- Email: [email protected]
Clinical surveillance testing after lung cancer operations
Clinical Surveillance Testing After Lung Cancer Operations Keith S. Naunheim, MD, Katherine S. Virgo, PhD, Margaret A. Coplin, MA, and Frank E. Johnson, MD Department of Surgery, Saint Louis University Health Sciences Center and John Cochran Veterans Affairs Medical Center, St. Louis, Missouri
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 I 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.
he 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 r e c o m m e n d e d for all patients after an operation for lung cancer [3], there are no welldesigned trials demonstrating significant benefit from this practice. The explosion in medical technology over the last three decades has made multiple testing procedures widely available. A m o n g 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.
T
Accepted for publication Aug 1, 1995. Address reprint requests to Dr Naunheim, Department of Surgery, Saint Louis University Health Sciences Center, 3635Vista Ave at Grand Blvd, St. Louis, MO 63110-0250. © 1995 by The Society of Thoracic Surgeons
(Ann Thorac Surg 1995;60:1612-6)
Material and M e t h o d s In January 1994, surveys were mailed to all 3,700 m e m bers 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, 0003-4975/95/$9.50 SSDI 0003-4975(95)00762-8
Ann Thorac Surg 1995;60:1612-6
N A U N H E 1 M ET A L CLINICAL SURVEILLANCE TESTING
What is your follow-up schedule after complete surgical excision of a Stage I (T1NOM0 or T2NOM0) non-small cell lung carcinoma in an otherwise healthy patient? Please write the number of times you would require visits, tests o r procedures during each soecific time interval. If you do not perform the lest during an interval, please enter a zero in the box. All boxes should have a number entered. lstyr 2ndyr 3rdyr 4thyr 5thyr Postop
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fig 1. Format used in questionnaire. (CT = computed tomographic; MRI -- magnetic resonance imaging.)
Clinic visit Complete blood count Liver function tests Chest x-ray Chest CT scan Head CT scan Bone scan MRI Bronchoscopy Spotum cytology
I I I I I I
Ii
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 1). 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 ILIA)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. 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 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 1. The frequency of postoperative testing obtained by respondents in the first 5 years for TNM stages I, II, and IIIA is depicted in Table 2. 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. 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 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
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Ann Thorac Surg 1995;60:1612-6
Table 1. Demographic Profile of 768 Respondents" Variable
No. of Respondents
Respondent age (y) 30-39 40-49 50-59 60-69 >-70 Missing Practice type Private Academic US government Other Practice profile (%)b 0-25 26-50 51-75 76-100 Missing
122 (16) 239 (31) 236 (31) 148 (19) 15 (2) 8 (1) 490 (64) 226 (29) 48 (6) 19 (2) 275 (36) 182 (24) 88 (11) 204 (27) 19 (2)
a Numbers in parentheses are percentages, b This is percentage of practice comprising noncardiac thoracic surgery.
