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Use of Hematopoietic Colony-Stimulating Factors: Comparison of the 1994 and 1997 American Society of Clinical Oncology Surveys Regarding ASCO Clinical Practice Guidelines

From the Health Services Research Committee, American Society of Clinical Oncology, Alexandria, VA.

Address reprint requests to Thomas J. Smith, MD, Massey Cancer Center, Virginia Commonwealth University, 401 College Street, Richmond, VA 23290-0037; email tsmith{at}gems.vcu.edu

ABSTRACT

PURPOSE: The American Society of Clinical Oncology (ASCO) Health Services Research Committee sought to assess whether more appropriate patterns of colony-stimulating factor (CSF) use occurred after the publication of ASCO evidence-based practice guidelines in 1994 and 1996 for patients with solid tumors or lymphoma.

METHODS: In 1994 and 1997, questionnaires describing clinical scenarios were mailed to ASCO members who practiced medical oncology. Physicians were asked the extent to which they preferred to use a CSF for primary prophylaxis, secondary prophylaxis, or treatment of neutropenic complications. Multiple regression analyses were used to determine predictors of overall propensity to use CSFs and, when using a CSF, propensity to support longer schedules of CSF use.

RESULTS: Decreased use of CSFs was shown in the following situations: (1) treatment for febrile neutropenia without localizing signs (39% in 1994 v 29% in 1997) or with a right lower lobe infiltrate (54% v 46%); (2) primary prophylaxis with paclitaxel for ovarian cancer (20% v 11%) or cyclophosphamide, doxorubicin, and vincristine chemotherapy for small-cell lung cancer (8.4% v 4.6%); and (3) secondary prophylaxis after afebrile neutropenia following chemotherapy for germ cell tumors (44.5% v 36.0%). One third fewer physicians supported the extended use of CSFs until an absolute neutrophil count 10,000/mm³ or a WBC count 10,000/mm³ was reached, both counts serving as criteria for stopping CSF therapy. However, we observed high rates of CSF use despite ASCO guideline recommendations against use in the following clinical situations: (1) primary prophylaxis in patients at low risk of febrile neutropenia (6% v 16%); (2) secondary prophylaxis late in the course of curative and palliative therapy (80% v 53%); and (3) treatment of afebrile and uncomplicated febrile neutropenia (30% v 60%). In 1994 and 1997, fee-for-service physicians were more likely than other physicians to prefer use of CSF support while maintaining treatment dose and schedule instead of using dose-reduction strategies, and, when using a CSF, they were more likely to support longer CSF treatment schedules (P < .05 for both scenarios).

CONCLUSION: Decreased use and more appropriate use of CSFs in accordance with ASCO guideline recommendations occurred from 1994 to 1997, but there remain many opportunities to reduce CSF use with no clinical harm. Many oncologists continue to support the use of CSFs in scenarios and with scheduling criteria that the guidelines and evidence do not support. ASCO's evidence-based guidelines should be linked with formal continuous quality improvement initiatives to substantially improve the quality of supportive oncology care.

The hematopoietic colony stimulating factors (CSFs), granulocyte colony-stimulating factor (G-CSF) and granulocyte-macrophage colony stimulating factor (GM-CSF), decrease the likelihood of neutropenic complications that result from chemotherapy, but their high cost and limited clinical influence led to concern about their appropriate use. In 1994, the American Society of Clinical Oncology (ASCO) surveyed physicians regarding their preferences about the use of CSFs and shortly thereafter published evidence-based, clinical practice guidelines for the use of CSFs.¹ Updated guidelines published in 1996 did not include any change in recommendations for the use of CSFs for patients who receive standard doses of chemotherapy.² The guidelines supported CSF use for only a limited number of clinical situations, including primary prophylaxis of febrile neutropenia (CSF given after the completion of the chemotherapy cycle and before neutropenia is documented) when the expected incidence is greater than 40%; secondary prophylaxis (CSF given in later cycles after febrile neutropenia in a prior cycle has been documented) to maintain dose intensity when dose reduction is not appropriate; and as treatment (CSF given at the time of diagnosis of afebrile or febrile neutropenia) with antibiotics only for patients at high risk of septic complications.

