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Ann Thorac Surg 1995;60:1612-1616
© 1995 The Society of Thoracic Surgeons


Original Articles: General Thoracic

Clinical Surveillance Testing After Lung Cancer Operations

Keith S. Naunheim, MD, Katherine S. Virgo, PhD, Margaret A. Coplin, MA, Frank E. Johnson, MD

Department of Surgery, Saint Louis University Health Sciences Center and John Cochran Veterans Affairs Medical Center, St. Louis, Missouri

Accepted for publication August 1, 1995.


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1.
 References
 
Background. Although routine clinical surveillance testing after lung cancer operation has important clinical implications for patients and financial implications for society, the ideal surveillance strategy is unknown.

Methods. We surveyed The Society of Thoracic Surgeons membership by questionnaire to characterize the current practice of follow-up among experts in lung cancer treatment. There were 2,009 responses (54% return) from the 3,700 members; 768 of those responding both operate on and provide long-term follow-up for lung cancer patients. These responses form the basis of this study.

Results. The follow-up methods most frequently used during a 5-year follow-up include clinic visit, chest roentgenography, complete blood cell count, liver function testing, and chest computed tomography. Sputum cytology, head computed tomography, bone scanning, chest magnetic resonance imaging, and bronchoscopy are used infrequently. Although there is wide variation in the frequency of use of these ten methods, there is significant (p < 0.05) decrease in the frequency of testing over time for all tests except sputum cytology and chest magnetic resonance imaging. The survey also requested information regarding motivation behind routine clinical surveillance testing. Although the presumed rationale for such follow-up includes probable clinical benefit for the patient, fewer than half of respondents believe that such surveillance testing would yield a survival benefit for either stage I (44% of respondents) or advanced-stage patients (17% of respondents) after lung cancer resection. Only 1 of 4 respondents believe that the current literature documents any survival benefit. Other reasons for follow-up include maintenance of rapport with colleagues or patients and medicolegal liability concerns.

Conclusions. This survey provides direct evidence regarding current surveillance practices among thoracic surgeons. There appears to be marked variation among members of The Society of Thoracic Surgeons in frequency of and rationale for routine clinical surveillance testing.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1.
 References
 
The National Cancer Database [1] has demonstrated that approximately 21% of patients with bronchogenic carcinoma are treated by surgical resection. Routine clinical surveillance testing (RCST) is commonly used in lung cancer patients after resection. Of the approximately 170,000 cases of lung cancer anticipated in 1995, there will be an estimated 35,000 patients treated by surgical resection who will be monitored for recurrence throughout their postoperative period [2]. Although lifelong testing has been recommended for all patients after an operation for lung cancer [3], there are no well-designed trials demonstrating significant benefit from this practice. The explosion in medical technology over the last three decades has made multiple testing procedures widely available. Among these are chest roentgenography, liver function tests, complete blood cell count, sputum cytology, flexible bronchoscopy, computed tomography, scintigraphic testing, and magnetic resonance imaging. With so many tests available and no consensus on their usefulness, clinicians have had to devise their own strategies for follow-up. This survey was undertaken to assess both the current follow-up practice of the thoracic surgical community and the rationale for such testing.


    Material and Methods
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1.
 References
 
In January 1994, surveys were mailed to all 3,700 members of The Society of Thoracic Surgeons (STS). This was done with the permission of and in cooperation with The Society. A mailing list of the membership was obtained from the STS, and all active members residing in the United States and elsewhere were surveyed. The survey instrument was composed of two parts, an introductory cover letter and the survey itself. The cover letter explained the purpose of the survey and requested information regarding whether the surgeon actually performed lung resection and whether he or she personally followed such patients. Only those surgeons who both operate on and provide follow-up for lung cancer patients were asked to complete the entire questionnaire.

The survey requested demographic information regarding age (30 to 39 years, 40 to 49 years, 50 to 59 years, 60 to 69 years, 70 years and older), society membership (The American Association for Thoracic Surgery, Society of Surgical Oncology, General Thoracic Surgery Club), type of practice (private, academic, United States government, other), and percentage of practice constituted by noncardiac thoracic surgery (0% to 25%, 26% to 50%, 51% to 75%, 76% to 100%). After this, respondents were asked to describe their surveillance schedule after complete surgical excision for non-small cell lung cancer in an otherwise healthy patient. A pilot study among thoracic surgeons had produced a list of ten procedures and tests considered clinically useful in the postoperative setting. Respondents were instructed to write the number of times they require visits, tests, or procedures during each 1-year interval after curative resection for stage I (T1 N0 M0 or T2 N0 M0) non-small cell cancer (Fig 1Go). Both tests performed in the office setting (clinic visit, complete blood count, liver function tests, chest roentgenography, sputum cytology) and those performed in the hospital on an outpatient basis (chest computed tomography, head computed tomography, bone scanning, chest magnetic resonance imaging, bronchoscopy) were included in the survey. Respondents were also asked whether they use a different follow-up schedule after curative resection for advanced (stage II, stage IIIA) non-small cell lung cancer. Those responding in the affirmative were asked to fill out a follow-up schedule as they had for stage I patients.



