and 2- to 3-cm lung cancers had similar distributions of stage). Is the propensity to metastasize predetermined by genetics? Does metastasis for most lung cancers occur at a size smaller than can be routinely detected by CT (Fig. 1A,1B)?

View larger version (107K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —65-year-old woman with incidence of 8-mm grade 4, stage IIIA (T1 N2 MO) squamous cell carcinoma detected on screening CT. CT scan shows primary lung tumor.

View larger version (140K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —65-year-old woman with incidence of 8-mm grade 4, stage IIIA (T1 N2 MO) squamous cell carcinoma detected on screening CT. Positron emission tomography scan shows intense focal uptake in both right upper lobe nodule (straight arrow) and right paratracheal node (curved arrow). Both were shown at surgery to be involved with tumor.

Some say that lung cancer is deadly and that there is no hope of significantly decreasing mortality by earlier detection. They contend that the outcome will be the same as that of the chest radiography studies from the 1970s. The tens of billions of dollars spent per year in screening would mean fewer funds for more successful alternatives. Furthermore, they say, Americans might get the message that it is safer to smoke now that lung cancer can seemingly be cured with screening. Certainly, they raise concerns about false-positive findings and overdiagnosis leading to increased cost of treatment and to increased morbidity and mortality rates. They say it would be a blow to patients' quality of life when they find out that they are among the nearly 70% of those screened who have a positive finding that could be cancer but will not know whether the nodule is indeed a cancer for months or years.

What is overdiagnosis, and is it, in fact, harmful? Fewer than 1% of Americans experience potentially lethal renal cell carcinoma. Approximately 0.5% die from this form of cancer. Yet when one looks closely at the kidneys in autopsies, more than 22% of these persons are found to have unsuspected histologic renal cell carcinoma [24]. Most of these cancers are not fatal. Renal cell carcinoma is the kind of disease that patients die with and not from. A serious concern has been raised that the better our methods of detection, the more overdiagnosis of renal cell cancers we will have [25, 26]. As more of these cancers are resected, more persons will die of surgical complications, with little or no decrease in mortality. Did we actually "save" the lives of the four participants in whom we identified renal cell carcinomas, or are we fooling ourselves?

Could the same thing be true for lung cancer? Adenocarcinoma appears to be overrepresented in the CT screening of lung cancer cell types (60-80% with CT vs 40% expected), and a large proportion appears to be well differentiated, which is associated with longer survival. This finding suggests the possibility of overdiagnosis bias in CT screening trials.

Autopsy data also raise concerns about overdiagnosis. One study showed that one sixth of lung cancers found at autopsy were not clinically recognized and were not related to the patient's death [27]. Are these "extra cancers" ones that cause patients' deaths? The closer we look at the lung and the kidney in "healthy" persons, the more "disease" we find. But is it pseudodisease [28,29,30,31]? Another type of overdiagnosis is pathologic overdiagnosis in which there is inter- and intraobserver variation in the diagnosis of disorders such as lung adenomas and atypical adenomatous hyperplasia. The misclassification of indolent premalignant or benign conditions like cancer will not decrease disease-specific mortality rates but will apparently increase survival rates.

A number of interesting studies from Japan showed that a large proportion of lung cancers occurred in persons who never smoked. In fact, one series showed the same rate of cancer, approximately 0.5%, in screened smokers and in those who never smoked [32]. This finding does not fit with clinical experience in which we see that most patients who die of lung cancer are heavy long-term smokers. Are these cancers overdiagnosed?

The volume doubling time of the cancers in one series of patients who never smoked was more than twice as long as that of cancers in smokers [33]. In that series, 31% of 61 cancers examined were well-differentiated adenocarcinomas. These cancers had a mean size of 10 mm, and only one of 19 was seen on chest radiography. One hundred percent of them were stage I. Their mean doubling time was 813 days. A volume doubling time of 813 days means that it would take 16 years for a 3-mm lung cancer to undergo seven volume doublings to reach 15 mm in diameter. Is that the kind of lung cancer that will kill? Surgical wedge resection of those cancers does kill—at a rate of 3.8% [5]. Morbidity (chronic pain, atrial fibrillation, infection, respiratory insufficiency) is an important quality-of-life issue that often is overlooked in the analysis of "effectiveness." First, do no harm.

