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Ann Thorac Surg 2000;69:1696-1700
© 2000 The Society of Thoracic Surgeons


Original articles: General thoracic

Who should follow up lung cancer patients after operation?

Sébastien Gilbert, MDa, Kenneth R. Reid, MDa, Miu Y. Lam, PhDb, Dimitri Petsikas, MDa

a Department of Surgery, Queen’s University, Kingston, Ontario, Canada
b Department of Community Health and Epidemiology, Queen’s University, Kingston, Ontario, Canada

Address reprint requests to Dr Petsikas, Division of Cardiothoracic Surgery, Queen’s University, 102 Stuart St, Kingston, ON K7L 2V6 Canada
e-mail: fargoc{at}post.queensu.ca


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. It is unclear whether follow-up by a thoracic surgeon after lung cancer resection alters survival.

Methods. The charts of 245 early stage (<= IIB) non–small cell lung cancer patients, diagnosed between 1988 and 1995, were reviewed. Follow-up data were complete to January 1, 1997, in 96.3% (236 of 245) of cases.

Results. Ninety of the 111 recurrences were detected before discharge from the thoracic clinic. Despite clinic follow-up, 66.7% (60 of 90) were identified by the family physician, and only 28.9% (26 of 90) by the surgeon. The remaining 4.4% (4 of 90) were detected by other physicians. Ninety-six percent (25 of 26) surgeon-detected recurrences had suspicious clinical or chest radiographic findings, compared with 92% for family physician–detected recurrences (55 of 60; not significant). The cost per recurrence detected by surgeons was Can $4,367. A 75% cost savings could ensure if patients were followed up by their family physician. There was no 5-year survival benefit for patients whose recurrence was detected by the surgeon.

Conclusions. Long-term follow-up after limited-stage non–small cell lung cancer resection could possibly be performed by a family physician alone without compromising overall survival, and with significant cost savings.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
In recent years, there has been a growing interest in improving follow-up strategies in surgically treated lung cancer patients. The importance of follow-up resides in the early detection and potentially curative treatment of recurrence [1]. Other concerns include maintenance of a sound patient–physician relationship and avoidance of medicolegal conflicts [2]. Various follow-up guidelines have already been published [3, 4]. Routine clinical surveillance testing after pulmonary resection for non–small cell lung cancer (NSCLC) is still widely accepted [5]. Survey data demonstrate a wide variation in follow-up practices among thoracic surgeons in the United States [6]. In one retrospective study, intensive follow-up did not improve outcome when compared with a strategy including less-frequent clinic visits and investigations [3]. Another retrospective trial on the usefulness of follow-up testing in surgically treated NSCLC found no improvement in outcome for recurrences detected in asymptomatic patients [1]. These authors suggest that regular follow-up of asymptomatic patients may be unnecessary and overly expensive [1].

Unlike breast cancer follow-up, postoperative surveillance of lung cancer patients has yet to be evaluated prospectively [7]. Evidence supporting regular thoracic surgery clinic follow-up in postoperative lung cancer patients is scant.

Two previous studies have reported significant proportions of recurrences detected outside scheduled clinic appointments [1, 8]. Unfortunately, it is unclear whether patients obtained a thoracic consultation on their own or were referred by another physician. This raises concerns regarding the effectiveness of regular thoracic surgery clinic follow-up in detecting cancer recurrences. This issue is addressed in the present study, along with the impact of thoracic surgery clinic follow-up on survival.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The Kingston General Hospital database was searched to identify patients treated surgically for a pulmonary neoplasm between January 1, 1988, and December 31, 1995. The following exclusion criteria were applied: (1) malignancy other than NSCLC stage IA to IIB, (2) history of previous pulmonary malignancy, (3) synchronous lung cancer primaries, (4) inability to withstand pulmonary resection, (5) use of adjuvant therapy (eg, radiation, chemotherapy), and (6) death within 30 days of operation.

