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1932
How Tumor Stage Affects Surgeons’ Surveillance
Strategies after Surgery for Carcinoma of the Upper
Aerodigestive Tract
Frank E. Johnson, M.D.1,2
Katherine S. Virgo, Ph.D.1,2
Marc F. Clemente, M.D.1.2
Michael H. Johnson1
Randal C. Paniello, M.D.1,3
BACKGROUND. The factors that influence decision-making among surgeons are not
well understood. The authors evaluated how tumor stage in otherwise healthy
patients subjected to potentially curative surgery for upper aerodigestive tract
(UADT) epidermoid carcinoma affects the self-reported follow-up strategies employed by practicing surgeons.
METHODS. Hypothetical patient profiles and a detailed questionnaire based on
1
Surgery Service, Department of Veterans Affairs Medical Center, St. Louis, Missouri.
2
Department of Surgery, Saint Louis University
School of Medicine, St. Louis, Missouri.
3
Department of Otolaryngology, Washington
University School of Medicine, St. Louis, Missouri.
these profiles were mailed to the 824 members of the Society of Head and Neck
Surgeons (SHNS) and the 522 members of the American Society for Head and
Neck Surgery who were not members of SHNS. The effect of TNM stage on the
surveillance strategies chosen by the respondents was analyzed.
RESULTS. Ten of the 14 most commonly employed surveillance modalities were
ordered significantly more frequently with increasing TNM stage. This effect persisted through 5 years of follow-up, but the differences across stages were small.
Only 30% of respondents modified their strategies according to the patient’s TNM
stage.
CONCLUSIONS. Most surgeons performing surveillance after potentially curative
surgery in otherwise healthy patients with UADT carcinoma use the same followup strategy irrespective of TNM stage. These data permit rational design of a
randomized clinical trial of two alternate follow-up plans. Cancer 1998;82:
1932–7. q 1998 American Cancer Society.
KEYWORDS: surveillance, upper aerodigestive tract, carcinoma, TNM stage, survey.
C
Supported in part by the Department of Veterans Affairs Medical Center, St. Louis, Missouri.
Address for reprints: Frank E. Johnson, M.D.
Department of Surgery, St. Louis University
Health Sciences Center, 3635 Vista Avenue, St.
Louis, MO 63110-0250.
The views expressed in this article are those of
the authors and should not be construed to
reflect the official position of Saint Louis University, Washington University, or the Department
of Veterans Affairs.
Received July 31, 1997; revision received December 1, 1997; accepted December 10, 1997.
ure of epidermoid carcinoma of the upper aerodigestive tract
(UADT) was rare until this century and the natural history of this
disorder frequently was unmodified by effective therapy. For example,
Ulysses S. Grant, a dominant figure in the American Civil War and a
former President, was offered only symptomatic therapy for his tonsillar carcinoma late in the 19th century because surgery was judged
to be too hazardous.1 With the advent of modern techniques, the
diagnosis now can be made reliably and safely in most patients. Current concepts of pathophysiology permit rational therapy, and the
majority of patients in the U. S. undergo therapy with curative intent.
The global incidence of squamous cell carcinoma of the UADT
has been estimated at 500,000 cases per year.2 Among the approximately 50,000 new cases of head and neck carcinoma diagnosed annually in the U. S., the majority of patients with early stage disease
will be cured, and the majority with late stage disease will not.3 Patients with recurrence of the index lesion are often, but not always,
incurable.4 In addition, second primary UADT neoplasms are frequent
in this patient population. The therapy of second primary UADT tu-
q 1998 American Cancer Society
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W: Cancer
Cancer Patient Follow-Up/Johnson et al.
