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Journal of Clinical Oncology, Vol 26, No 4 (February 1), 2008: pp. 606-611 © 2008 American Society of Clinical Oncology. DOI: 10.1200/JCO.2007.13.8222 Outcomes and Cost of Outpatient or Inpatient Management of 712 Patients With Febrile Neutropenia
From the Section of Health Services Research, Department of Biostatistics; Departments of Thoracic/Head & Neck Medical Oncology, General Internal Medicine, Ambulatory Treatment and Emergency Care, Breast Medical Oncology, and Sarcoma Medical Oncology; Department of Infectious Diseases and Infection Control, Quantitative Sciences Division, The University of Texas M.D. Anderson Cancer Center, Houston, TX; New York Lung Cancer Alliance, New York, NY; and Massachusetts General Hospital, Boston, MA Corresponding author: Linda S. Elting, DrPH, Section of Health Services Research, Department of Biostatistics, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd (Unit 447), Houston, TX 77030; e-mail: lelting{at}mdanderson.org
Purpose We retrospectively compared the outcomes and costs of outpatient and inpatient management of low-risk outpatients who presented to an emergency department with febrile neutropenia (FN). Patients and Methods A single episode of FN was randomly chosen from each of 712 consecutive, low-risk solid tumor outpatients who had been treated prospectively on a clinical pathway (1997-2003). Their medical records were reviewed retrospectively for overall success (resolution of all signs and symptoms of infection without modification of antibiotics, major medical complications, or intensive care unit admission) and nine secondary outcomes. Outcomes were assessed by physician investigators who were blinded to management strategy. Outcomes and costs (payer's perspective) in 529 low-risk outpatients were compared with 123 low-risk patients who were psychosocially ineligible for outpatient management (no access to caregiver, telephone, or transportation; residence > 30 minutes from treating center; poor compliance with previous outpatient therapy) using univariate statistical tests. Results Overall success was 80% among low-risk outpatients and 79% among low-risk inpatients. Response to initial antibiotics was 81% among outpatients and 80% among inpatients (P = .94); 21% of those initially treated as outpatients subsequently required hospitalization. All patients ultimately responded to antibiotics; there were no deaths. Serious complications were rare (1%) and equally frequent between the groups. The mean cost of therapy among inpatients was double that of outpatients ($15,231 v $7,772; P < .001). Conclusion Outpatient management of low-risk patients with FN is as safe and effective as inpatient management of low-risk patients and is significantly less costly.
In 1997, a guideline for management of low-risk outpatients with febrile neutropenia (FN) was initiated at The University of Texas M.D. Anderson Cancer Center. Low-risk patients were identified using a clinical algorithm previously used in feasibility trials.1,2 Clinical characteristics suggestive of a low risk of medical complications during therapy were combined with psychosocial criteria indicating access to caregivers at home, telephone and transportation in case of emergency, and a history of compliance with other outpatient regimens. Over time, we observed that approximately 15% of patients who were clinically eligible for outpatient management were managed as inpatients because they were psychosocially ineligible, creating an opportunity to compare the outcomes of clinically similar inpatients and outpatients. We conducted a retrospective comparison of the clinical and economic outcomes of low-risk patients treated for FN in inpatient and outpatient settings, the largest reported to our knowledge to date. We hypothesized that outpatients’ responses to antibiotic therapy were not lower, rates of complications and mortality were not higher, and durations of antibiotic therapy and fever were not longer than inpatients'. We further hypothesized that the cost of outpatient care was significantly lower than the cost of inpatient care.
Before its initiation, the study was reviewed and approved by the institutional review board at The University of Texas M.D. Anderson Cancer Center. We then constructed a retrospective cohort consisting of consecutive patients registered on the low-risk pathway between 1997 and 2003. For each of the 712 patients, we randomly selected one episode of FN. The paper and electronic records of each patient were abstracted by experienced research nurses. Three participating physicians (C.L., S.G., and J.T.) validated key data elements of every episode (infection diagnosis, response to antibiotic treatment, and complications) using an electronic system that blinded investigators to each patient's in- or outpatient status. External reviewers (R.G., J.A.T.) conducted a second blinded review of a randomly chosen sample of 10% of the episodes to ensure that key data elements were not systematically misclassified because of misinterpretation by clinical associates from the same institution. Agreement between the internal and external blinded reviewers was 97%. Two instances of difference of opinion were decided by a blinded review performed by the other external reviewer.