b e r e p r e s e n t e d in this survey. Also, the vast majority of o u r r e s p o n d e n t s were from the U n i t e d States, a n d foll o w - u p r o u t i n e s m a y differ s u b s t a n t i a l l y in other countries. No i n f o r m a t i o n was s o u g h t r e g a r d i n g the cost or clinical b e n e f i t of follow-up. However, given these limitations, the s u r v e y still p r o v i d e s v a l u a b l e i n f o r m a t i o n . More t h a n 50% of the STS m e m b e r s r e s p o n d e d , w h i c h is a n excellent result for such a survey. It is i n t e r e s t i n g that o n l y a p p r o x i m a t e l y 60% of thoracic s u r g e o n s p e r f o r m i n g l u n g resection actually p r o v i d e l o n g - t e r m oncologic surveillance. The m o s t i m p o r t a n t f i n d i n g of this s t u d y is that there is wide variation in the follow-up strategies u n d e r t a k e n by thoracic surgeons. A l t h o u g h clinic visits, chest r o e n t g e n -
ography, c o m p l e t e b l o o d counts, a n d liver f u n c t i o n tests were u n d e r t a k e n b y virtually all r e s p o n d e n t s , other tests (head c o m p u t e d t o m o g r a p h y , b o n e s c a n n i n g , chest comp u t e d t o m o g r a p h y , b r o n c h o s c o p y , s p u t u m cytology) were r o u t i n e l y p e r f o r m e d b y s o m e s u r g e o n s a n d totally i g n o r e d b y others. The wide variation in follow-up is n o t particularly s u r p r i s i n g c o n s i d e r i n g the d e a r t h of literature o n the subject. There are no specific g u i d e l i n e s s u g g e s t e d b y either the A m e r i c a n C a n c e r Society or the A m e r i c a n College of Surgeons. N o r is there m e n t i o n of p o s t o p e r a t i v e surveillance testing for a n y thoracic oncologic p r o b l e m in the r e c e n t l y p u b l i s h e d cardiothoracic surgical practice g u i d e l i n e s [41. A review of four w i d e l y r e s p e c t e d textbooks of thoracic s u r g e r y [5-8[ r e v e a l e d that the topic of p o s t o p e r a t i v e surveillance testing after l u n g cancer resection a p p e a r s in the i n d e x of o n l y one textbook [81. That citation i n c l u d e s a single p a r a g r a p h r e g a r d i n g the n e e d of follow-up b u t does n o t p r o v i d e a p r o g r a m of actual testing. The issue of the o p t i m a l clinical surveillance r e g i m e n has b e e n a d d r e s s e d for several types of cancer. Two r e c e n t studies of b r e a s t c a n c e r [9, 10] suggest that a m i n i m a l i s t strategy yields survival b e n e f i t s i n d i s t i n g u i s h a b l e from those of a n i n t e n s i v e follow-up strategy. Conversely, a r e c e n t s t u d y d e a l i n g with the follow-up for u p p e r aerodigestive tract cancers [11] suggests that patients followed m o r e i n t e n s e l y s e e m to have a b e t t e r o u t c o m e with l o n g e r survival. Studies c o n c e r n i n g foll o w - u p for colon cancer [12, 13], a l t h o u g h controversial, have i n d i c a t e d that i n t e n s i v e follow-up has no effect on survival. W h a t is clear is that there is a h u g e e c o n o m i c stake in i d e n t i f y i n g w h a t follow-up is beneficial a n d w h a t is s u p e r f l u o u s . Virgo a n d colleagues [14] have d e m o n strated that in the case of colon cancer, h u n d r e d s of m i l l i o n s of dollars w o u l d be s p e n t a n n u a l l y if aggressive follow-up r e g i m e n s were u s e d for all patients. The m a g n i t u d e of the e c o n o m i c costs of surveillance will likely prove just as great for b r o n c h o g e n i c carcinoma, as the i n c i d e n c e of this disease is e v e n h i g h e r t h a n that of colon
Table 2. Frequency of Postoperative Testing in Years 1 Through 5`'/' Year Method Clinic visit Chest roentgenography CBC LFT Chest CT Sputum cytology Bone scanning Bronchoscopy Head CT Chest MRI
1
2
3
4
5
Totalc
3.72 (1.87) 3.31 (1.73) 1.25 (1.94) 1.04 (1.82) 0.30 (0.98) 0.20 (1.36) 0.08 (0.84) 0.11 (1.23) 0.06 (0.33) 0.01 (0.10)
2.66 (1.83) 2.49 (1.63) 0.89 (1.70) 0.83 (1.67) 0.24 (0.94) 0.17 (1.32) 0.06 (0.82) 0.05 (0.82) 0.03 (0.24) 0.01 (0.02)
1.88 (1.45) 1.82 (1.44 0.65 (1.49 0.62 (1.48 0.17 (0.58 0.15 (1.27 0.03 (0.43 0.03 (0.28 0.02 (0.15) 0.01 (0.04)
1.58 (1.30) 1.53 (1.28) 0.56 (1.34) 0.52 (1.33) 0.15 (0.45) 0.13 (1.18) 0.03 (0.27) 0.02 (0.20) 0.02 (0.13) 0.01 (0.04)
1.43 (1.28) 1.38 (1.26) 0.54 (1.39) 0.50 (1.32) 0.15 (0.45) 0.13 (1.17) 0.03 (0.27) 0.02 (0.21) 0.02 (0.13) 0.01 (0.04)
11.27d 10.53 d
3.894 3.514 1.01~ 0.78 0.23~ 0.23f 0.154
0.05
Data are shown as the average frequency with which the 768 respondents would perform each test with the standard deviation in parentheses, b The p value denotes significance of variation in testing frequency over time for each method as analyzed with a one-way analysis of variance, c This column represents the sum of the averages for years I through 5. d Significance:p < 0.0001. ~"Significance:p < 0.05. ~Significance:p < 0.001. CBC = complete blood cell count; CT - computed tomography; LFT = liver function tests; MRI = magnetic resonance imaging.