If CT screening leads to overdiagnosis of lung cancer, one would expect an increase in stage I disease, an increase in resectability, an increase in 5-year survival, and an increase in the total number of cancers but no change in the number of advanced cancers and no decrease in lung cancer deaths [28,29,30]. This result is exactly what was found in the Mayo Lung Project from the 1970s, which has recently been reviewed by researchers at the National Cancer Institute [34]. The Mayo Lung Project involved 9211 men who were randomized to either screening by chest radiography or usual care. In this study, the investigators found nearly twice as many early-stage cancers in the screening group as in the control group. The cancers in the screened patients were more resectable, and those patients lived longer. However, no difference existed in the number of advanced-stage cancers between the control and the screened groups, and after more than two decades of follow-up, no difference in mortality rates was observed between the two groups [34,35,36]. The Czech lung cancer project, with a cohort of 6346 participants, had similar results and also showed no difference in mortality rates [37].

In conclusion, CT is much more sensitive than chest radiography for the detection of early lung cancer. Clearly, too, CT reveals more early-stage lung cancers than does chest radiography. What is not clear is whether CT meets the criteria of an effective screening test [31]. Will the number of advanced stage cancers detected with CT screening decrease? Serious issues are raised by false-positive findings with regard to quality of life, radiation exposure, and intervention. Surgery triggered by false-positive findings could lead to higher morbidity and mortality rates among the participants in the screened group than any gain in disease-specific mortality rates.

Ancillary findings from CT screening raise hopes for decreased mortality from many conditions, including abdominal aortic aneurysms and renal cell carcinoma, but issues of overdiagnosis and operative mortality mute the enthusiasm.

The bottom line is that we are unequivocally required as scientists and health professionals to thoroughly study this new "beast" before jumping into what might be a quagmire. A randomized, controlled trial is the best way to address the controversy and probably the only way that third-party payers will ever agree to pay for this screening—if a trial shows positive results.

References

Top Introduction CT Screening: Mayo Clinic... Biomarkers Reasons for Optimism Reasons for Doubt References

 

