Journal of Clinical Oncology, Vol 19, Issue 8
(April), 2001: 2201-2205
© 2001 American Society for Clinical Oncology
Oral Mucositis and the Clinical and Economic Outcomes of Hematopoietic Stem-Cell Transplantation
By Stephen T. Sonis,
Gerry Oster,
Hank Fuchs,
Lisa Bellm,
Williamson Z. Bradford,
John Edelsberg,
Vanessa Hayden,
June Eilers,
Joel B. Epstein,
Francis G. LeVeque,
Carole Miller,
Douglas E. Peterson,
Mark M. Schubert,
Frederik K.L. Spijkervet,
Mary Horowitz
From Brigham and Women’s Hospital and Harvard School of Dental Medicine, Boston, and Policy Analysis, Inc, Brookline, MA; IntraBiotics Pharmaceuticals, Inc, Mountain View, and University of California, San Francisco, San Francisco, CA; University of Nebraska Medical Center, Omaha, NE; University of Washington Medical Center and Fred Hutchinson Cancer Research Center, Seattle, WA; Harper Hospital, Detroit, MI; Johns Hopkins Oncology Center, Baltimore, MD; University of Connecticut Health Center, Farmington, CT; University Hospital Groningen, Groningen, the Netherlands; and International Bone Marrow Transplant Registry, Milwaukee, WI.
Address reprint requests to Gerry Oster, PhD, Policy Analysis, Inc (PAI), Four Davis Court, Brookline, MA 02245.
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ABSTRACT
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PURPOSE: To explore the relationship between oral mucositis and selected clinical and economic outcomes in blood and marrow transplant patients.
PATIENTS AND METHODS: Subjects consisted of 92 transplant patients from eight centers who participated in a multinational pilot study of a new oral mucositis scoring system (Oral Mucositis Assessment Scale [OMAS]). In the pilot study, patients were evaluated for erythema and ulceration/pseudomembrane formation beginning on the first day of conditioning and continuing for 28 days. We examined the relationship between patients’ peak OMAS scores and days with fever (body temperature > 38.0°C), the occurrence of significant infection, days of total parenteral nutrition (TPN), and days of injectable narcotic therapy (all over 28 days), days in hospital (over 60 days), total hospital charges for the index admission, and vital status at 100 days.
RESULTS: Patients’ peak OMAS scores spanned the full range of possible values (0 to 5) and were significantly (P < .05) correlated with all of the outcomes of interest except days with fever (P = .21). In analyses controlling for type of graft (autologous v allogeneic) and study center, a 1-point increase in peak OMAS score was associated with (1) 1.0 additional day with fever (P < .01), (2) a 2.1-fold increase in risk of significant infection (P < .01), (3) 2.7 additional days of TPN (P < .0001), (4) 2.6 additional days of injectable narcotic therapy (P < .0001), (5) 2.6 additional days in hospital (P < .01), (6) $25,405 in additional hospital charges (P < .0001), and (7) a 3.9-fold increase in 100-day mortality risk (P < .01). Mean hospital charges were $42,749 higher among patients with evidence of ulceration compared with those without (P = .06).
CONCLUSION: Oral mucositis is associated with significantly worse clinical and economic outcomes in blood and marrow transplantation.
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INTRODUCTION
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ORAL MUCOSITIS is a frequent complication of the chemotherapy and radiotherapy regimens commonly used in oncologic practice. It is an especially severe problem for patients who are undergoing hematopoietic stem-cell transplantation (HSCT) because of the high-dose, myeloablative chemotherapy used for conditioning. In the transplant setting, oral mucositis is often so severe that patients require parenteral narcotics for relief of pain and, if oral intake is impossible, total parenteral nutrition (TPN). From the patient’s point of view, oral mucositis is often the single most debilitating complication of a transplant.1 In the presence of neutropenia, severe mucositis also may predispose patients to septicemia.2-4
There is no "gold standard" for diagnosing oral mucositis or assessing its severity. Most diagnostic tools are toxicity scales that emphasize the functional disability engendered by mucositis but neglect its anatomic characteristics (eg, size of ulcers, number of regions of the oral cavity affected).5 In addition, because the scoring of these scales is subjective and heavily influenced by the severity of pain experienced by the patient, the use of analgesics may impart a downward bias to the scores of patients with anatomically severe oral mucositis. The lack of an objective, reliable, and valid scale for measuring the extent of oral mucositis has been an impediment to research in this area.