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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 p e r f o r m e d on highrisk patient populations in the 1970s at Johns Hopkins [151, Memorial Sloan-Kettering [16], a n d the Mayo Clinic [17]. Although these screening studies did not definitively d e m o n s t r a t e a survival advantage for systemically screened high-risk patients, a greater percentage of lung cancers were d i a g n o s e d at an early stage, thus allowing potentially curative treatment. It might be h o p e d that a similar advantage could be achieved by aggressive postoperative RCST a n d that this might result in i m p r o v e d survival. However, in the only p u b l i s h e d analysis of RCST, Virgo and associates [18] c o m p a r e d a population of patients who were followed up intensively with one followed less intensively after lung resection p e r f o r m e d 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 w h e n all t u m o r stages were analyzed together and when stage ! tumors were analyzed separately. The r e s p o n d e n t s ' attitudes toward the clinical benefit of or rationale for routine surveillance testing were also interesting in their variation. The rationale b e h i n d the clinical benefit of RCST includes three concepts about which there was little a g r e e m e n t a m o n g 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 r e s p o n d e n t s believe that routine surveillance w o u l d either lead to cure (42%) or lengthen survival (45%) in such patients. However, 69% did believe i m p r o v e m e n t in quality of life might be achievable.
2. RCST allows early detection and cure of a second primary tumor (question 4). There was an o v e r w h e l m i n g sentim e n t (84%) that this is a true statement. However, it is i m p o r t a n t to realize that such a strategy will benefit only a m i n o r fraction of lung cancer patients. Only 21% of patients seen with lung cancer u n d e r g o operation [1], and only about 10% of those (2% of the total) will have d e v e l o p m e n t of a second p r i m a r y 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, 221. This indicates that a curative outcome for second p r i m a r y carcinoma can be anticipated in only 0.25% of patients who are seen with an initial p r i m a r y lung cancer, a figure that is disappointingly small considering the economic expenditure r e q u i r e d to identify a second p r i m a r y lung cancer. These progressively diminishing returns m a y also be the reason b e h i n d the a n s w e r to question 5.
3. RCST for stage I lung cancer patients yields what degree of benefit? (question 5a-c). Although a large majority (89%)
NAUNHEIM ET AL CLINICALSURVEILLANCETESTING
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believe that an occasional patient m a y 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 r e s p o n d e n t s thought that there was no documentation of clinical benefit that could be found in the literature. If the majority of r e s p o n d i n g 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 a t t e m p t to identify possible motivations for testing other than clinical benefit. More than two thirds of surgeons (69%) think that failure to p e r f o r m surveillance testing w o u l d hurt their r a p p o r t with patients, w h e r e a s less than half (42%) believe it w o u l d hurt their r a p p o r t with referring physicians. R e s p o n d e n t s were evenly split (49% true, 46% false) on the notion that failure to follow-up constituted malpractice. Although not specifically a d d r e s s e d in this survey, it a p p e a r s likely that RCST is p e r f o r m e d essentially as a matter of habit. Postoperative surveillance testing certainly falls into the category of accepted surgical dogma, though there a p p e a r s little d o c u m e n t a tion to s u p p o r t it. In conclusion, RCST is widely p e r f o r m e d 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 r e s p o n d e n t s believe there is survival benefit from testing either identified in their practice or docum e n t e d in the literature. Routine clinical surveillance testing a p p e a r s to be an i n g r a i n e d 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 s u p p o r t its use. This study highlights the n e e d for a prospective study to identify the a p p r o p r i a t e role a n d intensity of RCST in patients after lung cancer resection.