TABLE 1
Rationale for Surveillance after Potentially Curative UADT Carcinoma
Treatment
Early detection of recurrence of the index tumor, leading to early treatment
Detection of second primary tumors, leading to early treatment
Detection of other smoking-related disorders that may warrant intervention
Detection of complications of initial therapy of the index tumor, leading to
remedial efforts
Audit of results of therapy for the index tumor
Rehabilitation
Psychologic support
Risk counseling for patient and family members
Avoidance of medical malpractice risks
Maintenance of rapport with referring physicians
Maintenance of rapport with patient
Routine health care maintenance to improve overall quality of life
UADT: upper aerodigestive tract.
mors always has been recognized as a sound enterprise with a reasonable chance of success.5 Patients
with resected carcinoma of the UADT also are at increased risk for other diseases related to tobacco
smoking such as atherosclerosis, emphysema, and
bladder carcinoma.6,7 These factors have led to a
strong demand on the part of patients for effective
treatment when recurrence, a new primary tumor, or
another smoking-related disorder is diagnosed. This
desire coincides with the aims of the surgeon who
performed the original surgery. The majority of surgeons follow their head and neck carcinoma patients
postoperatively8 and believe that earlier diagnosis of
malignancy may lead to a better chance of therapeutic
success. This line of reasoning underlies much of the
philosophy and practice of surveillance in patients
treated for cure. As our understanding of the biology
and natural history of this disease has improved, many
more diagnostic tests for detecting cancer have become available, leading to better patient outcomes.
The motivation for follow-up is difficult to define and
varies from physician to physician (Table 1). A recent
sampling of practice patterns at well known institutions around the world indicates that 14 specific modalities are used in postoperative surveillance. They
are: office visit, complete blood count, serum electrolytes ({ calcium), liver function tests, thyroid function
tests, serum tumor marker measurement,9 chest X-ray,
head/neck computed tomography (CT) scan, chest CT
scan, magnetic resonance imaging of the head/neck,
sonogram of the head/neck, bone scan, bronchoscopy, and esophagoscopy.8 However, many of these
are rarely used by surgeons in the U. S.3 None is simultaneously specific, comfortable, safe, inexpensive, and
convenient, but a combination of tests can be clinically useful.10
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1933
We have estimated the costs of several follow-up
strategies for carcinoma of the UADT,11 and they are
sizable. The rapid rise in medical care costs increasingly has led to the application of business methods
to control them.12 These market forces have tended
to restrict physician autonomy, provoking publicity,13
editorial comment,14,15,16 and animosity.16 A likely area
for cost-containment efforts is in the follow-up of
asymptomatic cancer patients. One method of cost
containment is to determine which surveillance methods are of actual value as measured by increased patient survival and/or quality of life. We previously reported the results of a survey of the members of the
Society of Head and Neck Surgeons (SHNS) designed
to evaluate how physicians actually caring for such
patients select their postoperative follow-up strategies.8 The members of the American Society for Head
and Neck Surgery (ASHNS) then were canvassed using
the same instrument to quantify their self-reported
practice patterns (unpublished data). Both societies
are influential; their members care for many UADT
carcinoma patients and often assess the results of
management and report them in the medical literature. Our surveys revealed that the posttreatment surveillance schemes advocated by members of these societies were quite similar to each other and to the
clinical practice guidelines issued by the two societies
recently.17 In this article. we report the effect of TNM
stage18 on the patterns of surveillance testing employed by these highly credentialed experts. These results do not permit us to recommend whether different follow-up strategies are warranted for patients
with different TNM stages. There are few data to document whether any surveillance scheme is beneficial,
whether measured by patient survival, quality of life,
or cost-adjusted parameters. However, the results do
permit the rational design of a randomized clinical
trial comparing more intensive and less intensive follow-up strategies. Such trials are needed to document
the advantages, disadvantages, and costs11 of posttreatment surveillance.
MATERIALS AND METHODS
Surveys of all active members of the SHNS and ASHNS
were performed in 1996. The survey instrument and
survey techniques have been described in detail elsewhere.8 All active members were sent the survey instrument, an introductory cover letter, and a self-addressed, stamped envelope. Only surgeons who personally follow their patients after UADT carcinoma
surgery were requested to complete the questionnaire.
The mechanism of soliciting respondents eliminated
nonsurgeon members of the societies. The surveillance tests employed were chosen after pilot studies
W: Cancer
1934
CANCER May 15, 1998 / Volume 82 / Number 10
of members indicated that no other tests were chosen
routinely. Other pertinent literature3,8 reinforced our
view that these surveillance tests represented a complete list. Those not responding to the first mailing
were solicited again 2 months later. Repeated-measures analysis of variance was used to compare practice patterns by TNM stage and postoperative year.
