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10.1245/ASO.2006.04.014
Annals of Surgical Oncology 13:1063-1071 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Geographical Variation in Surveillance Strategies After Curative-Intent Surgery for Upper Aerodigestive Tract Cancer

Frank E. Johnson, MD1,2, Michael H. Johnson, BS2, Marc F. Clemente, MD1,2, Randal C. Paniello, MD2,3 and Katherine S. Virgo, PhD1,2

1 Surgical Service, Veterans Affairs Medical Center, 915 North Grand Boulevard, St. Louis, Missouri 63106
2 Department of Surgery, Saint Louis University, St. Louis, Missouri
3 Department of Otolaryngology, Washington University, St. Louis, Missouri

Correspondence: Address correspondence and reprint requests to: Frank E. Johnson, MD, Saint Louis University Health Sciences Center, 3635 Vista Avenue at Grand Boulevard, St. Louis, MO 63110-0250, USA; E-mail: frank.johnson{at}med.va.gov.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Analysis of geographical variation in utilization of medical resources is often used to identify regions of overutilization or underutilization.

Methods: We surveyed the membership of the American Head and Neck Society regarding their recommended frequency of office visits and 13 imaging studies and blood tests for their patients after potentially curative therapy for upper aerodigestive tract cancers.

Results: Of the 1322 members surveyed, 610 (46%) responded: 420 responses (32%) were assessable. Responses were compared by US Census Region, Metropolitan Statistical Area, and managed care organization penetration rate. Overseas members (16% of assessable responses) comprised a separate category for the regional analysis. There were statistically significant variations in practice patterns among Census Regions for office visits, complete blood count, computed tomography of the head, sonography, and esophagoscopy. Non-US members recommended significantly more blood tests, imaging studies, and endoscopy than US members for routine cancer surveillance. Only the frequency of office visits differed significantly among Metropolitan Statistical Areas. Surprisingly, the penetration rate of managed care organizations had no significant effect on posttreatment surveillance intensity.

Conclusions: This analysis indicates that only a small portion of the wide variation in observed follow-up practice patterns can be explained by geographical determinants.

Key Words: Follow-up • Head and neck cancer • Geographical variation • Small-area analysis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Most surgeons follow up their cancer patients after treatment by using a variety of modalities, including office examinations, imaging studies, and blood tests. Many reasons are cited for performing such follow-up studies, but the major rationale is a desire to detect the recurrence of the index cancer or a second primary tumor.1,2 The frequency of use of these various modalities varies among surgeons, as shown in previous reports;1,3 such variation also has cost implications.4,5

There is no generally agreed-upon strategy for following up upper aerodigestive tract (UADT) cancer patients, but practice guidelines were published in 1996 by a Task Force of the American Head and Neck Society (AHNS).6 In a survey of surgeons who operate on UADT cancer patients and also follow them up, we found marked variation in the intensity of follow-up.1,3 The variation could not be attributed to surgeon age,7 tumor stage,8 or primary surgical specialty.3

Geographical variation in the utilization of medical services is often analyzed to determine whether overutilization or underutilization exists. In theory, geographical variation may be related to regional differences in training or to variation in the availability of certain services (e.g., expensive imaging devices). Such variation may also contribute to differences in the regional standards of care. Prior studies evaluating geographical variation in follow-up after treatment for cancer of the colon,9 lung,10 and prostate11 found little significant variability.

The goal of this study was to determine whether there is significant variation in the intensity of follow-up strategies among UADT cancer surgeons across US Census Regions or Metropolitan Statistical Areas (MSAs), by using our previously reported survey instrument.1 We also estimated whether the penetration rate of managed care organizations (MCOs), which is known to vary among geographical regions, would affect posttreatment follow-up of UADT cancer patients. MCOs are widely assumed to favor minimalist policies in allocation of resources because of their for-profit nature.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Custom-designed surveys were mailed to members of the American Society for Head and Neck Surgery and to members of the Society of Head and Neck Surgeons. These two societies have since merged and now comprise the AHNS. The three-page survey asked each surgeon to indicate how frequently he or she performed office examinations and 13 other examinations and blood tests during each of the first 5 years after surgery for UADT cancer. A second survey was mailed to nonrespondents 1 month later. The survey instrument has been previously published in its entirety.1

The imaging modalities included in the survey were chest radiograph (CXR), computed tomography (CT) of the head and neck, CT of the chest, magnetic resonance imaging (MRI) of the head and neck, ultrasonography of the head and neck, and bone scan. The blood tests included complete blood count (CBC), liver function tests (LFTs), thyroid function tests (TFTs), serum electrolyte (± calcium) levels, and specific tumor markers. Other examinations included esophagoscopy and bronchoscopy.

