Original Article
A Controlled Trial of Fluconazole to Prevent Fungal Infections in Patients Undergoing Bone Marrow Transplantation
N Engl J Med 1992; 326:845-851March 26, 1992
- Abstract
- Abstract
Background and Methods.
Superficial and systemic fungal infections are a major problem among severely immunocompromised patients who undergo bone marrow transplantation. We performed a doubleblind, randomized, multicenter trial in which patients receiving bone marrow transplants were randomly assigned to receive placebo or fluconazole (400 mg daily). Fluconazole or placebo was administered prophylactically from the start of the conditioning regimen until the neutrophil count returned to 1000 per microliter, toxicity was suspected, or a systemic fungal infection was suspected or proved.
Results.
By the end of the treatment period, 67.2 percent of the 177 patients assigned to placebo had a positive fungal culture of specimens from any site, as compared with 29.6 percent of the 179 patients assigned to fluconazole. Among these, superficial infections were diagnosed in 33.3 percent of the patients receiving placebo and in 8.4 percent of the patients receiving fluconazole (P<0.001). Systemic fungal infections occurred in 28 patients who received placebo as compared with 5 who received fluconazole (15.8 percent vs. 2.8 percent, P<0.001). Fluconazole prevented infection with all strains of candida except Candida krusei. Fluconazole was well tolerated, although patients who received it had a higher mean increase in alanine aminotransferase levels than patients who received placebo. Although there was no significant difference in overall mortality between the groups, fewer deaths were ascribed to acute systemic fungal infections in the group receiving fluconazole than in the group receiving placebo (1 of 179 vs. 10 of 177, P<0.001).
Conclusions.
Prophylactic administration of fluconazole to recipients of bone marrow transplants reduces the incidence of both systemic and superficial fungal infections. (N Engl J Med 1992;326:845–51.)
Media in This Article
Figure 1
Kaplan–Meier Estimates of the Percentage of Patients Given Fluconazole or Placebo Who Did Not Have Systemic Fungal Infections.Figure 2
Kaplan–Meier Estimates of the Percentage of Patients Given Fluconazole or Placebo Who Did Not Have Superficial Fungal Infections.Article Activity
- Article
BONE marrow transplantation is commonly used to treat cancer and aplastic anemia and is gaining a role in the treatment of genetic disorders.1 Although many bacterial and viral infections can now be prevented, superficial and systemic fungal infections remain important causes of morbidity and mortality in transplant recipients, even in view of the aggressive use of topical antifungal agents.2 Fluconazole, a triazole antifungal agent, is highly active against a variety of fungal pathogens that cause systemic mycoses.3 It is well absorbed orally and has been safe and effective both in treating superficial4 and systemic5 infections with candida species and as maintenance therapy for cryptococcal meningitis.6 Studies in animals suggest that fluconazole is effective in neutropenic hosts7 and that high doses may help prevent aspergillus infection.8 We performed a study to determine whether fluconazole can be used safely to reduce the incidence of mycoses in recipients of bone marrow transplants.
Methods
Patients
Potential study participants were at least 13 years of age and about to undergo allogeneic or autologous bone marrow transplantation at 1 of the 17 participating centers. Informed consent was obtained from the patients or their parents. Patients were excluded from the study if they weighed less than 34 kg, had a history of allergy or intolerance to imidazoles or azoles, had moderate or severe liver disease (defined as a level of aspartate aminotransferase, alanine aminotransferase, or alkaline phosphatase that was more than five times the upper limit of normal or a total bilirubin level of more than 43 μmol per liter [2.5 mg per deciliter]), or had an estimated creatinine clearance of less than 0.83 ml per second (50 ml per minute). A base-line pregnancy test was required for all women of childbearing age to exclude those who were pregnant. Patients were also excluded if they had received systemic antifungal agents within two weeks of the study or had evidence of a preexisting systemic fungal infection.
Study Protocol
After screening, patients were randomly assigned a study number from a sequential list kept by each hospital's pharmacy. Patients were assigned to receive fluconazole and placebo in a 1:1 ratio, and therapy was begun when the transplant-conditioning regimen was initiated. The study drug and an identical-appearing placebo were supplied to each participating center in a blinded manner. Patients received a daily oral dose of 400 mg of fluconazole or placebo. Those who were unable to tolerate oral medications received an intravenous preparation of 200 mg of fluconazole or placebo every 12 hours. If renal dysfunction developed, the dosage of fluconazole was decreased by 50 percent in patients with estimated creatinine clearances of less than 0.83 ml per second (50 ml per minute) and by 75 percent in patients with creatinine clearances of less than 0.33 ml per second (20 ml per minute). Treatment was continued until the neutrophil count had increased to more than 1.0×109 per liter (1000 per microliter) and had remained at this level for 7 days or until systemic fungal infection was suspected or proved; the maximal length of treatment with fluconazole or placebo was 10 weeks.