The 1994 survey of ASCO physicians performed before the publication of the initial CSF guidelines found that the majority of physicians supported patterns of use that were similar to those recommended in the subsequently published ASCO guidelines.³ However, overuse of CSFs appeared to be a problem in some situations. For example, more than half of the physicians chose to use CSFs in the treatment of uncomplicated febrile neutropenia, a condition for which CSF use was not supported by the evidence presented in the ASCO guidelines. The survey responses also showed some large variations, with physicians at academic medical centers and in health maintenance organization (HMO) practices more likely to prefer dose-reduction strategies, whereas fee-for-service physicians preferred the addition of CSFs. In 1997, the ASCO Health Services Committee surveyed random ASCO members to assess changes in patterns of CSF use that occurred after the publication of the ASCO guidelines.

METHODS

A random sample of 1,500 US physicians was selected from the ASCO membership list. Because physician identity was not included in the survey reply forms, it is not possible to know whether any physician participated in both surveys. The same firm that performed the earlier ASCO survey conducted the 1997 survey. Surveys were mailed to the members in early 1997. Subjects who failed to respond to the first mailing were sent a second mailing. Those who did not respond to either mailing were telephoned as a reminder; up to seven attempts were made to reach physicians. Subjects who described themselves as radiation or surgical oncologists were considered ineligible and were excluded from the calculation of the response rate and the analysis. The survey instructed potential respondents who spent fewer than 5 hours per week in clinical practice to return the questionnaire unanswered.

Survey
The 1997 survey was essentially unchanged from the 1994 survey, except for the addition of scenarios related to the use of CSFs for elderly patients with acute myelogenous leukemia. (Data regarding this method of treatment will be reported separately.) The survey solicited data on respondents' patterns of growth factor use by use of hypothetical clinical scenarios. These scenarios fell into three basic categories: (1)primary prophylaxis, (2) secondary prophylaxis, and (3) therapy. The survey also included questions regarding the frequency of CSF use, preferences for use of G-CSF versus GM-CSF, criteria for stopping CSF treatment, impact of reimbursement considerations on the use and choice of CSFs, existence of institutional guidelines on CSF use, and respondent sociodemographics, including specialty (oncology, hematology, or hematology/oncology), year of medical school graduation, practice setting (fee-for-service, HMO, or academic), number of years in practice (< 3 years or not), and average weekly new cancer patient volume (> 5 cancer patients or not).

Statistical Methods
Differences in respondent characteristics between the 1994 and 1997 surveys and changes in propensity to prescribe CSF for each scenario were evaluated by comparing the distribution of the responses in the 1994 survey to the responses in the 1997 survey, using the chi-square test. A P value of .05 for statistical significance was established beforehand; no adjustment was made for the number of statistical comparisons.

To characterize an overall propensity to prescribe CSFs for all respondents across all survey items, Likert-scale CSF use-rate categories were assigned to responses for each of the multiple-choice survey items. A one-to-five coding of responses (never, rarely, sometimes, mostly, and always) was performed on the basis of each respondent's willingness to indicate CSF use for each scenario. Cronbach's alpha coefficient was computed to test the internal consistency of the scale items. The simple ordered utilization score was computed across all scenarios. Higher utilization scores indicated a tendency to be a higher CSF user, whereas lower utilization scores indicated a tendency to be a low user. Mean differences in overall utilization propensity scores between 1994 and 1997 were compared by use of the t test.

In addition, a multivariate regression model was used to predict overall utilization propensity, and for conditions in which CSF use would be preferred, a second (logistic) regression model was used to predict propensity to use longer schedules of CSFs (defined as the use of CSFs for more than 10 days or a CSF treatment–cessation criterion of an absolute neutrophil count (ANC) of 10,000 cells/mm³ and/or a WBC count of 10,000 or more cells/mm³), with dependent variables including practice setting (academic, HMO, or fee-for-service), medical school graduation year (before 1970 or not), formal CSF guidelines in their practice setting (yes or no), new patient volume (an average of six or more new cancer patients per week or not), CSF patient volume (use of CSFs for six or more patients per week), primary specialty (hematology, oncology, or hematology/oncology), and year of response to survey (1994 or 1997).