Clinical Pathway for Management of Low-Risk Patients With FN
Outcomes
Statistical Considerations
The sample included a total of 712 low-risk patients of whom 589 (83%) were managed as outpatients and 123 (17%) as inpatients. The outpatients and inpatients were similar with respect to performance status, prevalence of comorbidities, dehydration, hypotension, documented infections, mean temperature at presentation and at discharge from the ED, and extent of disease (Table 1). Women, older patients, and those with uncontrolled cancer or mucositis were somewhat more likely to be treated as inpatients, whereas Asian patients and those with sarcoma were over-represented among outpatients. Inpatients had a higher mean absolute neutrophil count at baseline, but this difference was too small to be considered clinically significant. The mean MASCC risk score was significantly higher (better) among outpatients, but more than 90% of both groups would have been categorized as low risk by their MASCC scores.
Most of our hypotheses were proven correct (Table 2). Overall success occurred in 79% of inpatients and 80% of outpatients (P = .75). Overall success rates were not significantly different within propensity score strata. Outpatients’ and inpatients’ responses to the initial antibiotic regimen also were virtually identical overall (81% v 80%; P = .94) and among those with documented infections (66% v 70%; P = .14). Ultimately, 100% of all patients responded to therapy, and there were no deaths during the study. The mean durations of antibiotic therapy (8.5 v 9.2 days; P = .08) and fever (2.0 v 2.4 days; P = .04) were shorter among outpatients compared with inpatients.
Considering the 529 initially treated as outpatients, 121 required hospitalization for management of FN; thus, the response to outpatient management was 79% (Fig 1). Among those admitted were 21 patients with bacteremia, nine with pneumonia, 22 with other documented infections, 27 with complications, 29 who remained febrile after initial antibiotic therapy, and 13 who developed intolerance to oral medications caused by oral mucositis or nausea. Seven outpatients experienced treatment failure with outpatient therapy but responded to the initial antibiotics after hospitalization. Interestingly, using a threshold of 21 or higher, the baseline MASCC risk index would have excluded from outpatient therapy all of the outpatients who ultimately required hospitalization. This improved specificity would have come at the expense of hospitalization of only nine patients who were successfully managed as outpatients.
Compared with inpatient management, outpatient management was significantly less expensive on average ($15,231 v $7,799; P < .001; Table 2). Outpatients who required hospitalization had significantly higher inpatient charges than their counterparts who were treated as inpatients initially ($18,565 v $13,983; P = .008). However, after comparing outpatients who required hospitalization with similar inpatients (those who experienced treatment failure with initial antibiotic therapy), no significant differences were observed (P = .18), suggesting that the care of outpatients who experienced failure was not more expensive than the care of those who experienced failure in the inpatient setting.
In the 1960s, Bodey et al6 described the inverse relationship between FN-associated mortality and the absolute neutrophil count. Concurrently, Curtin and Marshall7 observed high mortality among leukemia patients in whom antibiotic administration was delayed until culture results were available. These observations led to clinical trials of empiric therapy,8 a practice that became widespread after publications by Schimpf et al.9 Infection was the most common cause of death among patients with cancer.10 On the basis of these early studies, broad-spectrum, intravenous antibiotic therapy, administered in the hospital from the onset of fever was the standard of care for FN for more than three decades.11 As superior antibiotics and regimens were developed, mortality from FN plummeted, particularly among patients with solid tumors. Oral regimens12,13 and monotherapy14-17 were tested to simplify care during FN. As these improvements were tested, it became increasingly clear that there was a subset of patients with FN who were at very low risk for poor clinical outcomes. This observation led to two parallel research pathways. Talcott et al18 observed patients with FN for development of complications and mortality. They identified a large population of outpatients who had low risk of complications or death. A second study validated these observations.19 The results of these studies formalized previous clinical observations and laid the foundation for risk assessment. Simultaneously, Rubenstein et al2 demonstrated the feasibility of outpatient therapy, comparing oral with intravenous regimens and selecting low-risk candidates for outpatient management using a clinical algorithm. As in Talcott's observational studies, complications were uncommon and no deaths were observed. The study was replicated in larger samples,1 community practices,20 in Europe,21 and in Asia.22 Complications were uncommon. However, the few deaths that were observed led to