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. 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:$1-59. 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
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9. 10. 11.
12. 13. 14. 15.
16.
17.
18. 19.
20. 21. 22.
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carcinoma. In: Shields TW, ed. General thoracic surgeD,. 4th ed. Baltimore: Williams & Wilkins, 1994:1178. Schapira DV, Urban N. A minimalist policy for breast cancer surveillance. JAMA 1991;265:380-2. 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. 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 a n d Neck Surgeons, Maui, Hawaii, May 1991. Tornqvist A, Ekelund G, Leandoer L. The value of intensive followup after curative resection for colorectal carcinoma. Br J Surg 1982;69:725-8. Ovaska J, Jarvinen H, Kujari H, Perttila I, Mecklin J. Surveillance after colon cancer: is it worthwhile? Gastroenterology 1990;99:1849-51. Virgo KS, Vernava AM, Longo WE, McKirgan LW, Johnson FE. Cost of patient followup after potentially curative colon cancer treatment. JAMA (in press). 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. 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. 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. Virgo KS, McKirgan LW, Caputo MC, et al. Post-treatment m a n a g e m e n t options for lung cancer patients. A n n Surg (in press). 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;38:33l-8. Shields TW, H u m p h r e y EW, Higgins GA, Keehn RJ. Longterm survivors after resection of lung carcinoma. J Thorac Cardiovasc Surg 1978;76:439-45. Rosengart TK, Martini N, Ghosn P, Burt M. Multiple primary lung carcinomas: prognosis and treatment. Ann Thorac Surg 1991;52:773-9. Antakli T, Schaefer RF, Rutherford JE, Read RC. Second primary lung cancer. Ann Thorac Surg 1995;59:863-7.
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Appendix 1. S u m m a r y Respondents
of
Opinions
Question
1. Routine follow-up testing is likely to
2.
3.
4.
5.
6.
7.
8.
9.
10.
result in a diagnosis of recurrent cancer early enough to institute potentially curative treatment for that recurrence. Routine follow-up testing which leads to early diagnosis of recurrent cancer usually allows for immediate palliative treatment that measurably lengthens patient survival. Routine follow-up testing which leads to early diagnosis of recurrent cancer allows usually for immediate palliative treatment that measurably improves the quality of the patient's remaining life span. Routine follow-up testing is likely to result in early diagnosis of a second primary lung cancer which can be cured. Routine follow-up testing for resected stage I non-small cell lung cancer patients sometimes allows for earlier detection and treatment of recurrent cancer or second primary lung cancers. In these instances, routine follow-up: a. Yields no survival benefit for any patient. b. Yields a survival benefit for a rare individual patient but has no measurable impact on overall survival for this group. c. Yields an appreciable survival benefit for the group as a whole. Routine follow-up testing for resected stage Il and stage IIIA n o n small cell lung cancer patients sometimes allows earlier detection and treatment of recurrent cancer or second primary lung cancers. In these instances routine follow-up: a. Yields no survival benefit for any patient. b. Yields survival benefit for a rare individual patient but has no measurable impact on overall survival for this group. c. Yields an appreciable survival benefit for the group as a whole. Failure to perform routine follow-up testing at least once per year would probably damage my rapport with referring physicians. Failure to perform routine follow-up testing at least once per year would probably damage my rapport with patients. Failure to perform routine follow-up testing at least once per year is malpractice. Current literature documents significant survival benefits for follow-up testing.
from 768
True False Missing (%) (%) (%) 42
56
2
45
52
3
69
27
3
84
14
2
5
89
7
54
41
4
44
49
7
19
74
7
75
21
3
17
75
8
42
54
3
69
28
3
49
46
6
26
66
8
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 I 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.
he 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 r e c o m m e n d e d for all patients after an operation for lung cancer [3], there are no welldesigned trials demonstrating significant benefit from this practice. The explosion in medical technology over the last three decades has made multiple testing procedures widely available. A m o n g 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.