RESULTS

Demographic and practice characteristics of ASCO respondents for the 1994 and 1997 surveys are listed in Table 1. The response rate of 49.4% for the 1994 survey increased to 60.2% for the 1997 survey. The distribution of practice settings of the respondents was similar for the two surveys, with over half of the respondents in fee-for-service settings, approximately one third in academic practices, and between 10% and 15% in HMO practices (Table 1). The distribution of the year of graduation was also similar, with 22% of the respondents in both surveys having graduated before 1970. Less than one quarter of the respondents in both surveys worked with formal CSF guidelines or in practice settings where guidelines were perceived to influence practice. The 1997 respondents were more likely to provide care for more than five new cancer patients per week (68.0% for the 1997 survey respondents v 62.2% for the 1994 respondents; P < .04) and were more likely to have a specialty of hematology/oncology (56.3% v 47.0%; P = .002). CSFs were used in fewer than five patients per week by three quarters of the physicians in both surveys.

Physicians who responded in 1997 had a lower propensity to use CSFs than did those from 1994 (P < 0.001). Those in a fee-for-service setting (P < .001) and those who graduated from medical school before 1970 (P = .004) had a higher propensity to use CSFs. Factors associated with a lower propensity to use long schedules of CSFs included 1997 response (P > .001), not having CSF use or practice guidelines in the practice setting (P = .04), and being in an academic or HMO practice (P = .05).

General Patterns of Use
Regardless of the criterion used, the 1997 respondents' threshold for discontinuing CSFs was one third lower than that for respondents in 1994 (Table 2). Only 15.9% of the 1997 cohort supported the Food and Drug Administration–approved criterion of discontinuing CSFs when an ANC of more than 10,000/mm³ was reached, compared with 22.1% in 1994 (P for trend < .05). Similarly, in 1997, only 33.9% of respondents supported discontinuation of CSFs when a WBC of more than 10,000 cells/mm³ was reached, compared with 46.1% in 1994 (P for trend < .05). Of those who identified a "days of therapy" criterion for discontinuing CSFs, 35.2% opted for 8 days or fewer in 1997, compared with 25.9% in 1994 (P for trend < .05). These changes are compatible with the ASCO guideline recommendation that "a shorter duration of administration (than specified in the package insert) that is sufficient to achieve a clinically adequate neutrophil recovery is a reasonable alternative. . . ."

The ASCO guidelines offered no recommendation regarding the comparative clinical activity of G-CSF and GM-CSF. Although G-CSF was preferred to GM-CSF by over 80% of respondents in both surveys, support for GM-CSF over G-CSF increased from 1.7% in 1994 to 4.0% in 1997 (P = .05). Reimbursement considerations were less important in 1997. Only 20.9% of respondents indicated that choice of a particular CSF was dependent on prior experiences with denial of reimbursement (decreased from 27.8% in 1994; P < .005), and only 23.9% reported that their decisions about whether to use CSFs at all were influenced by anticipated denial of reimbursement (decreased from 34.7% in 1994; P < .005).

Primary Prophylaxis
Rates of CSF use in the absence of any prior neutropenia were significantly lower in 1997 in three of four scenarios (Table 3). This change is in the direction recommended by the guidelines, which stated that "primary administration of CSFs be reserved for patients (with) . . . an expected incidence of (febrile neutropenia) 40%." However, 5.8% (for the scenario of adjuvant cyclophosphamide, doxorubicin, and fluorouracil treatment for breast cancer) to 15.8% (for the scenario of cyclophosphamide, doxorubicin, and vincristine treatment for small-cell lung cancer) of respondents reported that they would "always, usually, or sometimes" use a CSF in the three scenarios in which rates of febrile neutropenia well below 40% would be expected. In the one scenario in which higher rates of febrile neutropenia might occur (paclitaxel treatment for metastatic ovarian cancer), the proportion who would "always, usually, or sometimes" use a CSF also declined, from 53.5% to 38.7% (P < .05).