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Fig 1. . Format used in questionnaire. (CT = computed tomographic; MRI = magnetic resonance imaging.)

 
The second portion of the survey dealt with the personal opinions of thoracic surgeons concerning surveillance regimens. Respondents were asked a series of true or false questions regarding their views on the clinical benefit of and rationale behind RCST.

A self-addressed, stamped envelope was enclosed with the questionnaire, which was coded to allow identification of individual STS members. In this way, respondents to the first mailing were identified. A second mailing was sent in March 1994 to nonrespondents. On receipt of completed surveys, the data were entered into a computerized database (Statistical Package for Social Sciences) and analyzed. A one-way analysis of variance test was used to discern changes in the frequency of testing for each modality across years 1 through 5 after operation. A p value of less than 0.05 was considered significant.


    Results
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1.
 References
 
Surveys were mailed to 3,700 STS members, 2,009 of whom (54%) responded. Of the responding surgeons, 565 (28%) do not perform lung operations, 526 (26%) perform lung operations but do not provide follow-up, and 150 (7%) were either retired or dead. The remaining 768 surgeons (21% of all surveyed, 38% of respondents) returned surveys that were evaluable. The demographic profile of these 768 respondents is provided in Table 1Go.


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Table 1. . Demographic Profile of 768 Respondentsa
 
The frequency of postoperative testing obtained by respondents in the first 5 years for TNM stages I, II, and IIIA is depicted in Table 2Go. The last column shows the sum of the averages for each of the 5 years, a figure representing the total number of such tests performed during a routine 5-year follow-up. For all tests except sputum cytology and chest magnetic resonance imaging, the frequency of testing was significantly higher in the early years.


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Table 2. . Frequency of Postoperative Testing in Years 1 Through 5a,b
 
The final portion of the survey is depicted in Appendix 1. This comprised several questions designed to elicit each respondent's opinion regarding the potential clinical benefit of and motivation behind RCST.


    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1.
 References
 
There are certain limitations to any study that uses a questionnaire to survey a large number of people. There is the risk of inaccuracy or uncertainty when one asks for specific quantification as was done in this study. Other limitations specific to this study include the fact that this survey was sent only to members of the STS. There are surgeons performing lung cancer resection who are not thoracic surgical specialists and whose practice may not be represented in this survey. Also, the vast majority of our respondents were from the United States, and follow-up routines may differ substantially in other countries. No information was sought regarding the cost or clinical benefit of follow-up. However, given these limitations, the survey still provides valuable information. More than 50% of the STS members responded, which is an excellent result for such a survey. It is interesting that only approximately 60% of thoracic surgeons performing lung resection actually provide long-term oncologic surveillance.

The most important finding of this study is that there is wide variation in the follow-up strategies undertaken by thoracic surgeons. Although clinic visits, chest roentgenography, complete blood counts, and liver function tests were undertaken by virtually all respondents, other tests (head computed tomography, bone scanning, chest computed tomography, bronchoscopy, sputum cytology) were routinely performed by some surgeons and totally ignored by others. The wide variation in follow-up is not particularly surprising considering the dearth of literature on the subject. There are no specific guidelines suggested by either the American Cancer Society or the American College of Surgeons. Nor is there mention of postoperative surveillance testing for any thoracic oncologic problem in the recently published cardiothoracic surgical practice guidelines [4]. A review of four widely respected textbooks of thoracic surgery [58] revealed that the topic of postoperative surveillance testing after lung cancer resection appears in the index of only one textbook [8]. That citation includes a single paragraph regarding the need of follow-up but does not provide a program of actual testing.