To address this problem, a team of oral medicine specialists, oncologists, and oncology nurses from the United States, Canada, and Europe was convened in 1996 (Ciba-Oncogene Consensus Conference) to develop a new scoring system for evaluating the anatomic extent and severity of oral mucositis in research studies.6 The resulting scale was subsequently termed the Oral Mucositis Assessment Scale (OMAS). It has been used in a number of different settings and investigations, including a phase II clinical trial of a novel antimicrobial peptide.7
OMAS evaluates multiple regions of the oral cavity for erythema (none, mild/moderate, severe) and the presence and size of ulcerations or pseudomembranes (none, < 1 cm2, 1 to 3 cm2, > 3 cm2). In patients receiving ablative chemotherapy and bone marrow transplantation, OMAS scores have been reported to be significantly correlated with oral pain, difficulty swallowing, and inability to eat.6 In this study, we consider the relation between the severity of oral mucositis—as assessed by patients’ peak OMAS scores—and selected clinical and economic outcomes in blood and marrow transplantation.
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PATIENTS AND METHODS
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Overview
Data were obtained for 92 HSCT recipients who participated in a recent pilot study of the OMAS scoring system. In this pilot study, patients were evaluated for clinical manifestations of oral mucositis beginning on the first day of conditioning and continuing for 28 days; a detailed description of the study may be found elsewhere.6 We collected additional clinical and economic data for all subjects who participated in this pilot study and explored the relationship between their peak OMAS scores and the outcomes of care.
Study Subjects
Study subjects consisted of 92 patients from eight cancer centers who participated in a multinational pilot study of the OMAS scoring system and were (1) older than 12 years of age, (2) treated with a drug regimen for which the incidence of grade 3 or 4 mucositis as defined by the World Health Organization scale was at least 50% (commonly used regimens included cyclophosphamide and total-body irradiation; cyclophosphamide, thiotepa, and carboplatin; busulfan, melphalan, and thiotepa; and busulfan, cytarabine, cyclophosphamide, and methotrexate), (3) hospitalized during the chemotherapy treatment period, and (4) followed for greater than or equal to 21 days or until death.
Data Sources
Data for this study were obtained from three sources: (1) the OMAS pilot study, (2) the database of the International Bone Marrow Transplant Registry (IBMTR) and the Autologous Blood and Marrow Transplant Registry (ABMTR), and (3) medical and financial records of the cancer centers at which patients were treated. The study was approved by the institutional review board at each of the participating institutions.
In the OMAS pilot study, patients were evaluated for 28 days beginning on the first day of conditioning. Assessments occurred daily, except on weekends and holidays, for the first 12 days; thereafter, patients were seen each Monday, Wednesday, and Friday. Clinical examination of the mouth was performed using a standardized halogen light source. Eight regions of the oral cavity were evaluated for erythema and ulceration/pseudomembranes: the maxillary labial mucosa, the mandibular labial mucosa, the right buccal mucosa, the left buccal mucosa, the right lateral and ventral tongue, the left lateral and ventral tongue, the floor of the mouth and lingual frenum, and the soft palate and fauces. All clinical exams for any given patient were performed by the same assessor. Assessors did not take part in patient care decisions.