Secondary Prophylaxis
As noted in Table 4, 44.5% of 1994 respondents reported they would use a CSF as secondary prophylaxis for an afebrile neutropenic patient receiving chemotherapy for testicular cancer. Regarding this use of CSFs, there was a significant reduction to 35.7% in 1997 (P < .05). These responses are not consistent with the guideline, which states that ". . . intervention with a CSF in afebrile neutropenic patients is not recommended."

There was even more support for CSF use for secondary prophylaxis of febrile neutropenia, especially for patients with curable diseases, with no statistically significant differences between 1994 and 1997. In the cycle after an episode of febrile neutropenia, 88.8% and 80.4% of respondents (1994 and 1997, respectively) would add a CSF to the same dose of chemotherapy in early and late cycles of cyclophosphamide, doxorubicin, vincristine, and prednisone treatment for non-Hodgkin's lymphoma (Table 4). Fifty-three percent of respondents would use a CSF to maintain doses of chemotherapy, and 14.0% would use a CSF in conjunction with a dose reduction for secondary prophylaxis in palliative chemotherapy for small-cell lung cancer. It is difficult to determine whether such uses of CSFs adhere to the guideline because the guideline did not clearly recommend either dose reduction or use of CSFs. However, the high rates of use do not seem consistent with the intent of the recommendation because no clinical benefit has been found from the small increase in dose intensity possible with CSFs.^4,5

Treatment of Neutropenia
As listed in Table 5, 30% of all respondents indicated that they would use CSFs to treat afebrile neutropenia "always, usually, or sometimes," a rate unchanged from 1994. These responses are not consistent with the guideline, which states that ". . . intervention with a CSF in afebrile neutropenic patients is not recommended."

The rate of using a CSF for treatment of uncomplicated febrile neutropenia "always, usually, or sometimes" was even higher at 60.5% but had declined from 73.4% in 1994 (P < .05). This change is in the direction supported by the guidelines, which stated that ". . . for the majority of patients with febrile neutropenia, the available data do not clearly support the routine initiation of CSFs. . . ." The guidelines indicated that this use "may be reasonable in patients with prognostic factors that are predictive of clinical deterioration such as pneumonia, hypotension, multiorgan dysfunction . . . or fungal infection." The proportion of survey respondents who reported that they would use a CSF in the scenario that described a patient with febrile neutropenia and a right lower lobe infiltrate "always, usually, or sometimes" was 79.9%, a decrease from 84.4% in 1994 (P < .05).

Utilization Scores by Practice Setting
The Cronbrach's alpha coefficient for the 11-item utilization scale was 0.80. Overall, the preference for CSF use was lower in 1997, with an overall mean utilization score of 30.4% (standard deviation, 6.1) in 1997 versus 32.2% (standard deviation, 6.2) in 1994 (P < .05). Significant predictors of lower propensity to use CSFs were responding to the 1997 survey versus the 1994 survey (P < .001), not being in a fee-for-service setting (P < .001), and having graduated medical school after 1970 (P = .004). In addition, use of a logistic regression model showed that in settings where CSFs would be used, three factors were significantly associated with a lower likelihood of using long CSF schedules: not being in a fee-for-service setting (odds ratio, 0.69; P = .05), not having a CSF guideline in the practice setting (odds ratio, 0.73; P = .04), and responding in 1997 and not in 1994 (odds ratio, 0.85; P < .001).

DISCUSSION

The main objective of evidence-based guidelines is to reduce the inappropriate use of scarce medical resources while providing support for appropriate use.⁶ On the basis of results from surveys conducted before and after the dissemination of ASCO CSF guidelines, we found evidence for both decreased use and more appropriate use of CSFs since the publication of the guidelines. In particular, the survey results indicated that there was a significant decrease in support for the use of CSFs in the 11 clinical settings that encompassed primary prophylaxis (four scenarios), secondary prophylaxis (four scenarios), and treatment of febrile neutropenia (three scenarios). There was also a small but significant decrease in support for the use of CSFs in primary prophylaxis with a regimen with a less than 40% rate of febrile neutropenia, secondary prophylaxis after afebrile neutropenia, and therapy for febrile neutropenia—settings in which CSF use was not recommended by ASCO guidelines. Finally, there was a 15% decrease in the odds of physicians supporting longer CSF schedules, including a routine use of 10 days of CSF treatment or use of a CSF treatment–cessation criterion of 10,000 WBCs/mm³ or an ANC of 10,000/mm³, changes that were supported by the ASCO guidelines.