Patients were clinically evaluated at base line, twice weekly for the duration of treatment, and again 14 days after treatment was stopped. Cultures of specimens from the oropharynx, feces or perirectal area, and urine were obtained at base line and weekly thereafter until 14 days after the end of the treatment period. In addition to monitoring for signs and symptoms of infection and for any adverse effects, creatinine, electrolytes, aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, and total bilirubin were measured at least weekly. A complete blood count, with differential and platelet counts, and urinalysis were performed at least twice weekly, and chest films were required every two weeks. Blood samples and cultures for fungi in addition to the weekly surveillance cultures were obtained as deemed clinically indicated by the primary care physicians. Concomitant therapy with systemic antifungal agents was not allowed. The date of onset of any side effects, as well as their duration, severity, and possible relation to the therapy, was recorded. Decisions to discontinue and to readminister the study drug or placebo were made on a case-by-case basis after discussion between the individual investigator and the study monitor, both of whom were unaware of the group to which the patient had been assigned.
Fungal colonization was considered to be present if surveillance cultures yielded a fungus isolated from skin, mucous membrane, or both in the absence of clinical findings of fungal infection. Although no topical antifungal prophylaxis was allowed in either group during treatment, topical clotrimazole therapy was allowed for up to 14 days for patients who had evidence of superficial fungal infection, defined as clinically apparent infections of the oropharynx, skin, or genitalia along with positive cultures. A suspected case of systemic fungal infection was defined broadly as any episode, such as persistent fever despite treatment with broad-spectrum antibacterial agents, for which the physician felt compelled to treat empirically with amphotericin B but for which a fungal infection could not be established. A definite systemic fungal infection was defined as one in which there was both clinical evidence of blood or tissue infection and a culture or biopsy specimen from the involved site demonstrating a pathogenic fungal organism. Once a systemic fungal infection was suspected or proved, the study drug or placebo was discontinued, and the infection was treated as deemed appropriate by the investigator. Patients with infections or toxic reactions were included in the analyses if the complications occurred during treatment or within 11 days (8 fluconazole half-lives) after treatment was stopped.
Statistical Analysis
All statistical analyses were performed as two-tailed tests. Results are reported for all patients enrolled in the study (intention-to-treat analysis), except for one patient who was randomly assigned to placebo and who had positive pretreatment blood cultures for aspergillus. Confidence limits for differences between the groups were computed with the normal approximation to the binomial distribution. Kaplan–Meier estimates of survival were computed with the SAS procedure LIFETEST. Gehan's modified Wilcoxon test, the log-rank test, and likelihood-ratio chi-square tests were used to check for the equality of two survival distributions.9 Interactions between centers and treatments were assessed with the Breslow—Day statistic.10 Changes between base-line and final values for hematologic, hepatic, renal, and electrolyte indexes were compared with the Wilcoxon rank-sum test.
Results
Subjects' Characteristics at Base Line
The group assigned to fluconazole had a larger proportion of male subjects than the group assigned to placebo (59 percent vs. 44 percent, P<0.01). There were no significant differences between the two groups in age, race, or weight (data not shown) at the time randomization, or in primary diagnoses. Fifty-two percent of the patients in the fluconazole group received allogeneic transplants, whereas 56 percent of the placebo group received autologous grafts (P = 0.12). The proportion of patients with fungal colonization at base line was not significantly different in the fluconazole and placebo groups (44.1 percent vs. 38.9 percent, P = 0.38). No significant effects of the treatment center on study outcomes were observed.