Statistical significance was set at P õ 0.05.
modalities. However, this effect is clinically small. Test
frequency did not differ significantly by stage for esophagoscopy, ultrasonography, bronchoscopy, and tumor markers. Significant main effects (P õ 0.01) of
years after surgery also were detected for all followup modalities except bone scan and tumor markers.
In addition, a significant interaction effect (P õ 0.01)
between stage and year after surgery was detected for
all follow-up modalities except tumor markers.
RESULTS
There were 351 responses from the 824 SHNS members (44% of 800; 24 were returned as addressee unknown); 199 of the SHNS respondents perform surgery
on UADT carcinoma patients, provide long term follow-up, and described their follow-up in sufficient detail to be evaluable. There were 259 responses from
the 522 ASHNS members who were not SHNS members (93 were members of both) (50% return rate); 221
of the ASHNS respondents were evaluable according
to the same criteria. These 420 responses form the
basis of this analysis. Most society members practice
in large and medium-sized cities. Thus, one limitation
of this study is that surgeons in rural practice may not
be represented fully. However, a full spectrum of ages
was represented. The age distribution was õ 40 years
(13%), 40 – 49 years (36%), 50 – 59 years (33%), 60 – 69
years (15%), and ú 70 years (3%); these data were
missing for 1% of respondents.
The frequencies of the 14 surveillance tests requested by respondents for hypothetical patients with
Stage I, II, or III / resectable IV disease described in
the survey instrument are tabulated (Table 2). The
mean frequency of testing increases only slightly, if at
all, for each modality as TNM stage increases. This
would suggest that follow-up strategies generally are
selected irrespective of TNM stage. In fact, 295 of the
420 respondents (70%) reported that they follow TNM
Stage I, II, and III / resectable IV patients identically.
Only 125 (30%) vary the strategy by TNM stage. Correlation analysis revealed that the mean frequency of
use of most follow-up modalities was highly correlated
(correlation coefficient ú 0.75) across years after surgery. In other words, the follow-up strategy in Year 1
was highly correlated with the strategy selected for
Year 2, which also was highly correlated with that selected for Year 3, and so on. Because observations
from the same subject are not independent, repeatedmeasures analysis of variance was chosen as the
method of analysis. Repeated-measures analysis of
variance was performed on the data to compare means
for each testing modality by stage and by year after
surgery, and to test the interaction between stage and
year after surgery. Significant main effects (P õ 0.01)
were detected for TNM stage for 10 of 14 follow-up
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DISCUSSION
Little is known regarding how surgeons reach decisions. The data reported here indicate that, in otherwise healthy patients subjected to potentially curative
surgery, the intensity of follow-up chosen by surgeons
largely is independent of TNM stage. The office visit
is the mainstay of surveillance, although other modalities also are used regularly. Expensive and invasive
studies are used rarely. This is the first direct, empiric
evidence from a nationwide sample of surgeons documenting that the effect of tumor stage on surveillance
strategy is small, although statistically significant. This
stage-specific effect persists for at least 5 years after
surgery for all the commonly employed testing modalities. Any randomized controlled clinical trial of follow-up strategies should take into account these current follow-up practice patterns to be acceptable to
physicians entering patients. Such trials are feasible,19
although they are costly and difficult to perform, with
many potentially confounding variables.3
Medicine is an art as well as a science. Many consider it a calling. In recent years medicine also has
been viewed as a business, bringing cost-benefit analysis and customer satisfaction assessment to the fore.
We previously have shown that follow-up is expensive.11 The cost of high intensity follow-up is, not surprisingly, several times that of low intensity followup, a discrepancy that will be increasingly difficult to
defend in the future. Virtually all analyses indicate that
the risk of recurrence of the index carcinoma increases
with increasing TNM stage, but the practice patterns
documented here do not reflect a clinically important
variation in strategy for patients of different stages.