The follow-up schedule consisted of clinic visits every 3 to 4 months during the first 2 years, biannually from the second to the fifth year, and yearly thereafter. The records of the thoracic surgery clinic, the regional cancer center database, referring family practitioners, and peripheral hospitals were used to determine disease-free and overall survival. Whenever necessary, patients or close relatives were contacted to complete existing records. The follow-up period extended from January 1, 1988, to December 31, 1997, ensuring a minimum postoperative follow-up of 2 years for each subject. Follow-up terminated at death, loss to follow-up, or at the end of the study period. The length of surgical follow-up, disease-free survival, and overall survival were calculated from the day of operation. Surgical follow-up ended with the last scheduled thoracic clinic appointment. The end of the disease-free interval was marked by either the onset of clinical symptoms or by the appearance of radiologic or pathologic findings consistent with cancer recurrence.

Recurrences were identified through one or more of the following: history and physical examination, chest radiography, computed tomography, nuclear bone scintigraphy, abdominal ultrasonography, or biopsy. It was also noted whether the recurrence was diagnosed by the thoracic surgeon or by another physician.

Local recurrence was defined as reappearance of cancer in the hilar or mediastinal nodes, the bronchial stump, or the ipsilateral lung parenchyma. Recurrence at any other site was considered distant. A recurrent pulmonary lesion of different histology than the index tumor was classified as a new primary tumor.

Cost analysis
The cost of follow-up appointments was determined using data from the hospital’s accounting department and from a referring family physician’s (FP) practice. The cost estimate of a surgical clinic appointment does not take into account expenses related to a hospital-based clinic (eg, rent, utilities, cost of commuting to a tertiary care center). The total cost of surgical clinic follow-up was calculated by multiplying the number of appointments by the cost per appointment. Using the length of surgical follow-up, and estimating that patients are seen six times during the first 2 years, and twice yearly thereafter, the number of thoracic clinic appointments can be calculated. The cost of detecting one recurrence was obtained by dividing the total follow-up cost by the number of recurrences detected in each setting, ie, surgery clinic versus FP’s office.

Statistical analysis
Survival intervals were calculated from the day of operation. A subject was considered disease-free until the appearance of a recurrence as identified by the different detection methods mentioned previously. Overall survival was defined as the time from operation until death, the date of the last follow-up visit, or the end of the follow-up period. All survival curves were calculated using the Kaplan-Meier method. Age, histology, pathologic stage, site of recurrence, disease-free survival less than 12 months, presentation at recurrence (asymptomatic versus symptomatic), and the physician detecting the recurrence (FP versus surgeon) were analyzed for prognostic significance. Multivariate analysis of these prognostic factors was performed using a proportional hazard regression model. Two-sided p values were calculated using either {chi}2 or log-rank tests where appropriate.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The study group included 245 surgically treated stage IA to IIB NSCLC patients. A total of 344 patients were scheduled for surgical treatment of an NSCLC between 1988 and 1995. Patients with stage III to IV NSCLC tumors were excluded. Of the remaining 268 patients, 8 died within 30 days of operation (3.2%), 6 could not tolerate pulmonary resection at the time of thoracotomy, 5 received adjuvant radiation therapy, 3 had a positive history of pulmonary neoplasm, and 1 patient had synchronous NSCLC primaries.

The sample included 144 men and 101 women with a median age of 64 years (range, 34 to 83 years). The histologic type and stage of the tumors are presented in Table 1. Various surgical procedures were performed depending on the location of the tumor and comorbid status (Table 1). The rate of major complications was 9%.


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Table 1. Study Population (n = 245)

 
Tumors were pathologically staged according to the TNM classification of malignant lung tumors [9]. Six patients (2.4%) were staged clinically using tomograms or chest radiographs. Follow-up was completed to January 1997 in 96% of patients. Of the 9 patients lost to follow-up, 7 had been transferred to the care of their FP and were subsequently lost to follow-up, and 2 moved out of the referral area. The median length of follow-up was 41 months (range, 1 to 107 months).

Recurrences
Of the 245 patients, 111 (45.3%) experienced a recurrence during the study period. The distribution of recurrences is shown in Table 2. Pathologic confirmation of recurrence was obtained in 33.3% (37 of 111) of patients. The distribution of recurrences by stage is summarized in Table 3. A majority of recurrences (75 of 111, 67.6%) presented with positive findings on history or physical examination. Computed tomography, bone scintigraphy, abdominal ultrasound, pathologic and cytologic examination, and chest radiography were also used, alone or in combination, to assess recurrence in patients who presented with positive findings on history or physical examination. In patients without symptoms or signs of recurrence, a combination of modalities was more often required to make a diagnosis. Four patients were diagnosed on the basis of history and physical examination alone. Of these 4 patients, 3 were already receiving palliative care for significant comorbid disease, and 1 had a palpable chest wall nodule, which was excised.