Although these improvements are heartening, a substantial number of oncologists would use CSFs in scenarios in which the ASCO guidelines do not recommend such use. Important examples include primary prophylaxis after moderate-intensity chemotherapy regimens, when 6% to 16% of respondents would use CSFs; secondary prophylaxis for patients at low risk for febrile neutropenia or those for whom dose reduction would give equivalent results, chosen by 50% to 80% of respondents; and treatment of afebrile and febrile neutropenia, for which 30% and 60.5% of respondents would use CSFs.

Type of practice setting was the only factor significantly associated with variations in propensity to use CSFs as well as support for long CSF schedule regimens. Physicians who practiced in a fee-for-service setting were more likely to be users of CSFs and, when using a CSF, more likely to support long CSF schedule criteria than were those who practiced in academic or HMO settings. Whether this is due to differences in knowledge of the guidelines, clinical trial evidence, or some other factor is not known. However, our finding that having a CSF guideline in the practice setting was a significant predictor of shorter and more appropriate CSF schedule criteria suggests that guidelines may play some role in these improvements.

The limitations of the ASCO CSF surveys are important. First, data on actual practice patterns are needed, because what physicians say they do and what they actually do may be different.⁷ Second, the survey involved only 11 scenarios, whereas the actual clinical situations in which CSFs could be used are much more numerous. However, the scenarios were written to specifically address situations covered by the guidelines and represented common patient problems. Third, the results are from a sample of only 672 oncologists and may not be representative of the entire oncology community. Our high response rate and the similarity of the demographic characteristics of the respondents to those for the entire ASCO membership make this unlikely. Finally, the modest improvements in CSF use between 1994 and 1997 are likely to be attributable to several factors, including increased physician experience with the agents, publicized evidence, education programs, and insurance denial. Without a randomized trial of guidelines versus no guidelines in a single practice setting, it would be impossible to attribute improvements in CSF use solely to the guidelines.

The results from this survey provide reassurance that CSF use has modestly decreased in accordance with ASCO recommendations after the publication of the CSF guidelines and, for the most part, remains appropriate. The continued support for CSF use in cases of febrile and afebrile neutropenia for which data show no significant benefit,^8,9 and high use of CSFs in situations in which no clinical benefit has been shown regarding mild increases in dose intensity^4,5 suggest areas for improvement. The survey also indicates that financial considerations continue to be an important factor in determining the use of CSFs; fee-for-service physicians were significantly more likely to be high users of CSFs in 1994 and in 1997. Because no major improvement in disease or patient outcomes with standard chemotherapy regimens have been documented with the use of CSFs to date, more restricted use of these agents could result in equivalent outcomes at lower cost.

Why were ASCO guidelines not more effective in reducing the inappropriate use of CSFs? Guidelines clearly work to reduce practice variations, standardize care, and improve outcomes,^10,11 but changing practices can be difficult.¹² Successful guidelines include at least some of the following attributes: a strong basis in clinical evidence¹³ and practicality,¹⁴ local development and support,¹⁵ widespread dissemination,¹⁶ ease of access,^17,18 and linkage to accountability by audit of performance¹⁰ or reimbursement.¹⁹ ASCO's Health Service Research Committee has clearly demonstrated its ability to create evidence-based guidelines. The optimal strategy for the dissemination and implementation of the guidelines, determination of accountability for adherence to them, and determination of whether ASCO members or physicians at local practice sites should perform these tasks has not been determined.

ACKNOWLEDGMENTS

Supported by an unrestricted grant from the American Society of Clinical Oncology

NOTES

Presented as an oral presentation at the Thirty-Fourth Annual Meeting of the American Society of Clinical Oncology, Los Angeles, CA, May 16-19, 1998.

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Submitted August 11, 1998; accepted July 7, 1999.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Bennett, C. L. Articles by Smith, T. J. Search for Related Content PubMed PubMed Citation Articles by Bennett, C. L. Articles by Smith, T. J.