Surveys were excluded if the surgeon reported being retired, not performing head and neck surgery, or not performing follow-up. Respondents were assigned to an MSA and a US Census Region (Fig. 1Go) according to their society membership address.12 Responses from AHNS members from outside the United States constituted a 10th region. Respondents from Puerto Rico were grouped in the South Atlantic region.


Figure 1
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  		FIG. 1. Map of the United States showing the nine US Census Regions and divisions.

 
Finally, MCO penetration rate data were added to the database. On the basis of a frequency analysis of MCO penetration rates by state, a categorical variable was created that corresponded to penetration rate quartiles of 0% to 10%, 11% to 20%, 21% to 30%, and 31% to 100%. Quartiles were divided in this fashion so that each included an equal number of respondents. For the MSA and MCO penetration rate analyses, foreign respondents were excluded because of a lack of MSA data and nonapplicability of the MCO penetration rate concept to foreign responses.

Responses were subdivided into three tumor-node-metastasis stage groups (I, II, and III plus resectable IV) corresponding to the three vignettes on the questionnaire. Data were requested for the first 5 years after potentially curative treatment for squamous cell UADT carcinoma. The completed surveys were entered into a computerized database and analyzed with SPSS (SPSS Inc, Chicago, IL). Because many advanced statistical methods require independence of observations, correlation analysis was used to determine whether an individual’s response for year 1 for a particular follow-up modality was independent of the response given for year 2 for that same modality. Similarly, correlation analysis was used to determine whether an individual’s response for tumor-node-metastasis stage I was independent of the response given for tumor-node-metastasis stage II for that same modality. Previous analyses for other cancer sites have shown that observations from the same subject generally are not independent. Thus, repeated-measures analysis of variance (ANOVA) was chosen as the method of analysis to compare practice patterns by Census Region, MSA, and MCO penetration rate.13 Statistical significance was set at P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The 1322 AHNS members surveyed returned 610 surveys (46%), of which 420 (32%) were assessable. The demographic data on assessable respondents were generally similar to those of nonassessable respondents.

Correlation analysis revealed that the mean frequency of use of most follow-up modalities was highly correlated (correlation coefficient >.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 was also highly correlated with that selected for year 3, and so on. Because observations from the same subject were not independent, repeated-measures ANOVA was the appropriate method of analysis, as predicted. Repeated-measures ANOVA was performed on the data to compare means for each testing modality by Census Region, MSA, and MCO penetration rate, controlling for stage and year after surgery. All possible interactions were also examined.

Repeated-Measures ANOVA: Census Region
Tables 1Go and 2Go list the means and standard deviations for the testing modalities by Census Region for a patient with tumor-node-metastasis stage I UADT cancer for year 1 only. Data for years 2 to 5 and for patients with more advanced UADT cancer were similar but are not shown. There were significant main effects of Census Region for five of the follow-up modalities (office visits, CBC, CT of the head, sonography, and esophagoscopy).


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  		TABLE 1. Frequency of test utilization by US Census Region in postoperative year 1 after potentially curative resection of UADT cancer (n = 420)a
 

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  		TABLE 2. Frequency of test utilization by US Census Region in postoperative year 1 after potentially curative resection of UADT cancer (n = 420)a
 
As expected, although they are not listed in Tables 1Go and 2Go, there were significant main effects of tumor-node-metastasis stage and year after surgery for most modalities. The exceptions for stage were sonography, tumor markers, and bone scan. For CBC, LFTs, and serum electrolyte levels, years 4 and 5 after surgery were grouped because of the presence of linear dependency among error terms. For the same reason, years 3 to 5 after surgery were combined for CT of the chest, and years 1 to 2 and years 3 to 5 after surgery were combined for bone scan, MRI, sonography, and bronchoscopy. For tumor markers, grouping of both years after surgery and stage was required (years 1 to 2 and years 3 to 5 after surgery were grouped, and tumor-node-metastasis stages II to III were combined).

There was only one follow-up modality (sonography) for which a significant two-way interaction between Census Region and stage existed. The two-way interaction between Census Region and years after surgery was significant for office visits, CBC, LFTs, serum electrolyte levels, CXR, CT of the head, and sonography. The two-way interaction between stage and years after surgery was frequently significant (office visits, TFTs, CXR, CT of the chest, CT of the head, MRI, and bone scan). There were no significant three-way interactions among region, stage, and years.