1. Swensen SJ, Jett JR, Sloan JA, et al. Screening for lung cancer with low-dose spiral computed tomography. Am J Respir Crit Care Med 2002;165:508 -513[Abstract/Free Full Text]
2. Strauss G, DeCamp M, Dibiccaro E, et al. Lung cancer diagnosis is being made with increasing frequency in former cigarette smokers. (abstr) Proc Am Soc Clin Oncol 1995;15(P):362
3. Yankelevitz DF, Reeves AP, Kostis WJ, Zhao B, Henschke CI. Small pulmonary nodules: volumetrically determined growth rates based on CT evaluation. Radiology 2000;217:251 -256[Abstract/Free Full Text]
4. Bernard A. Resection of pulmonary nodules using video-assisted thoracic surgery: the Thorax Group. Ann Thorac Surg 1996:61;202 -204[Abstract/Free Full Text]
5. Romano PS, Mark DH. Patient and hospital characteristics related to in-hospital mortality after lung cancer resection. Chest 1992;101:1332 -1337[Abstract/Free Full Text]
6. Welch HG. Informed choice in cancer screening. JAMA 2001;285:2776 -2778[Free Full Text]
7. Kaneko M, Eguchi K, Ohmatsu H, et al. Peripheral lung cancer: screening and detection with low-dose spiral CT versus radiography. Radiology 1996;201:798 -802[Abstract/Free Full Text]
8. Ohmatsu H, Kakinuma R, Kaneko M, Moriyama N, Kusumoto M, Eguchi K. Successful lung cancer screening with low-dose helical CT in addition to chest X-ray and sputum cytology: the comparison of two screening period with or without helical CT. (abstr) Radiology 2000;217(P):242
9. Henschke CI, McCauley DI, Yankelevitz DF, et al. Early Lung Cancer Action Project: overall design and findings from baseline screening. Lancet 1999;354:99 -105[Medline]
10. Muhm JR, Miller WE, Fontana RS, Sanderson DR, Uhlenhopp MA. Lung cancer detected during a screening program using four-month chest radiographs. Radiography 1983;148:609 -615
11. Quekel LG, Kessels AG, Goei R, van Engelshoven JM. Miss rate of lung cancer on the chest radiograph in clinical practice. Chest 1999;115:720 -724[Abstract/Free Full Text]
12. Sone S, Li F, Yang ZG, et al. Characteristics of small lung cancers invisible on conventional chest radiography and detected by population based screening using spiral CT. Br J Radiol 2000;73:137 -145[Abstract]
13. American Cancer Society. Cancer facts and figures 2000. Atlanta: American Cancer Society, 2000
14. Flehinger BJ, Kimmel M, Melamed MR. The effect of surgical treatment on survival from early lung cancer: implications for screening. Chest 1992;101:1013 -1018[Abstract/Free Full Text]
15. Clark RA. Screening for lung cancer with CT: experience at Moffitt Cancer Center and preliminary cost-effectiveness analysis. In: Müller NL, Grist TM, eds. 2001 Syllabus categorical course in diagnostic radiology: thoracic imaging—chest and cardiac. Oak Brook, IL: Radiological Society of North America, 2001:37 -45
16. DeVita VT Jr, Young RC, Canellos GP. Combination versus single agent chemotherapy: a review of the basis for selection of drug treatment of cancer. Cancer 1975;35:98 -110[Medline]
17. Yang M, Hasegawa S, Jiang P, et al. Widespread skeletal metastatic potential of human lung cancer revealed by green fluorescent protein expression. Cancer Res 1998;58:4217 -4221[Abstract/Free Full Text]
18. Folkman J. Seminars in medicine of the Beth Israel Hospital, Boston: clinical applications of research on angiogenesis. N Engl J Med 1995;333:1757 -1763[Free Full Text]
19. Rak JW, St. Croix BD, Kerbel RS. Consequences of angiogenesis for tumor progression, metastasis and cancer therapy. Anticancer Drugs 1995;6:3 -18[Medline]
20. Liotta LA, Kleinerman J, Saidel GM. Quantitative relationships of intravascular tumor cells, tumor vessels, and pulmonary metastases following tumor implantation. Cancer Res 1974;34:997 -1004[Abstract/Free Full Text]
21. Swartz MA, Kristensen CA, Melder RJ, et al. Cells shed from tumours show reduced clonogenicity, resistance to apoptosis, and in vivo tumorigenicity. Br J Cancer 1999;81:756 -759[Medline]
22. Patz EF Jr, Rossi S, Harpole DH Jr, Herndon JE, Goodman PC. Correlation of tumor size and survival in patients with stage IA non-small cell lung cancer. Chest 2000;117:1568 -1571[Abstract/Free Full Text]
23. Heyneman LE, Herndon JE, Goodman PC, Patz EF Jr. Stage distribution in patients with a small (< or = 3 cm) primary nonsmall cell lung carcinoma: implication for lung carcinoma screening. Cancer 2001;92:3051 -3055[Medline]
24. Xipell JM. The incidence of benign renal nodules (a clinicopathologic study). J Urol 1971;106:503 -506[Medline]
25. Stanley RJ. Inherent dangers in radiologic screening. AJR 2001;177:989 -992[Free Full Text]
26. Feldman AR, Kessler L, Myers MH, Naughton MD. The prevalence of cancer: estimates based on the Connecticut Tumor Registry. N Engl J Med 1986;315:1394 -1397[Abstract]
27. Chan CK, Wells CK, McFarlane MJ, Feinstein AR. More lung cancer but better survival: implications of secular trends in "necropsy surprise" rates. Chest 1989;96:291 -296[Abstract/Free Full Text]
28. Welch HG, Schwartz LM, Woloshin S. Are increasing 5-year survival rates evidence of success against cancer? JAMA 2000;283:2975 -2978[Abstract/Free Full Text]
29. Black WC, Welch HG. Screening for disease. AJR 1997;168:3 -11[Abstract/Free Full Text]
30. Black WC, Welch HG. Advances in diagnostic imaging and overestimations of disease prevalence and the benefits of therapy. N Engl J Med 1993;328:1237 -1243[Free Full Text]
31. Obuchowski NA, Graham RJ, Baker ME, Powell KA. Ten criteria for effective screening: their application to multislice CT screening for pulmonary and colorectal cancers. AJR 2001;176:1357 -1362[Free Full Text]
32. Sone S, Takashima S, Li F, et al. Mass screening for lung cancer with mobile spiral computed tomography scanner. Lancet 1998;351:1242 -1245[Medline]
33. Hasegawa M, Sone S, Takashima S, et al. Growth rate of small lung cancers detected on mass CT screening. Br J Radiol 2000;73:1252 -1259[Abstract]
34. Marcus PM, Bergstralh EJ, Fagerstrom RM, et al. Lung cancer mortality in the Mayo Lung Project: impact of extended follow-up. J Natl Cancer Inst 2000;92:1308 -1316[Abstract/Free Full Text]
35. Fontana RS, Sanderson DR, Woolner LB, et al. Screening for lung cancer: a critique of the Mayo Lung Project. Cancer 1991;67[suppl]:1155S -1164S
36. Flehinger BJ, Melamed MR, Zaman MB, Heelan RT, Perchick WB, Martini N. Early lung cancer detection: results of the initial (prevalence) radiologic and cytologic screening in the Memorial Sloan-Kettering study. Am Rev Respir Dis 1984;130:555 -560[Medline]
37. Kubik AK, Parkin DM, Zatloukal P. Czech study on lung cancer screening: post-trial follow-up of lung cancer deaths up to year 15 since enrollment. Cancer 2000;89[suppl]:2363S -2368S