The chance of successful salvage therapy, which is
modest, may well not justify an intensive search for
such recurrence. In addition, history and physical examination represents a reasonably sensitive tool for
diagnosis of recurrent disease.10 Cost-effectiveness
also may be a factor in physician decision-making.
Conversely, because potentially curative treatment of
metachronous second primary tumors has a realistic
chance of a favorable outcome,5 a stronger justification can be offered for this practice. The risk of a second primary UADT tumor in this patient population
W: Cancer
Cancer Patient Follow-Up/Johnson et al.
1935
TABLE 2
Stage-Specific Follow-Up Practice Patterns
Stage Ib
Stage II
Stage III/ (resectable) IV
Postop
year
No.a
Mean { SD
No.
Mean { SD
No.
Mean { SD
Office visit
1
2
3
4
5
411
409
409
409
408
8.6 { 3.4
5.0 { 1.7
3.4 { 1.1
2.4 { 0.9
1.8 { 0.8
410
407
407
407
406
8.8 { 3.3
5.2 { 1.7
3.5 { 1.1
2.5 { 1.0
1.9 { 0.9
411
408
408
408
407
9.0 { 3.3
5.3 { 1.8
3.6 { 1.2
2.6 { 1.1
2.0 { 1.0
Complete blood
count
1
2
3
4
5
386
372
370
370
370
0.9 { 1.3
0.6 { 0.9
0.5 { 0.7
0.4 { 0.6
0.4 { 0.6
385
371
371
369
370
0.9 { 1.3
0.6 { 0.9
0.5 { 0.8
0.4 { 0.6
0.4 { 0.6
385
373
371
371
371
1.1 { 1.4
0.7 { 1.0
0.6 { 0.9
0.5 { 0.7
0.4 { 0.7
Serum electrolytes
({calcium)
1
2
3
4
5
369
354
352
350
350
0.6 { 0.9
0.4 { 0.7
0.3 { 0.6
0.2 { 0.5
0.2 { 0.5
367
352
352
349
349
0.6 { 1.0
0.4 { 0.8
0.3 { 0.6
0.2 { 0.5
0.2 { 0.5
371
358
356
354
354
0.7 { 1.1
0.5 { 0.9
0.4 { 0.7
0.3 { 0.6
0.3 { 0.6
Liver function
tests
1
2
3
4
5
382
368
368
365
367
0.7 { 1.1
0.5 { 0.8
0.4 { 0.7
0.4 { 0.6
0.4 { 0.6
377
366
366
363
365
0.8 { 1.2
0.5 { 0.8
0.5 { 0.7
0.4 { 0.6
0.4 { 0.6
381
370
367
366
366
0.9 { 1.3
0.7 { 1.0
0.6 { 0.8
0.5 { 0.7
0.4 { 0.7
Thyroid function
tests
1
2
3
4
5
381
365
361
360
359
0.6 { 0.8
0.4 { 0.6
0.3 { 0.6
0.3 { 0.5
0.2 { 0.5
376
360
357
356
355
0.6 { 0.8
0.4 { 0.6
0.3 { 0.6
0.3 { 0.5
0.3 { 0.5
378
364
360
359
358
0.7 { 0.8
0.5 { 0.7
0.4 { 0.6
0.3 { 0.6
0.3 { 0.5
Tumor marker
1
2
3
4
5
295
288
286
286
287
0.1 { 0.4
0.1 { 0.3
0.1 { 0.3
0.1 { 0.3
0.1 { 0.3
297
289
288
288
289
0.1 { 0.4
0.1 { 0.3
0.1 { 0.3
0.1 { 0.3
0.1 { 0.3
297
289
288
288
289
0.1 { 0.4
0.1 { 0.3
0.1 { 0.3
0.1 { 0.3
0.1 { 0.3
Chest X-ray
1
2
3
4
5
402
396
396
394
394
1.2 { 0.8
1.1 { 0.6
0.9 { 0.6
0.9 { 0.5
0.9 { 0.5
398
394
394
394
394
1.3 { 0.8
1.1 { 0.7
1.0 { 0.6
0.9 { 0.5
0.9 { 0.5
401
396
396
396
396
1.4 { 0.9
1.2 { 0.7
1.0 { 0.6
0.9 { 0.5
0.9 { 0.5
Head and neck
CT
1
2
3
4
5
369
353
353
350
350
0.3 { 0.5
0.1 { 0.4
0.1 { 0.3
0.0 { 0.2
0.0 { 0.2
365
352
353
350
349
0.3 { 0.6