Repeated-Measures ANOVA: MSA
Tables 3Go through 5GoGo list the means and standard deviations for the testing modalities by MSA for a patient with tumor-node-metastasis stage I UADT cancer for year 1 only. Data for years 2 to 5 and for patients with more advanced UADT cancer were similar but are not shown. Only five MSAs (Chicago, Houston, Philadelphia, Pittsburgh, and New York) had a sufficient number of respondents to analyze separately and thus were not grouped into "other MSA." "Non-MSA" represents those in rural areas. There were no significant main effects of MSA for any follow-up modality except office visit (P < .05).


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  		TABLE 3. Frequency of test utilization by Metropolitan Statistical Area (MSA) in postoperative year 1 after potentially curative resection of UADT cancer: most frequently utilized tests (n = 352)a
 

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  		TABLE 4. Frequency of test utilization by Metropolitan Statistical Area (MSA) in postoperative year 1 after potentially curative resection of UADT cancer: less frequently utilized tests (n = 352)a
 

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  		TABLE 5. Frequency of test utilization by Metropolitan Statistical Area (MSA) in postoperative year 1 after potentially curative resection of UADT cancer: less frequently utilized tests (n = 352)a
 
As expected, there were significant main effects of stage and years after surgery for most modalities. The exceptions for stage were sonography, bronchoscopy, esophagoscopy, tumor markers, and bone scan. The exceptions for years after surgery were sonography, tumor markers, and bone scan. For CBC, LFTs, and esophagoscopy, years 4 and 5 after surgery were grouped because of the presence of linear dependency among error terms. For the same reason, years 3 to 5 after surgery were combined for serum electrolyte levels, and years 1 to 2 and years 3 to 5 after surgery were combined for CT of the chest, MRI, sonography, and bronchoscopy. For tumor markers and bone scan, grouping of both years after surgery and stage was required (years 1 to 2 and years 3 to 5 after surgery were grouped, and tumor-node-metastasis stages II to III were combined).

Significant two-way interactions involving MSA were infrequent. The two-way interaction between MSA and stage was significant only for CBC and sonography. The two-way interaction between MSA and years after surgery was significant for serum electrolyte levels. Two-way interactions between stage and years after surgery were significant for office visits, CT of the chest, CT of the head, MRI, bronchoscopy, and TFTs. Significant three-way interactions among MSA, stage, and years after surgery were rare (CBC, sonography, TFTs, and serum electrolyte levels).

Repeated-Measures ANOVA: MCO Penetration Rates
Tables 6Go through 8GoGo list the means and standard deviations for the testing modalities by MCO penetration rate for a patient with tumor-node-metastasis stage I UADT cancer for year 1 only. Data for years 2 to 5 and for patients with more advanced UADT cancer were similar but are not shown. There were no significant main effects of MCO penetration rate for any follow-up modality.


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  		TABLE 6. Frequency of test utilization by managed care organization (MCO) penetration rate in postoperative year 1 after potentially curative resection for UADT cancer: most frequently utilized tests (n = 352)a
 

View this table:
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  		TABLE 7. Frequency of test utilization by managed care organization (MCO) penetration rate in postoperative year 1 after potentially curative resection for UADT cancer: less frequently utilized tests (n = 352)a
 

View this table:
[in this window]
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  		TABLE 8. Frequency of test utilization by managed care organization (MCO) penetration rate in postoperative year 1 after potentially curative resection for UADT cancer: less frequently utilized tests (n = 352)a
 
As expected, there were significant main effects of stage and years after surgery for most modalities. The exceptions for years after surgery were sonography, tumor markers, and bone scan. For CBC and LFTs, years 4 and 5 after surgery were grouped because of the presence of linear dependency among error terms. For the same reason, years 3 to 5 after surgery were combined for serum electrolyte levels. Years 1 to 2 and years 3 to 5 after surgery were combined for CT of the chest, MRI, bronchoscopy, and esophagoscopy. For sonography, tumor markers, and bone scan, grouping of both years after surgery and stage was required (years 1–2 and years 3–5 after surgery were grouped, and tumor-node-metastasis stages II to III were combined).