The issue of the optimal clinical surveillance regimen has been addressed for several types of cancer. Two recent studies of breast cancer [9, 10] suggest that a minimalist strategy yields survival benefits indistinguishable from those of an intensive follow-up strategy. Conversely, a recent study dealing with the follow-up for upper aerodigestive tract cancers [11] suggests that patients followed more intensely seem to have a better outcome with longer survival. Studies concerning follow-up for colon cancer [12, 13], although controversial, have indicated that intensive follow-up has no effect on survival. What is clear is that there is a huge economic stake in identifying what follow-up is beneficial and what is superfluous. Virgo and colleagues [14] have demonstrated that in the case of colon cancer, hundreds of millions of dollars would be spent annually if aggressive follow-up regimens were used for all patients. The magnitude of the economic costs of surveillance will likely prove just as great for bronchogenic carcinoma, as the incidence of this disease is even higher than that of colon cancer. It is imperative that the value of such an expenditure be proved so that scarce medical resources are not wasted.

Proponents of active postoperative surveillance testing point to the large screening studies performed on high-risk patient populations in the 1970s at Johns Hopkins [15], Memorial Sloan-Kettering [16], and the Mayo Clinic [17]. Although these screening studies did not definitively demonstrate a survival advantage for systemically screened high-risk patients, a greater percentage of lung cancers were diagnosed at an early stage, thus allowing potentially curative treatment. It might be hoped that a similar advantage could be achieved by aggressive postoperative RCST and that this might result in improved survival. However, in the only published analysis of RCST, Virgo and associates [18] compared a population of patients who were followed up intensively with one followed less intensively after lung resection performed in the setting of a Veterans Affairs hospital. This was a retrospective analysis and subject to the limitations of such studies. However, the investigators found no significant survival benefit in patients followed intensively versus those followed less intensively. This was true both when all tumor stages were analyzed together and when stage I tumors were analyzed separately.

The respondents' attitudes toward the clinical benefit of or rationale for routine surveillance testing were also interesting in their variation. The rationale behind the clinical benefit of RCST includes three concepts about which there was little agreement among the respondents.

  1. RCST is likely to result in early diagnosis of recurrent cancer so that clinical benefit (cure, lengthened survival, palliation) may be achieved (questions 1–3). Less than half the respondents believe that routine surveillance would either lead to cure (42%) or lengthen survival (45%) in such patients. However, 69% did believe improvement in quality of life might be achievable.
  2. RCST allows early detection and cure of a second primary tumor (question 4). There was an overwhelming sentiment (84%) that this is a true statement. However, it is important to realize that such a strategy will benefit only a minor fraction of lung cancer patients. Only 21% of patients seen with lung cancer undergo operation [1], and only about 10% of those (2% of the total) will have development of a second primary during follow-up [19, 20]. Studies suggest that only half of such patients (1% of all lung cancer patients) are operative candidates, and that among those candidates, there is only a 25% 5-year survival [19, 21, 22]. This indicates that a curative outcome for second primary carcinoma can be anticipated in only 0.25% of patients who are seen with an initial primary lung cancer, a figure that is disappointingly small considering the economic expenditure required to identify a second primary lung cancer. These progressively diminishing returns may also be the reason behind the answer to question 5.
  3. RCST for stage I lung cancer patients yields what degree of benefit? (question 5a-c). Although a large majority (89%) believe that an occasional patient may benefit in an anecdotal situation (question 5a), only 44% believe there would be a significant cumulative survival benefit in the group as a whole (question 5c). This is corroborated by the answers to question 10 in which 66% of respondents thought that there was no documentation of clinical benefit that could be found in the literature.

If the majority of responding surgeons do not believe there is a significant clinical benefit resulting from clinical surveillance testing, then why is it routinely performed? The final questions in the survey were an attempt to identify possible motivations for testing other than clinical benefit. More than two thirds of surgeons (69%) think that failure to perform surveillance testing would hurt their rapport with patients, whereas less than half (42%) believe it would hurt their rapport with referring physicians. Respondents were evenly split (49% true, 46% false) on the notion that failure to follow-up constituted malpractice. Although not specifically addressed in this survey, it appears likely that RCST is performed essentially as a matter of habit. Postoperative surveillance testing certainly falls into the category of accepted surgical dogma, though there appears little documentation to support it.

In conclusion, RCST is widely performed by thoracic surgeons who follow their patients after lung resection. There is wide variation in both the selection of surveillance techniques and the frequency of testing. Fewer than half the respondents believe there is survival benefit from testing either identified in their practice or documented in the literature. Routine clinical surveillance testing appears to be an ingrained habit, the motivation for which involves a combination of attempts to meet patient expectations, deal with medicolegal liability, and provide clinical benefit. However, there is little objective evidence to support its use. This study highlights the need for a prospective study to identify the appropriate role and intensity of RCST in patients after lung cancer resection.