T
Accepted for publication Aug 1, 1995. Address reprint requests to Dr Naunheim, Department of Surgery, Saint Louis University Health Sciences Center, 3635Vista Ave at Grand Blvd, St. Louis, MO 63110-0250. © 1995 by The Society of Thoracic Surgeons
(Ann Thorac Surg 1995;60:1612-6)
Material and M e t h o d s In January 1994, surveys were mailed to all 3,700 m e m bers 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, 0003-4975/95/$9.50 SSDI 0003-4975(95)00762-8
Ann Thorac Surg 1995;60:1612-6
N A U N H E 1 M ET A L CLINICAL SURVEILLANCE TESTING
What is your follow-up schedule after complete surgical excision of a Stage I (T1NOM0 or T2NOM0) non-small cell lung carcinoma in an otherwise healthy patient? Please write the number of times you would require visits, tests o r procedures during each soecific time interval. If you do not perform the lest during an interval, please enter a zero in the box. All boxes should have a number entered. lstyr 2ndyr 3rdyr 4thyr 5thyr Postop
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fig 1. Format used in questionnaire. (CT = computed tomographic; MRI -- magnetic resonance imaging.)
Clinic visit Complete blood count Liver function tests Chest x-ray Chest CT scan Head CT scan Bone scan MRI Bronchoscopy Spotum cytology
I I I I I I
Ii
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 1). 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 ILIA)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. 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 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 1. The frequency of postoperative testing obtained by respondents in the first 5 years for TNM stages I, II, and IIIA is depicted in Table 2. 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. 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 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
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Table 1. Demographic Profile of 768 Respondents" Variable
No. of Respondents
Respondent age (y) 30-39 40-49 50-59 60-69 >-70 Missing Practice type Private Academic US government Other Practice profile (%)b 0-25 26-50 51-75 76-100 Missing
122 (16) 239 (31) 236 (31) 148 (19) 15 (2) 8 (1) 490 (64) 226 (29) 48 (6) 19 (2) 275 (36) 182 (24) 88 (11) 204 (27) 19 (2)
a Numbers in parentheses are percentages, b This is percentage of practice comprising noncardiac thoracic surgery.
b e r e p r e s e n t e d in this survey. Also, the vast majority of o u r r e s p o n d e n t s were from the U n i t e d States, a n d foll o w - u p r o u t i n e s m a y differ s u b s t a n t i a l l y in other countries. No i n f o r m a t i o n was s o u g h t r e g a r d i n g the cost or clinical b e n e f i t of follow-up. However, given these limitations, the s u r v e y still p r o v i d e s v a l u a b l e i n f o r m a t i o n . More t h a n 50% of the STS m e m b e r s r e s p o n d e d , w h i c h is a n excellent result for such a survey. It is i n t e r e s t i n g that o n l y a p p r o x i m a t e l y 60% of thoracic s u r g e o n s p e r f o r m i n g l u n g resection actually p r o v i d e l o n g - t e r m oncologic surveillance. The m o s t i m p o r t a n t f i n d i n g of this s t u d y is that there is wide variation in the follow-up strategies u n d e r t a k e n by thoracic surgeons. A l t h o u g h clinic visits, chest r o e n t g e n -