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Table 2. Recurrences by Site

 

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Table 3. Recurrences by Stage

 
Of the total number of recurrences, 70.3% (78 of 111) were detected by the FP, 23.4% (26 of 111) by the thoracic surgeon, and 5.4% (6 of 111) by the oncologist, the respirologist, or the pathologist. This information could not be obtained in 1 case (0.9%). Of the total number of recurrences, 81.1% (90 of 111) occurred while the patient was followed up in the thoracic surgery clinic. Within this subgroup, 66.7% (60 of 90) of recurrences were detected by the FP, 28.9% (26 of 90) by the thoracic surgeon, and 4.4% (4 of 90) by other physicians.

Table 4 describes the method of detection for recurrences detected by the FP and for those detected by the surgeon, within the period of thoracic clinic follow-up. In the latter group of 90 patients, 63.3% (57 of 90) had a symptomatic recurrence, and 36.7% (33 of 90) were asymptomatic. The proportion of symptomatic recurrences was 78.3% (47 of 60) in the FP-detected group and 30.8% (8 of 26; p < 0.001) in the surgeon-detected group. Overall, in the asymptomatic group, 24.2% (8 of 33) of recurrences were identified by chest radiograph alone, and 69.7% (23 of 33) were identified using multiple modalities. Of the latter group, 78.3% (18 of 23) had a positive chest radiograph. Of the 26 recurrences detected by the surgeon, 21 (80.7%) had suspicious clinical or chest radiographic findings, whereas the proportion of FP-detected recurrences with clinical or positive chest radiographic findings was 91.6% (55 of 60; p = 0.148).


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Table 4. Mode of Detection of Recurrences: Family Physician Versus Surgeona

 
Survival analysis
The five-year survival was 53%. Tumor stage (p = 0.0003), disease-free survival less than 12 months (p < 0.0001), and the presence of symptoms at the time of recurrence (p = 0.0379) all had a significant impact on survival. Age older than 70 years, cell type, and tumor location did not affect survival.

Within the period of surgical follow-up, recurrences detected by the surgeon were compared with those detected by the FP. As mentioned previously, symptomatic and asymptomatic recurrences were unevenly distributed between the surgeon and FP groups. Because the mode of presentation is a significant prognostic factor, survival of patients with surgeon-detected versus FP-detected recurrences was compared in both asymptomatic and symptomatic cases. There was no significant difference in 5-year survival in patients whose recurrences were detected by the surgeon as opposed to by the FP (Figs 1, 2).



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Fig 1. Overall survival in patients with symptomatic recurrences (n = 55) detected by surgeon or family physician (FP). Analysis excludes patients who had a recurrence of cancer after discharge from thoracic clinic follow-up. (NS = not significant.)

 


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Fig 2. Overall survival in patients with asymptomatic recurrences (n = 31) detected by surgeon or family physician (FP). Analysis excludes patients who had a recurrence of cancer after discharge from thoracic clinic follow-up. (NS = not significant.)

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Arguments in favor of routine surveillance of postoperative lung cancer patients include the potential for early detection of a recurrence or a new primary aerodigestive tract tumor [6, 7]. Identification and treatment of potential complications of the operation, along with maintenance of a good surgeon–patient relationship, are also part of the rationale for routine follow-up [4]. Such practice is ingrained in surgery residency training, and its justification is probably based more on surgical dogma than on experimental evidence.

In NSCLC, most surgical treatment failures occur outside the chest. Accordingly, 64.9% of subjects in this study had a distant recurrence. Despite regular surgical clinic follow-up, a physician other than the thoracic surgeon (64 of 90; 71.1%) detected most recurrences. These recurrences were detected during the interval between clinic appointments. Within the period of active surgical clinic follow-up, the majority of patients who had a recurrence presented with symptoms (75 of 90; 67.6%). The ratio of symptomatic to asymptomatic recurrences was significantly lower in the surgeon-detected group than in the FP-detected group. This can be explained by the fact that visits to the surgical clinic were scheduled regardless of the presence of symptoms. Visits to the FP in the interval between surgical clinic appointments were likely prompted by the appearance of symptoms, which could explain the higher proportion of symptomatic recurrences detected by the FP. Cough, hemoptysis, chest pain, febrile illness, anorexia, weight loss, and change in mental status are complaints common to a wide variety of diseases, including lung cancer recurrence. Patients may not necessarily associate these symptoms with recurrence. Moreover, thoracic surgeons may have difficulty dealing with such complaints in a timely fashion because of operating room time constraints during regular office hours. The wide majority of these complaints are probably dealt with by the FP. On this basis, the FP may be more likely to detect recurrences than the surgeon.