0.2 { 0.4
0.1 { 0.3
0.1 { 0.2
0.0 { 0.2
372
357
356
353
352
0.4 { 0.6
0.2 { 0.5
0.2 { 0.4
0.1 { 0.3
0.1 { 0.3
Chest CT
1
2
3
4
5
363
351
349
349
349
0.1 { 0.3
0.0 { 0.2
0.0 { 0.1
0.0 { 0.1
0.0 { 0.1
359
350
348
348
348
0.1 { 0.4
0.1 { 0.3
0.0 { 0.2
0.0 { 0.1
0.0 { 0.1
361
348
348
348
347
0.2 { 0.4
0.1 { 0.3
0.1 { 0.3
0.0 { 0.2
0.0 { 0.2
MRI of head/neck
1
2
3
4
5
363
349
347
347
347
0.1 { 0.3
0.0 { 0.2
0.0 { 0.2
0.0 { 0.1
0.0 { 0.1
360
346
346
345
346
0.1 { 0.3
0.0 { 0.2
0.0 { 0.2
0.0 { 0.1
0.0 { 0.1
360
348
346
346
346
0.1 { 0.4
0.1 { 0.3
0.0 { 0.2
0.0 { 0.1
0.0 { 0.1
Modality
(continued)
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W: Cancer
1936
CANCER May 15, 1998 / Volume 82 / Number 10
TABLE 2 (continued)
Stage Ib
Stage II
Stage III/ (resectable) IV
Postop
year
No.a
Mean { SD
No.
Mean { SD
No.
Mean { SD
Sonogram of
head/neck
1
2
3
4
5
360
350
348
347
348
0.1 { 0.5
0.0 { 0.4
0.0 { 0.2
0.0 { 0.1
0.0 { 0.1
356
347
346
345
346
0.1 { 0.5
0.1 { 0.4
0.0 { 0.3
0.0 { 0.2
0.0 { 0.2
358
348
347
346
347
0.1 { 0.5
0.1 { 0.4
0.0 { 0.3
0.0 { 0.3
0.0 { 0.3
Bone scan
1
2
3
4
5
362
351
350
349
349
0.1 { 0.2
0.0 { 0.1
0.0 { 0.2
0.0 { 0.1
0.0 { 0.1
359
349
349
348
348
0.1 { 0.2
0.0 { 0.2
0.0 { 0.2
0.0 { 0.1
0.0 { 0.1
360
350
350
349
349
0.1 { 0.3
0.0 { 0.2
0.0 { 0.3
0.0 { 0.1
0.0 { 0.1
Bronchoscopy
1
2
3
4
5
367
355
353
351
349
0.2 { 0.5
0.1 { 0.3
0.0 { 0.2
0.0 { 0.2
0.0 { 0.2
362
350
349
347
346
0.2 { 0.5
0.1 { 0.3
0.1 { 0.3
0.0 { 0.2
0.0 { 0.2
363
352
351
349
348
0.2 { 0.5
0.1 { 0.4
0.1 { 0.3
0.0 { 0.2
0.0 { 0.2
Esophagoscopy
1
2
3
4
5
367
355
353
351
350
0.2 { 0.6
0.1 { 0.4
0.1 { 0.3
0.0 { 0.2
0.0 { 0.2
362
349
349
347
347
0.2 { 0.6
0.1 { 0.4
0.1 { 0.3
0.1 { 0.2
0.0 { 0.2
363
352
350
348
348
0.2 { 0.6
0.1 { 0.5
0.1 { 0.3
0.1 { 0.3
0.1 { 0.2
Modality
Postop: postoperative; SD: standard deviation; CT: computed tomography; MRI: magnetic resonance imaging.
a
Number of respondents per matrix cell.
b
Mean number of times the specified testing modality was requested during a given year postoperatively for a patient with a given TNM stage. During the first postoperative year after potentially curative surgery
for a hypothetical patient with Stage I epidermoid carcinoma of the upper aerodigestive tract, for example, the 402 respondents would order a chest X-ray 1.2 times, on average.
has been estimated at approximately 2 – 7% per year
and this risk,3,5 unlike the risk of recurrence, is not
known to vary by TNM stage of the index lesion. Other
serious diseases related to tobacco smoking also might
be detected in a rational surveillance scheme.