understandable concern that, although outpatient management was feasible, it might not be as effective as inpatient management. Although two of the aforementioned trials involved random assignment to inpatient or outpatient therapy,21,22 neither was large enough to identify differences in rarely occurring events (ie, mortality) between outpatients and inpatients. An adequately powered study, initiated in the United States, could not be completed as a result of poor enrollment. Thus, the effectiveness of inpatient and outpatient management of low-risk FN patients was never formally tested in an adequately powered comparative trial.23-25 We initiated the present study to fill that gap in knowledge. However, the interpretation of our results should be undertaken only after consideration of our study's limitations. First, it is critical to remember that this was an observational study, not a randomized trial of outpatient and inpatient management strategies. On the basis of prospective assessments in the ED and retrospective review of the medical records, the inpatients and outpatients treated on the guideline were clinically similar and differed only in psychosocial characteristics. However, it is possible that decisions to assign some patients to inpatient therapy were influenced by unmeasured clinical factors not reflected in the recorded assessments. If that occurred frequently, we may have underestimated the response rate that would be observed in a population of truly low-risk patients treated in the hospital. Second, we studied patients treated in a single comprehensive cancer center. In previous studies we have observed that our patients differ from cancer patients in the community in that they have more advanced cancers, but are younger and have fewer comorbidities.26 It is also possible that patients who present to referral institutions are more motivated to comply with therapy than are those in the population at large. To the extent that these differences influence outcomes of FN, our results may lack generalizability. Despite these limitations, our results are consistent with previous findings; outpatients’ and inpatients’ overall success rates and responses to initial therapy were virtually identical,21,22,27,28 major complications were rare28-34 and equally common in both groups, and no patient died during therapy.1,2,21,28-36 Although generally consistent with results from clinical trials, our response rates to initial therapy among both outpatients (81%) and inpatients (80%) would rank among the lowest previously reported (77% to 96%). This is a common observation when comparing outcomes observed in clinical trials with those in general oncology practice.26,37 Similarly, the rate of hospital admission among outpatients in our study (21%) was more than double that observed previously in clinical trials conducted in our institution using the same selection criteria (7% and 8%).1,2,38 Although not quite as favorable as those observed in carefully controlled clinical trials, our results still support the effectiveness of outpatient management of FN. Compared with outpatients, we observed slightly longer durations of fever and antibiotic therapy among inpatients. One explanation for this observation is that the inpatients responded more slowly to antibiotic therapy. Slower response to therapy has been reported among patients with complex infections such as pneumonia and cellulitis.39,40 However, documented infections were similarly distributed among inpatients and outpatients and probably do not explain this difference. The similarity between inpatients and outpatients with respect to performance status, comorbidities, hypotension, and dehydration also argues against this explanation. We believe the observed differences reflect differences between inpatient and outpatient management in prescribing (open-ended prescription in the hospital v closed-ended 7-day prescription in the outpatient setting) and frequency of temperature measurement (several times v one time per day recorded). As expected, outpatient management was less expensive than inpatient management, even after accounting for the cost of hospitalization in 21% of outpatients. These findings were consistent with previous studies of the resource utilization and cost of inpatient and outpatient management of FN.24,27,41-45
Given the similarity of inpatients’ and outpatients’ outcomes and the favorable economic profile of the outpatient strategy, use of our clinical algorithm for management of low-risk FN patients seems justifiable. However, the 21% hospitalization rate suggests considerable room for improvement. The MASCC risk index, which was published after our guideline was initiated, may provide such improvement.5 At the recommended threshold ( Compared with inpatient management, outpatient management of low-risk patients with FN identified by our clinical algorithm is equally safe and effective and is significantly less expensive in our comprehensive cancer center. Similarities between this retrospective analysis and previous reports of outpatient strategies in other academic and community practices support the generalizability of our findings to the entire population of low-risk cancer patients with FN.