Data from these clinical exams were used to calculate an OMAS score for each patient at each assessment. In the OMAS system, erythema is evaluated using a 3-point scale as follows: 0 = none (no change in the color of the mucosa), 1 = mild/moderate (increase in intensity of color of mucosa), and 2 = severe (mucosa color of fresh blood). Ulceration/pseudomembrane formation at each site is evaluated using a 4-point scale as follows: 0 = no lesions, 1 = cumulative surface area of lesion(s) in a single site less than 1 cm2, 2 = cumulative surface area of lesion(s) in a single site greater than or equal to 1 cm2 and less than or equal to 3 cm2, and 3 = cumulative surface area of lesion(s) in a single site greater than 3 cm2. The value of OMAS at any given assessment is obtained by summing the erythema and ulceration/pseudomembrane subscores at each site (possible score range, 0 to 5), and then averaging these scores across all eight sites. Patients’ clinicians were blinded to the OMAS scores of their patients through the use of sealed envelopes.
The data collection process for all remaining information differed according to whether patients had information on file with the IBMTR or ABMTR. The IBMTR and ABMTR are voluntary registries that collect detailed demographic and clinical information on blood and marrow transplant patients from participating institutions using a standardized data collection instrument (the IBMTR/ABMTR Core Form).8 Not all transplant centers, however, participate in these registries.
For patients for whom a Core Form was available, demographic and clinical data were obtained from the IBMTR/ABMTR database. Selected data elements not reported to the IBMTR/ABMTR and hence unavailable on the Core Form (eg, number of days with fever, number of days of injectable narcotics) were collected directly from the centers at which patients were treated using a brief supplemental case report form that we designed specifically for this purpose. For patients for whom a Core Form was unavailable, data were abstracted from the records of the centers at which patients were treated using an abbreviated version of the IBMTR/ABMTR Core Form as well as the above-mentioned supplemental case report form. Hospital charges were obtained from UB-92 inpatient bills, which were unavailable for patients at the two non-U.S. study centers (n = 22).
Outcomes
We examined seven clinical and economic outcomes as follows: (1) the total number of days patients were febrile (body temperature  38.0°C) within 28 days of the first day of conditioning, (2) the incidence of significant infection within 28 days of the first day of conditioning, (3) the total number of days patients received TPN within 28 days of the first day of conditioning, (4) the total number of days patients received injectable narcotics within 28 days of the first day of conditioning, (5) the total number of days patients spent in hospital within 60 days of the first day of conditioning, (6) total hospital charges for the index admission (ie, the one during which the transplant occurred), and (7) mortality within 100 days of the first day of conditioning.
Analyses
We determined each patient’s peak OMAS score over all assessments, beginning on the first day of conditioning and extending through day 28 or the last day of follow-up, whichever came first. We then examined the relationship between patients’ peak OMAS scores and the clinical and economic outcomes of interest using Pearson’s product-moment correlations. We also used logistic regression (for dichotomous measures) and linear regression (for continuous measures) to estimate the independent contribution of peak OMAS score to the outcomes of interest, controlling for type of graft and study site. Once estimated, the regression equations were used to calculate adjusted values for the measures of interest across quartiles of the range of observed OMAS scores.
We also stratified patients according to whether or not they had evidence of ulceration at any time during follow-up. Evidence of ulceration was defined in terms of an OMAS ulceration/pseudomembrane subscore greater than 0 at any of the eight oral cavity sites at any assessment. We then similarly estimated (using linear and logistic regression, controlling for type of graft and study site) the independent contribution of ulceration to the outcomes of interest. All analyses were performed using PC SAS for Windows (Version 6.12 and higher. Cary, NC, SAS Institute, 1990).
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RESULTS
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Of the 92 study subjects, 42 received autografts and 50 received allografts ( Table 1). Autograft patients were slightly older than those receiving allografts, and more likely to be women. Autograft and allograft patients had similar pretransplant Karnofsky performance scores. The majority of autografts were performed for the treatment of solid tumors, while most allograft patients had hematologic malignancies. Patients were followed for an average of 25 days from the start of conditioning (range, 12 to 28 days); oral examinations were conducted an average of 13 times over this period (range, 7 to 17).