ography, c o m p l e t e b l o o d counts, a n d liver f u n c t i o n tests were u n d e r t a k e n b y virtually all r e s p o n d e n t s , other tests (head c o m p u t e d t o m o g r a p h y , b o n e s c a n n i n g , chest comp u t e d t o m o g r a p h y , b r o n c h o s c o p y , s p u t u m cytology) were r o u t i n e l y p e r f o r m e d b y s o m e s u r g e o n s a n d totally i g n o r e d b y others. The wide variation in follow-up is n o t particularly s u r p r i s i n g c o n s i d e r i n g the d e a r t h of literature o n the subject. There are no specific g u i d e l i n e s s u g g e s t e d b y either the A m e r i c a n C a n c e r Society or the A m e r i c a n College of Surgeons. N o r is there m e n t i o n of p o s t o p e r a t i v e surveillance testing for a n y thoracic oncologic p r o b l e m in the r e c e n t l y p u b l i s h e d cardiothoracic surgical practice g u i d e l i n e s [41. A review of four w i d e l y r e s p e c t e d textbooks of thoracic s u r g e r y [5-8[ r e v e a l e d that the topic of p o s t o p e r a t i v e surveillance testing after l u n g cancer resection a p p e a r s in the i n d e x of o n l y one textbook [81. That citation i n c l u d e s a single p a r a g r a p h r e g a r d i n g the n e e d of follow-up b u t does n o t p r o v i d e a p r o g r a m of actual testing. The issue of the o p t i m a l clinical surveillance r e g i m e n has b e e n a d d r e s s e d for several types of cancer. Two r e c e n t studies of b r e a s t c a n c e r [9, 10] suggest that a m i n i m a l i s t strategy yields survival b e n e f i t s i n d i s t i n g u i s h a b l e from those of a n i n t e n s i v e follow-up strategy. Conversely, a r e c e n t s t u d y d e a l i n g with the follow-up for u p p e r aerodigestive tract cancers [11] suggests that patients followed m o r e i n t e n s e l y s e e m to have a b e t t e r o u t c o m e with l o n g e r survival. Studies c o n c e r n i n g foll o w - u p for colon cancer [12, 13], a l t h o u g h controversial, have i n d i c a t e d that i n t e n s i v e follow-up has no effect on survival. W h a t is clear is that there is a h u g e e c o n o m i c stake in i d e n t i f y i n g w h a t follow-up is beneficial a n d w h a t is s u p e r f l u o u s . Virgo a n d colleagues [14] have d e m o n strated that in the case of colon cancer, h u n d r e d s of m i l l i o n s of dollars w o u l d be s p e n t a n n u a l l y if aggressive follow-up r e g i m e n s were u s e d for all patients. The m a g n i t u d e of the e c o n o m i c costs of surveillance will likely prove just as great for b r o n c h o g e n i c carcinoma, as the i n c i d e n c e of this disease is e v e n h i g h e r t h a n that of colon
Table 2. Frequency of Postoperative Testing in Years 1 Through 5`'/' Year Method Clinic visit Chest roentgenography CBC LFT Chest CT Sputum cytology Bone scanning Bronchoscopy Head CT Chest MRI
1
2
3
4
5
Totalc
3.72 (1.87) 3.31 (1.73) 1.25 (1.94) 1.04 (1.82) 0.30 (0.98) 0.20 (1.36) 0.08 (0.84) 0.11 (1.23) 0.06 (0.33) 0.01 (0.10)
2.66 (1.83) 2.49 (1.63) 0.89 (1.70) 0.83 (1.67) 0.24 (0.94) 0.17 (1.32) 0.06 (0.82) 0.05 (0.82) 0.03 (0.24) 0.01 (0.02)
1.88 (1.45) 1.82 (1.44 0.65 (1.49 0.62 (1.48 0.17 (0.58 0.15 (1.27 0.03 (0.43 0.03 (0.28 0.02 (0.15) 0.01 (0.04)
1.58 (1.30) 1.53 (1.28) 0.56 (1.34) 0.52 (1.33) 0.15 (0.45) 0.13 (1.18) 0.03 (0.27) 0.02 (0.20) 0.02 (0.13) 0.01 (0.04)
1.43 (1.28) 1.38 (1.26) 0.54 (1.39) 0.50 (1.32) 0.15 (0.45) 0.13 (1.17) 0.03 (0.27) 0.02 (0.21) 0.02 (0.13) 0.01 (0.04)
11.27d 10.53 d
3.894 3.514 1.01~ 0.78 0.23~ 0.23f 0.154
0.05
Data are shown as the average frequency with which the 768 respondents would perform each test with the standard deviation in parentheses, b The p value denotes significance of variation in testing frequency over time for each method as analyzed with a one-way analysis of variance, c This column represents the sum of the averages for years I through 5. d Significance:p < 0.0001. ~"Significance:p < 0.05. ~Significance:p < 0.001. CBC = complete blood cell count; CT - computed tomography; LFT = liver function tests; MRI = magnetic resonance imaging.