Although all authors completed the disclosure declaration, the following author(s) indicated a financial or other interest that is relevant to the subject matter under consideration in this article. Certain relationships marked with a "U" are those for which no compensation was received; those relationships marked with a "C" were compensated. For a detailed description of the disclosure categories, or for more information about ASCO's conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors. Employment or Leadership Position: None Consultant or Advisory Role: Linda S. Elting, Endo Pharmaceuticals (C); Ya-Chen Tina Shih, Berlex Laboratories (C); Kenneth Rolston, Cubist Pharmaceuticals (C), Astellas Pharma (C) Stock Ownership: None Honoraria: None Research Funding: Linda S. Elting, Amgen, MGI Pharma; Kenneth Rolston, Cubist Pharmaceuticals, Elan, Schering-Plough Expert Testimony: None Other Remuneration: None
Conception and design: Linda S. Elting, Charles Lu, Sharon H. Giordano, Jonathan C. Trent, Catherine Cooksley, Elenir B.C. Avritscher, Kenneth Rolston Financial support: Linda S. Elting Administrative support: Linda S. Elting Provision of study materials or patients: Charles Lu, Carmelita P. Escalante, Kenneth Rolston Collection and assembly of data: Linda S. Elting, Charles Lu, Sharon H. Giordano, Catherine Cooksley, Elenir B.C. Avritscher, Richard J. Gralla, James A. Talcott Data analysis and interpretation: Linda S. Elting, Charles Lu, Sharon H. Giordano, Jonathan C. Trent, Catherine Cooksley, Ya-Chen Tina Shih, B. Nebiyou Bekele, Richard J. Gralla, James A. Talcott Manuscript writing: Linda S. Elting, Jonathan C. Trent, Ya-Chen Tina Shih, James A. Talcott, Kenneth Rolston Final approval of manuscript: Linda S. Elting, Charles Lu, Sharon H. Giordano, Jonathan C. Trent, Catherine Cooksley, Elenir B.C. Avritscher, Ya-Chen Tina Shih, Joe Ensor, B. Nebiyou Bekele, Richard J. Gralla, Kenneth Rolston
We thank Lisa Hughes, Linda Yancey, Brendell Williams, Kimberly Edwards, and Roxana Duran for data collection and the physicians and nurses of the Emergency Department for clinical management of the patients, without which this project would have been impossible.
Supported by a Research Scholar Grant from the American Cancer Society (RSGHP-02-184-01-PBP). Presented in part at the 41st Annual Meeting of the American Society for Clinical Oncology, May 13-17, 2005, Orlando, FL. Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.
1. Rolston K, Rubenstein E, Elting L, et al: Ambulatory management of febrile episodes in low-risk neutropenic patients. Presented at the 35th Interscience Conference on Antimicrobial Agents in Chemotherapy, September 17-20, 1995, San Francisco, CA 2. Rubenstein EB, Rolston K, Benjamin RS, et al: Outpatient treatment of febrile episodes in low-risk neutropenic patients with cancer. Cancer 71:3640-3646, 1993[CrossRef][Medline] 3. Escalante CP, Weiser MA, Manzullo E, et al: Outcomes of treatment pathways in outpatient treatment of low risk febrile neutropenic cancer patients. Support Care Cancer 12:657-662, 2004[Medline] 4. Uys A, Rapoport BL, Anderson R: Febrile neutropenia: A prospective study to validate the Multinational Association of Supportive Care of Cancer (MASCC) risk-index score. Support Care Cancer 12:555-560, 2004[Medline] 5. 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Antimicrob Agents Chemother 26:870-875, 1984 17. Pizzo PA, Hathorn JW, Hiemenz J, et al: A randomized trial comparing ceftazidime alone with combination antibiotic therapy in cancer patients with fever and neutropenia. N Engl J Med 315:552-558, 1986[Abstract] 18. Talcott JA, Finberg R, Mayer RJ, et al: The medical course of cancer patients with fever and neutropenia: Clinical identification of a low-risk subgroup at presentation. Arch Intern Med 148:2561-2568, 1988 19. Talcott JA, Siegel RD, Finberg R, et al: Risk assessment in cancer patients with fever and neutropenia: A prospective, two-center validation of a prediction rule. J Clin Oncol 10:316-322, 1992[Medline] 20. Gralla R, Eisenberg PD, Bizette GA: Two outpatient oral trials using ciprofloxacin plus amoxicillin/clavulanate for febrile neutropenia in lower risk patients. Support Cancer Care 8:241, 2000 21. 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Copyright © 2008 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
2 test or Fisher's exact test, where appropriate. Durations of hospitalization, fever, and antibiotic therapy and charges were reported as means with 95% CIs. Differences between means were tested for statistical significance using t tests, assuming unequal variance, except that comparisons of mean charges employed Mann-Whitney tests owing to the skewness of the data. All P values were two tailed. Because of small differences between inpatients and outpatients in the age and sex distributions, prevalence of mucositis, and baseline Multinational Association of Supportive Care in Cancer (MASCC) risk score,
21), the MASCC index would have assigned to inpatient treatment all of the 121 patients who were treated unsuccessfully as outpatients. Prospective assessments of the effectiveness and feasibility of using the MASCC risk index are ongoing. 