Table 2 lists selected outcomes by type of graft. In general, allograft patients experienced worse outcomes than autograft patients. Mean hospital charges for the index admission were, on average, approximately $70,000 higher among patients receiving allografts.
Patients’ peak OMAS scores spanned the full range of possible values. Scores were significantly higher among allograft recipients ( Table 3). Among autograft recipients, 83% had evidence of ulceration at one or more assessments; the corresponding number for allograft patients was 88%.
Table 4 lists Pearson’s correlation coefficients for patients’ peak OMAS scores and the outcomes of interest. On an overall basis, peak OMAS scores were significantly correlated with all of the outcomes of interest except days with fever (P = .21 for the latter measure). Among autograft patients, peak OMAS scores were significantly (P < .05) correlated with febrile days and the risk of significant infection. Among allograft patients, peak OMAS scores were significantly correlated with TPN days, injectable narcotic days, hospital charges, and 100-day mortality.
In multivariate analyses (linear regression for continuous variables, logistic regression for dichotomous variables) controlling for type of graft and study site, a 1-point increase in peak OMAS was found to be associated with 1.0 additional day with fever (P < .01), a 2.1-fold increase in the risk of significant infection (P < .01), 2.7 additional days of TPN (P < .0001), 2.6 additional days of injectable narcotic therapy (P < .0001), 2.6 additional days in hospital (P < .01), $25,405 in additional hospital charges (P < .0001), and a 3.9-fold increase in 100-day mortality (P < .01). Table 5 lists estimated values for the outcomes of interest (on the basis of logistic or linear regression as appropriate) by approximate quartiles of the distribution of actual OMAS scores.
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Table 5. Estimated Values for Selected Clinical and Economic Outcomes by Approximate Quartiles of Distribution of Peak OMAS Scores*
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Similar findings were noted when patients with evidence of ulceration were compared with those without, although this binary measure was not as highly correlated with the outcomes of interest as peak OMAS ( Table 6). (An odds ratio could not be calculated for 100-day mortality, as all of the deaths occurred among patients with ulceration.) Controlling for type of graft and study site, hospital charges were almost $43,000 higher among patients with evidence of any ulceration compared with those without (P = .06).
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DISCUSSION
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Oral mucositis is a frequent and significant side effect of both cancer chemotherapy and radiation treatment. It is an especially severe problem in the setting of HSCT. From the point of view of the transplant recipient, oral mucositis may be the single most debilitating and bothersome complication of myeloablative therapy.1 Loss of integrity of the oral mucosa results in a portal of entry for resident microflora, thereby predisposing patients to infection, especially during periods of myelosuppression.9
To the best of our knowledge, the first study of the impact of oral mucositis on outcomes of care was conducted by Ruescher et al.4 Autologous transplant patients with oral ulcerations were reported to be three times more likely to develop alpha-hemolytic streptococcal bacteremia than those without ulcerations and to stay in hospital an additional 6 days.4 Although this study provided important information on the potential impact of oral mucositis in the transplant setting, it was conducted in a single institution. The authors also did not report information on differences in costs of care. Our study confirms and extends these earlier findings.
Using data from a recent pilot study of a new oral mucositis scoring system, we explored the relationship between the extent and severity of oral mucositis, as assessed by objective findings of the condition (ulceration and erythema), and selected clinical and economic outcomes in 92 blood and marrow transplant patients from eight study centers in the United States, Canada, and Europe. Our findings indicate that the extent and severity of oral mucositis is significantly correlated with days of injectable narcotics, TPN, and injectable antibiotics; risk of significant infection; hospital days; hospital charges; and mortality. Total hospital charges were almost $43,000 higher among patients with ulceration in contrast to those without.