Significant two-way interactions involving MCO penetration rates were infrequent. There were no significant two-way interactions between MCO penetration rate and stage. The two-way interaction between MCO penetration rate and years after surgery was significant only for CBC. The two-way interaction between stage and years after surgery was frequently significant (office visits, TFTs, CXR, CT of the chest, CT of the head, MRI, and bronchoscopy). There were no significant three-way interactions among MCO penetration rates, stage, and years after surgery.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The optimal surveillance strategy for UADT patients who have undergone potentially curative resection is not known, and the management of such patients varies widely among practitioners.1,3,7,8 Much of the variation among physicians in delivery of medical care is ascribable to the poor quality of available evidence concerning efficacy, effectiveness, and efficiency of the intervention under consideration.14,15 We believe that this is the most likely explanation for the diverse surveillance strategies documented in our survey.1,3 Overuse, underuse, and misuse of medical interventions have been identified by the Institute of Medicine of the National Academy of Sciences as a large, expensive problem.16 The presence of considerable variation in a particular medical practice suggests that some medical decisions are inappropriate. From time to time these analyses attract attention in the popular press.17 Identifying the causes can benefit society by providing opportunities to avoid wasting scarce resources (when the cost of a medical practice is too high to warrant its use) and opportunities to improve health (when the benefits of a medical practice are high enough to justify its expense). In UADT cancer care, the economic implications of follow-up programs are large because of the size of the patient population.18

This study suggests that geographical factors account for some, but not most, of the variation in the use of surveillance methods after primary treatment. The analysis has several limitations. Surveys provide information at just one point in time that may be difficult to interpret in light of a constantly changing medical environment.19 The number of respondents per MSA was consistently small (only five MSAs had enough respondents for analysis without grouping in this study) and may be biased toward the point of view of a single, large medical center in a particular MSA. Furthermore, by using MSA as one of the geographical units of analysis, it is assumed that physicians treat only patients from the MSA in which their office is located and that there is little crossover among MSAs. This assumption affects principally our MSA analysis and was considered reasonable because most of our respondents were in either the "other MSA" or "non-MSA" categories and the amount of crossover would need to be large to distort the results appreciably.

Despite these limitations, the current analysis is the first to directly estimate the effect of the practicing surgeons’ geographical location on the intensity of testing after curative surgery. Some tests were used more commonly by foreign respondents, as shown by the Census Region analysis. The small number of foreign respondents per country and even per continent precluded further analysis.

Local professional groups and opinion leaders are important in determining treatment and surveillance strategies,20,21 especially in small or rural areas. However, large metropolitan areas are not exempt because of the presence of large cancer centers and the homogenization of practice patterns that tends to occur within these centers. The observed variation may also be due to other independent factors (types of health care systems, health-related behaviors, cultural factors such as patient expectations and lifestyles, and so on), particularly among non-US countries.22

For some surgical procedures, the presence of small-area variation determines the likelihood that a patient will receive surgery.23–25 Physicians’ attitudes may also affect testing intensity, and differences in physicians’ attitudes may explain the geographical variation identified. Coyte et al.26 recently reviewed the effect of small-area variation in rates of myringotomy with insertion of tympanostomy tubes by surveying otolaryngologists and primary care physicians. They found substantial variation in surgical practice and showed that the opinions of primary care physicians were the dominant determinant. In contrast, the opinions of the surgeons, rather than referring physicians, predicted rates of surgery. Such studies suggest that reducing variation by educating physicians whose practice patterns vary substantially from evidence-based guidelines may be worthwhile.

This study evaluated variation in testing by MCO penetration rate. Our findings do not support the suggestion that MCOs foster a minimalist approach to surveillance practices. A similar study of prostate cancer patient follow-up suggested that increasing the MCO penetration rate did not lead to decreased posttreatment surveillance.27 How the intensity of posttreatment follow-up affects quality of life and life expectancy is unknown for most cancers. Breast cancer patient follow-up intensity, however, does not seem to affect either duration of survival or quality of life.28

Our survey neither considered how physicians act on tests obtained nor addressed whether the test-ordering pattern affects patient outcomes. Clearly, many patients with UADT carcinoma undergo excision by general surgeons, otolaryngologists, surgical oncologists, plastic surgeons, and others who were not surveyed. Follow-up after resection is often delegated to medical oncologists, family practitioners, or others. Their strategies may differ from those described here. Cooper et al.29 addressed the issue of geographical variation and patient outcomes in a recent review of follow-up testing after surgery for nonmetastatic colorectal carcinoma. Many of the differences they observed in testing frequency were explained by clinical criteria, but considerable variation in the use of surveillance procedures was found across the nine US Census Regions. Nevertheless, there were no differences in all-cause or disease-specific death rates. Studies of geographical variation in the rates of coronary artery bypass grafting30 and breast-conserving surgery31 have revealed differences, but the effect of these differences on clinical results is very difficult to assess.