Ann Thorac Surg 1995;60:1612-6
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 p e r f o r m e d on highrisk patient populations in the 1970s at Johns Hopkins [151, Memorial Sloan-Kettering [16], a n d the Mayo Clinic [17]. Although these screening studies did not definitively d e m o n s t r a t e a survival advantage for systemically screened high-risk patients, a greater percentage of lung cancers were d i a g n o s e d at an early stage, thus allowing potentially curative treatment. It might be h o p e d that a similar advantage could be achieved by aggressive postoperative RCST a n d that this might result in i m p r o v e d survival. However, in the only p u b l i s h e d analysis of RCST, Virgo and associates [18] c o m p a r e d a population of patients who were followed up intensively with one followed less intensively after lung resection p e r f o r m e d 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 w h e n all t u m o r stages were analyzed together and when stage ! tumors were analyzed separately. The r e s p o n d e n t s ' attitudes toward the clinical benefit of or rationale for routine surveillance testing were also interesting in their variation. The rationale b e h i n d the clinical benefit of RCST includes three concepts about which there was little a g r e e m e n t a m o n g 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 r e s p o n d e n t s believe that routine surveillance w o u l d either lead to cure (42%) or lengthen survival (45%) in such patients. However, 69% did believe i m p r o v e m e n t in quality of life might be achievable.
2. RCST allows early detection and cure of a second primary tumor (question 4). There was an o v e r w h e l m i n g sentim e n t (84%) that this is a true statement. However, it is i m p o r t a n t to realize that such a strategy will benefit only a m i n o r fraction of lung cancer patients. Only 21% of patients seen with lung cancer u n d e r g o operation [1], and only about 10% of those (2% of the total) will have d e v e l o p m e n t of a second p r i m a r y 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, 221. This indicates that a curative outcome for second p r i m a r y carcinoma can be anticipated in only 0.25% of patients who are seen with an initial p r i m a r y lung cancer, a figure that is disappointingly small considering the economic expenditure r e q u i r e d to identify a second p r i m a r y lung cancer. These progressively diminishing returns m a y also be the reason b e h i n d the a n s w e r to question 5.
3. RCST for stage I lung cancer patients yields what degree of benefit? (question 5a-c). Although a large majority (89%)
NAUNHEIM ET AL CLINICALSURVEILLANCETESTING
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believe that an occasional patient m a y 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 r e s p o n d e n t s thought that there was no documentation of clinical benefit that could be found in the literature. If the majority of r e s p o n d i n g 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 a t t e m p t to identify possible motivations for testing other than clinical benefit. More than two thirds of surgeons (69%) think that failure to p e r f o r m surveillance testing w o u l d hurt their r a p p o r t with patients, w h e r e a s less than half (42%) believe it w o u l d hurt their r a p p o r t with referring physicians. R e s p o n d e n t s were evenly split (49% true, 46% false) on the notion that failure to follow-up constituted malpractice. Although not specifically a d d r e s s e d in this survey, it a p p e a r s likely that RCST is p e r f o r m e d essentially as a matter of habit. Postoperative surveillance testing certainly falls into the category of accepted surgical dogma, though there a p p e a r s little d o c u m e n t a tion to s u p p o r t it. In conclusion, RCST is widely p e r f o r m e d 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 r e s p o n d e n t s believe there is survival benefit from testing either identified in their practice or docum e n t e d in the literature. Routine clinical surveillance testing a p p e a r s to be an i n g r a i n e d 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 s u p p o r t its use. This study highlights the n e e d for a prospective study to identify the a p p r o p r i a t e role a n d intensity of RCST in patients after lung cancer resection.