In prior studies, assessment of the severity of mucositis has often been confounded by other factors. Scales that combine objective and subjective outcomes, for example, are subject to alteration by the administration of analgesics. In our study, we assessed the extent and severity of mucositis using the OMAS, which was developed in 1996 by a team of U.S., Canadian, and European oral medicine specialists, oncologists, oncology nurses, experts in pain assessment, and statisticians. OMAS has been reported to have reasonable interrater reliability and validity,6 and has been successfully used in diverse settings and investigations. The results of this study suggest that OMAS is also a significant predictor of important outcomes in blood and marrow transplant patients. OMAS may therefore fill the need for a standardized, validated, and objective scoring system to assess the efficacy of interventions targeted at oral mucositis. The lack of such a measure has been an impediment to clinical research.
Peak mucositis scores were higher among allograft patients; this is likely related to the conditioning regimens (eg, total-body irradiation) that they receive and the use of methotrexate for graft-versus-host disease prophylaxis.10 Total hospital charges also were higher among allograft recipients. The lack of association between mucositis severity and significant infection and febrile days after allogeneic transplantation is probably explained by the greater frequency and severity of other transplant-related complications after allografting, which may obscure the impact of mucositis. Mucositis appears to be a much more important risk factor for infection after autotransplantation.
Severe mucositis appears to be associated with a marked increase in mortality. This finding is likely associative, rather than causative, and points to the importance of the mouth as a sentinel for clinical changes in other sites. Rappaport et al, for example, reported that oral mucositis was a good predictor of other indices of gastrointestinal toxicity associated with conditioning regimens for transplantation9; a relationship between oral mucositis and hepatic veno-occlusive disease has been reported by Wingard et al.11
Our findings are derived from patients’ peak OMAS scores (ie, worst mucositis) rather than an assessment of mucositis severity over time. Teleologically, the duration of mucositis should also be predictive of outcomes and costs. Peak mucositis, however, appears to be a reliable predictor of risk. The question arises whether patients with, for example, 3 days of severe mucositis are at the same risk as those with 10 days. The answer has yet to be established. Nonetheless, one would expect that prolonged management of mucositis carries additional clinical and economic costs. Consequently, a therapy that reduced both the duration and the acuity of this condition would likely be more beneficial than one that did one or the other.
In summary, we believe that our study has important implications. Our findings indicate that the extent and severity of oral mucositis in HSCT patients is positively correlated with the use of TPN and injectable narcotic therapy, the risk of significant infection and death, and total hospital days and charges. New therapies that are effective in reducing oral mucositis therefore have the potential to improve clinical outcomes and reduce costs of care.
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ACKNOWLEDGMENTS
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Supported by a research grant From IntraBiotics Pharmaceuticals Inc.
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REFERENCES
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1.
Bellm LA, Epstein JB, Rose-Ped A, et al: Patient reports of complications of bone marrow transplantation. Support Care Cancer 8: 33-39, 2000[Medline]
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Classen DC, Burke JP: Streptococcus mitis sepsis in bone marrow transplant patients receiving oral antimicrobial prophylaxis. Am J Med 89: 441-466, 1989
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Elting LS, Bodey GP, Keefe BH: Septicemia and shock syndrome due to viridans streptococcus: A case-control study of predisposing factors. Clin Infect Dis 14: 1201-1207, 1992[Medline]
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Ruescher TJ, Sodeifi A, Scrivani SJ, et al: The impact of mucositis on a-hemolytic streptococcal infection in patients undergoing autologous bone marrow transplantation for hematologic malignancies. Cancer 82: 2275-2281, 1998[Medline]
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Dodd MJ, Facione NC, Dibble SL, et al: Comparison of methods to determine the prevalence and nature of oral mucositis. Cancer Pract 4: 312-318, 1993
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Pico JL, Avila-Garavito A, Naccache P: Mucositis: Its occurrence, consequences, and treatment in the oncology setting. Oncologist 3: 446-451, 1998[Free Full Text]
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Submitted September 7, 2000;
accepted January 7, 2001.
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TOP
ABSTRACT
INTRODUCTION