    Appendix 1.
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1.
 References
 


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Summary of Opinions from 768 Respondents
 

    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1.
 References
 
Address reprint requests to Dr Naunheim, Department of Surgery, Saint Louis University Health Sciences Center, 3635 Vista Ave at Grand Blvd, St. Louis, MO 63110-0250.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1.
 References
 

  1. Menck HR, Garfinkel L, Dodd GD. Preliminary report of the National Cancer Data Base. CA 1991;41:7–18.
  2. Wingo PA, Tong T, Bolden S. Cancer statistics 1995. CA 1995;45:8–30.[Medline]
  3. Ginsberg RJ. Follow-up supervision after resection for lung cancer. In: Delarue NC, Eschapasse H, eds. International trends in general thoracic surgery: lung cancer. 1st ed. Philadelphia: WB Saunders, 1985:274–9.
  4. The Society of Thoracic Surgeons Committee on Practice Guidelines. Practice guidelines in cardiothoracic surgery. Ann Thorac Surg 1995;60:S1–59.[Medline]
  5. Sabiston DC, Spencer FC, eds. Surgery of the chest. 5th ed. Philadelphia: WB Saunders, 1990.
  6. Baue AE, Geha AS, Hammond GL, Laks H, Naunheim KS, eds. Glenn's thoracic and cardiovascular surgery. 5th ed. Norwalk, CT: Appleton & Lange, 1991.
  7. Roth JA, Ruckdeschel JC, Weisenburger TH, eds. Thoracic oncology. 1st ed. Philadelphia: WB Saunders, 1989.
  8. Shields TW. Surgical treatment of non-small cell bronchial carcinoma. In: Shields TW, ed. General thoracic surgery. 4th ed. Baltimore: Williams & Wilkins, 1994:1178.
  9. Schapira DV, Urban N. A minimalist policy for breast cancer surveillance. JAMA 1991;265:380–2.[Medline]
  10. Del Turco MR, Palli D, Cariddi A, Ciatto S, Pacini P, Distante V. Intensive diagnostic followup after treatment of primary breast cancer: a randomized trial. JAMA 1994;271:1593–7.[Abstract]
  11. Manni JJ, DeVisscher A. Routine follow-up in patients with curative intention for squamous cell carcinoma of the larynx, pharynx and oral cavity: does it make sense [Abstract]? Presented at the 37th Annual Meeting of the Society of Head and Neck Surgeons, Maui, Hawaii, May 1991.
  12. Tornqvist A, Ekelund G, Leandoer L. The value of intensive followup after curative resection for colorectal carcinoma. Br J Surg 1982;69:725–8.[Medline]
  13. Ovaska J, Jarvinen H, Kujari H, Perttila I, Mecklin J. Surveillance after colon cancer: is it worthwhile? Gastroenterology 1990;99:1849–51.[Medline]
  14. Virgo KS, Vernava AM, Longo WE, McKirgan LW, Johnson FE. Cost of patient followup after potentially curative colon cancer treatment. JAMA (in press).
  15. Frost JK, Ball WC, Levin ML, et al. Early lung cancer detection: results of the initial (prevalence) radiologic and cytologic screening in the Johns Hopkins study. Am Rev Respir Dis 1984;130:549–54.[Medline]
  16. Flehinger BJ, Melameo MR, Zaman MB, et al. Early lung cancer detection: results of the initial (prevalence) radiologic and cytologic screening in the Memorial Sloan-Kettering study. Am Rev Respir Dis 1984;130:555–60.[Medline]
  17. Fontana RS, Sanderson DR, Taylor WF, et al. Early lung cancer detection: results of the initial (prevalence) radiologic and cytologic screening in the Mayo Clinic study. Am Rev Respir Dis 1984;130:561–5.[Medline]
  18. Virgo KS, McKirgan LW, Caputo MC, et al. Post-treatment management options for lung cancer patients. Ann Surg (in press).
  19. Pairolero PC, Williams DE, Bergstralh EJ, Piehler JM, Bernatz PE, Payne WS. Postsurgical stage I bronchogenic carcinoma: morbid implications of recurrent disease. Ann Thorac Surg 1984;38:331–8.[Abstract]
  20. Shields TW, Humphrey EW, Higgins GA, Keehn RJ. Long-term survivors after resection of lung carcinoma. J Thorac Cardiovasc Surg 1978;76:439–45.[Medline]
  21. Rosengart TK, Martini N, Ghosn P, Burt M. Multiple primary lung carcinomas: prognosis and treatment. Ann Thorac Surg 1991;52:773–9.[Abstract]
  22. Antakli T, Schaefer RF, Rutherford JE, Read RC. Second primary lung cancer. Ann Thorac Surg 1995;59:863–7.[Abstract/Free Full Text]



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