Several practice guidelines are available for cancer patient follow-up, but they are based on weak evidence developed by informal consensus or by assessing expert opinions and recommendations. Although randomized clinical trials do not necessarily lead to rapid or appropriate changes in clinical practice,20,21,32 the development of evidence-based guidelines would likely limit inappropriate medical tests, reduce variation in practice patterns among physicians, minimize cost, and result in better patient care. However, in the absence of well-publicized evidence from high-quality clinical trials, uniformity in the postoperative care of UADT cancer patients will prove difficult to achieve.

In conclusion, UADT cancer remains common in the United States. It is typically a disease of middle age that is often curable but has a significant risk for recurrence. Follow-up regimens that are both cost-effective and timely are required, but the evidence to date suggests that considerable variation exists in surveillance intensity. This analysis indicates that geographical determinants such as MSA and region do account for a small but significant portion of the variability in physician surveillance. A likely reason for the variability is the low quality of evidence supporting any specific strategy. Prospective trials are needed to clearly delineate the most appropriate method for follow-up. The Institute of Medicine of the National Academy of Sciences has endorsed this view and recommended that the U.S. Congress should provide sufficient support to the U.S. Department of Health and Human Services for the U.S. Preventive Services Task Force and the U.S. Task Force on Community Preventive Services to conduct timely assessments of the benefits, harms and costs associated with screening tests and other preventive interventions.33

Received for publication April 13, 2005. Accepted for publication December 22, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Johnson FE, Johnson MH, Virgo KS. Current follow-up strategies after potentially curative resection of upper aerodigestive tract epidermoid carcinoma: results of a survey of members of the Society of Head and Neck Surgeons. Int J Oncol 1997; 10:927–31.
  2. de Visscher AVM, Mani JJ. Routine long-term follow-up in patients treated with curative intent for squamous cell carcinoma of the larynx, pharynx, and oral cavity: does it make sense? Arch Otolaryngol Head Neck Surg 1994; 120: 934–9.[Abstract]
  3. Paniello RC, Virgo KS, Johnson MH, Clemente MF, Johnson FE. Practice patterns and clinical guidelines for posttreatment follow-up of head and neck cancers: a comparison of two professional societies. Arch Otolaryngol Head Neck Surg 1999; 125:309–13.[Abstract/Free Full Text]
  4. Virgo KS, Paniello RC, Johnson FE. Costs of posttreatment surveillance for patients with upper aerodigestive tract cancer. Arch Otolaryngol Head Neck Surg 1998; 124:564–72.[Abstract/Free Full Text]
  5. Welch WP, Miller ME, Welch HG, Fisher ES, Wennberg JE. Geographic variation in expenditures for physicians’ services in the United States. N Engl J Med 1993; 328:621–7.[Abstract/Free Full Text]
  6. American Society for Head and Neck Surgery, Society of Head and Neck Surgeons. Clinical Practice Guidelines for the Diagnosis and Management of Cancer of the Head and Neck. Pittsburgh, PA (ASHNS), and Arlington, VA (SHNS), 1996.
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  9. Johnson FE, McKirgan LW, Coplin MA, et al. Geographic variation in patient surveillance after colon cancer surgery. J Clin Oncol 1996; 14:183–7.[Abstract]
  10. Johnson FE, Naunheim KS, Coplin MA, Virgo KS. Geographic variation in the conduct of patient surveillance after lung cancer surgery. J Clin Oncol 1996; 14:2940–9.[Abstract]
  11. Powell TM, Thompsen JP, Virgo KS, et al. Geographic variation in patient surveillance after radical prostatectomy. Ann Surg Oncol 2000; 7:339–45.[Abstract/Free Full Text]
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  26. Coyte PC, Croxford R, Asche CV, To T, Feldman W, Friedberg J. Physician and population determinants of rates of middle-ear surgery in Ontario. JAMA 2001; 286:2128–35.[Abstract/Free Full Text]
  27. Powell TM, Thompsen JP, Virgo KS, et al. Geographic variation in patient surveillance after radical prostatectomy. Ann Surg Oncol 2000; 7:339–45.[Abstract/Free Full Text]
  28. The GIVIO Investigators. Impact of follow-up testing on survival and health-related quality of life in breast cancer patients: a multicenter randomized controlled trial. JAMA 1994; 271:1587–92.[Abstract]
  29. Cooper GS, Yuan Z, Chak A, Rimm AA. Geographic and patient variation among Medicare beneficiaries in the use of follow-up testing after surgery for nonmetastatic colorectal carcinoma. Cancer 1999; 85:2124–31.[CrossRef][Medline]
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  31. Nattinger AB, Gottlieb MS, Veum J, Yahnke D, Goodwin JS. Geographic variation in the use of breast-conserving treatment for breast cancer. N Engl J Med 1992; 326:1102–7.[Abstract]
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