CiteULike

Complore

Connotea

Del.icio.us

Digg

Reddit

Technorati

This article has been cited by other articles:

				K. Awai, K. Murao, A. Ozawa, Y. Nakayama, T. Nakaura, D. Liu, K. Kawanaka, Y. Funama, S. Morishita, and Y. Yamashita Pulmonary Nodules: Estimation of Malignancy at Thin-Section Helical CT--Effect of Computer-aided Diagnosis on Performance of Radiologists Radiology, April 1, 2006; 239(1): 276 - 284. [Abstract] [Full Text] [PDF]

				H. MacMahon, J. H. M. Austin, G. Gamsu, C. J. Herold, J. R. Jett, D. P. Naidich, E. F. Patz Jr, and S. J. Swensen Guidelines for Management of Small Pulmonary Nodules Detected on CT Scans: A Statement from the Fleischner Society Radiology, November 1, 2005; 237(2): 395 - 400. [Abstract] [Full Text] [PDF]

				J. P. Wisnivesky, D. Yankelevitz, and C. I. Henschke The Effect of Tumor Size on Curability of Stage I Non-small Cell Lung Cancers Chest, September 1, 2004; 126(3): 761 - 765. [Abstract] [Full Text] [PDF]

				J. F. Schaefer, J. Vollmar, F. Schick, R. Vonthein, M. D. Seemann, H. Aebert, R. Dierkesmann, G. Friedel, and C. D. Claussen Solitary Pulmonary Nodules: Dynamic Contrast-enhanced MR Imaging--Perfusion Differences in Malignant and Benign Lesions Radiology, August 1, 2004; 232(2): 544 - 553. [Abstract] [Full Text] [PDF]

				C. I. Henschke, D. F. Yankelevitz, D. P. Naidich, D. I. McCauley, G. McGuinness, D. M. Libby, J. P. Smith, M. W. Pasmantier, and O. S. Miettinen CT Screening for Lung Cancer: Suspiciousness of Nodules according to Size on Baseline Scans Radiology, April 1, 2004; 231(1): 164 - 168. [Abstract] [Full Text] [PDF]

				W. J. Scott Metachronous lung cancer: the role of improved postoperative surveillance J. Thorac. Cardiovasc. Surg., March 1, 2004; 127(3): 633 - 635. [Full Text] [PDF]

				R MacRedmond, P M Logan, M Lee, D Kenny, C Foley, and R W Costello Screening for lung cancer using low dose CT scanning Thorax, March 1, 2004; 59(3): 237 - 241. [Abstract] [Full Text] [PDF]

				D. F. Yankelevitz, F. Earnest, and S. J. Swensen Screening for Lung Cancer: Is Informed Consent Sufficient? [letter] * Drs Earnest and Swensen respond: Radiology, December 1, 2003; 229(3): 929 - 930. [Full Text] [PDF]

				J. J. Fenton and R. A. Deyo Patient Self-Referral for Radiologic Screening Tests: Clinical and Ethical Concerns J Am Board Fam Med, November 1, 2003; 16(6): 494 - 501. [Abstract] [Full Text] [PDF]

				D. Yankelevitz and S. J. Swensen CT Screening for Lung Cancer Am. J. Roentgenol., June 1, 2003; 180 (6): 1736 - 1737. [Full Text] [PDF]

				F. M. Hall and L. F. Rogers CT Screening Examinations Am. J. Roentgenol., April 1, 2003; 180 (4): 1178 - 1179. [Full Text] [PDF]

				L. F. Rogers Whole-Body CT Screening: Edging Toward Commerce Am. J. Roentgenol., October 1, 2002; 179(4): 823 - 823. [Full Text] [PDF]

This Article Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Swensen, S. J. Search for Related Content PubMed PubMed Citation Articles by Swensen, S. J. Social Bookmarking                      What's this?