Systemic Fungal Infection
Proved systemic fungal infection occurred in 28 of the 177 patients receiving placebo (15.8 percent; 95 percent confidence interval, 10.4 percent to 21.2 percent) but in only 5 of the 179 patients receiving fluconazole (2.8 percent; 95 percent confidence interval, 0.4 percent to 5.2 percent; P<0.001). The Kaplan–Meier estimates of the percentage of patients in each group who did not have a systemic fungal infection showed that fluconazole had a significant protective effect (P = 0.001) (Fig. 1Figure 1
Kaplan–Meier Estimates of the Percentage of Patients Given Fluconazole or Placebo Who Did Not Have Systemic Fungal Infections.). Most proved systemic fungal infections occurred early in the neutropenic period after a median of 16 days of treatment. Table 1Table 1
Types of Fungi Isolated in Systemic Infections. shows the distribution of fungal isolates obtained from the patients with systemic infections in both groups. In marked contrast to the patients given placebo, the fluconazole-treated patients had no systemic infections with candida species other than Candida krusei. The incidence of infections due to other fungi, such as aspergillus and mucorales, was low, and there were no differences in incidence between the two treatment groups. The characteristics of the proved cases of systemic fungal infection and their clinical outcomes are summarized in Table 2Table 2
Characteristics and Outcomes of the Definite Cases of Systemic Fungal Infection.*. Tissue involvement with candida or torulopsis species was ultimately noted in 10 patients receiving placebo but in none of the patients receiving fluconazole (P<0.001). The tissue involvement was documented by autopsy or biopsy in 7 of the 10 patients and diagnosed clinically or by bronchoscopy in the other 3. The definite cases of candida or torulopsis infection of tissue involved multiple organs in three cases, the lung in two cases, the small bowel in one case, and the skin in one case. Our prospectively adopted definition of a definite systemic fungal infection allowed for the inclusion of urinary, esophageal, and lung infections without documented fungemia. When such cases of potentially less severe and localized disease were excluded from the analysis, there were 24 cases of systemic mycosis among placebo recipients and 4 cases among fluconazole recipients, and the difference between the groups was still significant (P<0.001).The mortality was high among patients with documented tissue involvement, including those infected with noncandidal species, regardless of whether they received fluconazole or placebo (11 of 13, 85 percent). Treatment with fluconazole reduced not only the total number of systemic fungal infections, but also the number of deaths ascribed to fungal infection either by an investigator who was unaware of the patient's group assignment or on the basis of autopsy results. Thus, death was attributed to fungal infection in 10 patients in the placebo group as compared with 1 in the fluconazole group (P<0.001); these deaths represented 36 percent and 20 percent, respectively, of the patients who had systemic fungal infections. One other patient in the fluconazole group in whom a fungal infection developed subsequently died. Although this death was attributed by the blinded investigator not to fungal infection but to renal failure and the adult respiratory distress syndrome, fungemia with C. krusei may have been a contributing factor. In the placebo group, 5 of the 6 cases of C. tropicalis infection were fatal, as compared with 2 of the 12 cases of C. albicans infection (P = 0.01), and death was attributed to candidemia.
Superficial Fungal Infection
Treatment with fluconazole significantly reduced and delayed the development of superficial fungal infections (P = 0.001) (Fig. 2Figure 2
Kaplan–Meier Estimates of the Percentage of Patients Given Fluconazole or Placebo Who Did Not Have Superficial Fungal Infections.). Superficial infections were reported in 15 of the 179 patients who received fluconazole (8.4 percent; 95 percent confidence interval, 4.3 percent to 12.4 percent) and in 59 of the 177 patients who received placebo (33.3 percent; 95 percent confidence interval, 26.4 percent to 40.3 percent; P<0.001). The reduction in superficial infections among patients receiving fluconazole was evident at each of the three most common sites of infection: the oropharynx, genital and rectal areas, and skin.Other Results of Prophylaxis
There were no significant differences in overall mortality between the groups at 90 days. There were 55 deaths among the 179 fluconazole recipients (30.7 percent) and 46 deaths among the 177 placebo recipients (26 percent, P = 0.38). Among fluconazole recipients, death was attributed to fungal infection in 1 patient, nonfungal infections in 18 patients, graft-versus-host disease or other noninfectious complications in 29 patients, and recurrent cancers in 7 patients. Among placebo recipients, death was attributed to fungal infection in 10 patients, nonfungal infections in 15 patients, graft-versus-host disease or other noninfectious complications in 16 patients, and recurrent cancers in 5 patients. Fluconazole was given for a mean of 22.6 days, and placebo for a mean of 19.7 days (P = 0.01). The predominant reason for the discontinuation of therapy was the empirical use of amphotericin B because of suspected fungal infection. Discontinuation for proved systemic infection, suspected treatment-related side effects, or abnormal laboratory values was less common. The majority of patients in both groups had unexplained fevers after transplantation. Such fevers were the most frequent reason for the discontinuation of therapy and the initiation of systemic amphotericin B therapy. This occurred in 116 of 177 patients in the placebo group and 101 of 179 patients in the fluconazole group (65.5 percent vs. 56.4 percent, P = 0.065). Kaplan–Meier analysis of the mean length of time until empirical antifungal therapy was initiated (17 days for placebo and 21 days for fluconazole) showed that the use of such therapy was delayed in patients receiving fluconazole (P<0.004). Among the patients who received empirical therapy, systemic fungal infection was subsequently documented in 21 of the 116 patients in the placebo group but in only 1 of the 101 