It is inevitable that the results of this survey will
be taken as de facto guidelines for current practice.
We discourage this, because our data supply no information on costs, benefits, and hazards of current practice. We also point out the wide variation among acknowledged experts.3
Two factors help insure that the results reported
herein are generalizable to the posttreatment surveillance of most patients with carcinoma of the UADT.
First, the majority of curative treatment of UADT carcinoma involves surgical extirpation, although there is
an upswing in nonsurgical therapy.20 Second, both
surveys document that surgeons usually follow their
patients postoperatively rather than referring them
elsewhere for follow-up. Assuming there is no major
difference in practice patterns between respondents
and nonrespondents to the surveys, the data obtained
in these surveys should serve as a solid proxy for the
follow-up received by the majority of UADT carcinoma
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patients undergoing potentially curative therapy in
North America.
For the purpose of proposing a randomized clinical trial, combined data from the SHNS and ASHNS
surveys were used to select two strategies: one more
intensive and one less intensive. Both are representative of the spectrum of current self-reported practice
among SHNS and ASHNS members (Table 3). A trial
based on these data should minimize the problem of
slow accrual because both follow-up arms are derived
from actual practice patterns. Such a trial should incorporate quality-of-life measurements as well as economic analyses. For each of the alternative strategies,
it would be possible to separately analyze efficiencies
of each modality in detecting recurrence of the index
lesion and new primary tumors, as well as other conditions of medical importance.
The costs of posttreatment cancer surveillance are
great enough to warrant formal study, particularly because current practices have not been proven to be
worthwhile. The tools to perform such a study are
available.19 The large costs of patient follow-up for all
varieties of cancer11 likely will not be sustainable in
an era of cost containment without well designed stud-
W: Cancer
Cancer Patient Follow-Up/Johnson et al.
TABLE 3
Potential Alternate Follow-Up Strategies Based on the Survey Results
2.
Follow-up
parameter
Postoperative
year
More intensive
strategya
Less intensive
strategya
3.
Office visit
1
2
3
4
5
12
6
4
4
4
6
3
2
2
2
4.
1
2
3
4
5
2
1
1
1
1
1
0
0
0
0
1
2
3
4
5
2
2
1
1
1
1
1
0
0
0
1
2
3
4
5
1
1
0
0
0
0
0
0
0
0
Blood testsb
Chest X-ray
CT of head and neck
5.
6.
7.
8.
9.
10.
CT: computed tomography.
a
Number of times each modality is requested, by postoperative year. No stratification according to
TNM stage, anatomic site, patient age, etc.
b
Complete blood count, Sequential Multiple Analysis of 20 serum chemical constituents, { serum
thyroid-stimulating hormone level.
11.
12.
ies to demonstrate the value of such an investment.
In studies of cancer screening in average risk or even
many high risk populations, cost-effectiveness is frustratingly difficult to demonstrate. Unfortunately, such
trials are quite expensive to mount. Detection of recurrent UADT carcinoma can lead to curative therapy.
Detecting such recurrences before they become symptomatic undoubtedly benefits a small number of patients, but the costs are high. National policymakers
and businessmen who are planning to manage health
care may soon require justification of the expense required to detect recurrences and proof that early detection will save lives at a cost that society is willing
to bear. If prompt treatment of UADT carcinoma recurrence or new primary tumors does save lives, then
a well controlled prospective study of alternative surveillance strategies will be needed to quantify the value
that is returned to society from this investment.
Welsh JD. Medical histories of Union generals. Kent, OH:
The Kent State University Press, 1996:138–40.
/ 7bc3$$1207
14.
15.
16.
17.
18.
19.
20.
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