In the present study, most recurrences were detected using widely accessible modalities. Overall, 93.7% (104 of 111) of recurrences were identified on the basis of history and physical examination with or without chest radiograph. Postsurgical lung cancer surveillance could be feasible in a setting in which a physician and simple radiographic techniques are available. Moreover, as only 2.3% (2 of 86; Table 4) of recurrences were detected by physical examination alone, perhaps detailed phone surveys administered by trained nurses could be as efficient as clinic appointments with a physician. The estimated cost per recurrence detected by the thoracic surgeon is Can $4,387. If FPs were following up these patients at the same frequency, the cost per recurrence detected would be Can $1,105. These figures account for the physician’s fees, office-related expenses, and the cost of a chest radiography interpreted by the radiologist. It becomes difficult to justify such an expense when considering the possibility that no survival advantage results from having a recurrence diagnosed by a thoracic surgeon.

The limitations of this study are inherent to its retrospective design and include selection, recall, interviewer, and misclassification biases. Caution is essential in using these data to make general statements or to guide clinical practice. However, our study raises questions regarding the rationale and efficiency of follow-up by the thoracic surgeon. It may be difficult to support regular thoracic clinic follow-up after tumor resection if most recurrences are detected outside this setting.

Indefinite postoperative follow-up is appealing from a scientific and interpersonal aspect because it allows the gathering of survival data, and may foster good surgeon–patient relationships. Indeed, surgeons could be reluctant to delegate this task, as it is an integral part of their training and is believed to be an important responsibility. Nevertheless, long-term follow-up after limited-stage NSCLC resection could possibly be performed by FPs without compromising overall survival, and with significant cost savings.


    Acknowledgments
 
Supported by E.J.P. Charrette Memorial Research Fund, Queen’s University, Canada.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Walsh G.L., O’Connor M., Willis K.M., et al. Is follow-up of lung cancer patients after resection medically indicated and cost-effective?. Ann Thorac Surg 1995;60:1563-1570.[Abstract/Free Full Text]
  2. Naunheim K.S., Virgo K.S., Coplin M.A., Johnson F.E. Clinical surveillance testing after lung cancer surgery. Ann Thorac Surg 1995;60:1612-1616.[Abstract/Free Full Text]
  3. Virgo K.S., McKirgan L.W., Michele M.A., et al. Post-treatment management options for patients with lung cancer. Ann Surg 1995;222:700-710.[Medline]
  4. Hiebert C.A. The "cured" lung cancer patient. Ann Thorac Surg 1995;60:1557-1558.[Free Full Text]
  5. Martini N., Ginsberg R.J. Postresection follow-up. In: Pearson F.G., Deslauriers J., Ginsberg R.J., Hiebert C.A., McKneally M.F., Urschel H.C., Jr, eds. Thoracic surgery, 1st ed. New York: Churchill Livingstone, 1995:759-763.
  6. Johnson F.E., Naunheim K.S., Coplin M.A., Virgo K.S. Geographic variation in the conduct of patient surveillance after lung cancer surgery. J Clin Oncol 1996;14:2940-2949.[Abstract]
  7. Edelman M.J., Meyers F.J., Siegel D. The utility of follow-up after curative cancer therapy. A critical review and economic analysis. J Gen Intern Med 1997;12:318-331.[Medline]
  8. Pairolero P.C., Williams D.E., Bergstralh E.J., Piehler J.M., Bernatz P.E., Payne W.S. Postsurgical stage I bronchogenic carcinoma. Ann Thorac Surg 1984;38:331-338.[Abstract]
  9. Sobin L.H., Wittekind C.H. TNM classification of malignant tumours, 5th ed. New York: Wiley-Liss, 1997:93-97.
Accepted for publication December 2, 1999.


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