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. 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:$1-59. 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
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9. 10. 11.
12. 13. 14. 15.
16.
17.
18. 19.
20. 21. 22.
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carcinoma. In: Shields TW, ed. General thoracic surgeD,. 4th ed. Baltimore: Williams & Wilkins, 1994:1178. Schapira DV, Urban N. A minimalist policy for breast cancer surveillance. JAMA 1991;265:380-2. 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. 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 a n d Neck Surgeons, Maui, Hawaii, May 1991. Tornqvist A, Ekelund G, Leandoer L. The value of intensive followup after curative resection for colorectal carcinoma. Br J Surg 1982;69:725-8. Ovaska J, Jarvinen H, Kujari H, Perttila I, Mecklin J. Surveillance after colon cancer: is it worthwhile? Gastroenterology 1990;99:1849-51. Virgo KS, Vernava AM, Longo WE, McKirgan LW, Johnson FE. Cost of patient followup after potentially curative colon cancer treatment. JAMA (in press). 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. 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. 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. Virgo KS, McKirgan LW, Caputo MC, et al. Post-treatment m a n a g e m e n t options for lung cancer patients. A n n Surg (in press). 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;38:33l-8. Shields TW, H u m p h r e y EW, Higgins GA, Keehn RJ. Longterm survivors after resection of lung carcinoma. J Thorac Cardiovasc Surg 1978;76:439-45. Rosengart TK, Martini N, Ghosn P, Burt M. Multiple primary lung carcinomas: prognosis and treatment. Ann Thorac Surg 1991;52:773-9. Antakli T, Schaefer RF, Rutherford JE, Read RC. Second primary lung cancer. Ann Thorac Surg 1995;59:863-7.
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Appendix 1. S u m m a r y Respondents
of
Opinions
Question
1. Routine follow-up testing is likely to
2.
3.
4.
5.
6.
7.
8.
9.
10.
result in a diagnosis of recurrent cancer early enough to institute potentially curative treatment for that recurrence. Routine follow-up testing which leads to early diagnosis of recurrent cancer usually allows for immediate palliative treatment that measurably lengthens patient survival. Routine follow-up testing which leads to early diagnosis of recurrent cancer allows usually for immediate palliative treatment that measurably improves the quality of the patient's remaining life span. Routine follow-up testing is likely to result in early diagnosis of a second primary lung cancer which can be cured. Routine follow-up testing for resected stage I non-small cell lung cancer patients sometimes allows for earlier detection and treatment of recurrent cancer or second primary lung cancers. In these instances, routine follow-up: a. Yields no survival benefit for any patient. b. Yields a survival benefit for a rare individual patient but has no measurable impact on overall survival for this group. c. Yields an appreciable survival benefit for the group as a whole. Routine follow-up testing for resected stage Il and stage IIIA n o n small cell lung cancer patients sometimes allows earlier detection and treatment of recurrent cancer or second primary lung cancers. In these instances routine follow-up: a. Yields no survival benefit for any patient. b. Yields survival benefit for a rare individual patient but has no measurable impact on overall survival for this group. c. Yields an appreciable survival benefit for the group as a whole. Failure to perform routine follow-up testing at least once per year would probably damage my rapport with referring physicians. Failure to perform routine follow-up testing at least once per year would probably damage my rapport with patients. Failure to perform routine follow-up testing at least once per year is malpractice. Current literature documents significant survival benefits for follow-up testing.
from 768
True False Missing (%) (%) (%) 42
56
2
45
52
3
69
27
3
84
14
2
5
89
7
54
41
4
44
49
7
19
74
7
75
21
3
17
75
8
42
54
3
69
28
3
49
46
6
26
66
8