patients in the fluconazole group (18.1 percent vs. 1 percent, P<0.001). During the study, fungal colonization decreased at each site cultured among the patients receiving fluconazole, whereas it increased among placebo recipients. Thus, by the end of prophylaxis the number of patients with a positive oropharyngeal, fecal, or urine culture had decreased from 78 (43.6 percent) to 53 (29.6 percent) in the fluconazole group (P<0.001 by the chi-square test) but had increased from 67 (37.8 percent) to 119 (67.2 percent) in the placebo group (P<0.001 for the comparison with base-line values and with values for fluconazole). Of the 78 fluconazole-treated patients who were colonized at base line, 45 (58 percent) subsequently had negative cultures, as compared with only 4 of 67 such patients (6 percent) who received placebo (P<0.001). Fifty-six of the 110 patients in the placebo group who were not colonized at base line subsequently became colonized, as compared with 20 of the 101 such patients in the fluconazole group (51 percent vs. 19.8 percent, P<0.001). Table 3Table 3
Types of Colonizing Fungi Isolated at Base Line and in the Last Culture Obtained during Active Prophylaxis. shows the distribution of fungal species isolated from any site at base line and at the end of study. There was an increase in the number of isolates of Torulopsis glabrata in both groups during the study. C. krusei was isolated somewhat more frequently after treatment with fluconazole (0 patients at base line vs. 4 at the time of the last culture, P = 0.06). Neither C. krusei nor T. glabrata was isolated significantly more frequently at the end of prophylaxis in the fluconazole group than in the placebo group.Clinical Side Effects and Abnormal Laboratory Values
There were no significant differences between the fluconazole and placebo groups in the number of patients with clinical side effects ascribed to treatment (31 patients vs. 30 patients). These side effects led to withdrawal of therapy in two patients receiving placebo and in one patient receiving fluconazole. The most common effects were nausea, occurring in 13 fluconazole recipients and 9 placebo recipients, and skin rash, occurring in 9 patients in each group. Abnormal laboratory values were extremely common during the process of bone marrow transplantation. The clinician investigators at the various study centers had the option of discontinuing treatment because of clinical side effects or abnormal laboratory values. Treatment was discontinued in 17 fluconazole recipients and 11 placebo recipients because of abnormal laboratory values (P = 0.34), in all cases elevated liver-function tests. Seven fluconazole recipients and three placebo recipients (P = 0.16) had hepatic dysfunction listed by an investigator as a factor contributing to their deaths, which were usually attributed to either venoocclusive or graft-versus-host liver disease. The alanine aminotransferase level was more than three times the upper limit of normal or, if the baseline value exceeded the upper limit of normal, was three times the base-line value in 29.4 percent of patients receiving fluconazole and in 21.9 percent of patients receiving placebo (P = 0.16). The mean alanine aminotransferase value increased by 100 U per liter in patients receiving fluconazole (from 32 U per liter at base line to 132 U per liter at the final evaluation) and by 35 U per liter in patients receiving placebo (from 37 U per liter at base line to 72 U per liter at the final evaluation, P = 0.024). We could define no subgroup with extreme hepatic sensitivity to fluconazole, since we found no significant differences between the treatment groups in the numbers of patients with more than 5-fold, 10-fold, or 20-fold increases in aspartate aminotransferase, alanine aminotransferase, bilirubin, or alkaline phosphatase levels. There were no differences in the frequency of any other abnormal laboratory values with the exception of eosinophilia (defined as a more than 50 percent increase in the number of eosinophils present at base line, or a count above 0.5 × l09 per liter [500 per microliter]), which occurred in six patients receiving fluconazole but in none of the patients receiving placebo (P = 0.015). Finally, there were no differences between the treatment groups in the pattern of the decline or recovery of the neutrophil count.
Discussion
Fungal infections remain a major problem in bone marrow transplantation. The nearly 16 percent incidence of systemic fungal infections noted among placebo recipients in our study is similar to that reported in previous studies from major centers for bone marrow transplantation, and these infections occur despite aggressive treatment with topical antifungal agents.2 , 11 , 12 The most common etiologic agents in such infections are candida species. For example, among 665 patients who underwent bone marrow transplantation at the University of Minnesota Hospital, systemic candidal infection was diagnosed in 76 patients (11.4 percent) and was thought to be the direct cause of death in one third of these patients.12 These results are consistent with the incidence of fungal infections in our placebo group and the mortality rate of approximately one third in these patients. Our results demonstrate that the prophylactic administration of fluconazole reduces the incidence of systemic candidiasis and significantly reduces the number of deaths from fungal infection. Nine of the 10 deaths among patients receiving placebo that were attributed to fungal infection occurred despite the initiation of empirical amphotericin therapy, suggesting that prophylactic therapy is preferable to empirical treatment. It is of interest that C. tropicalis infections occurred only in placebo recipients and appeared to be particularly virulent, a clinical observation consistent with findings in a murine neutropenic model of candidiasis.13 Fluconazole was also highly effective in reducing both fungal colonization and the incidence of superficial infections. The reduction in colonization may have been important in preventing systemic infections, since colonization has been shown to be related to the development of systemic candidiasis.12 In our study, 20 of the 28 patients with systemic infections due to candida or torulopsis had previously been colonized with the infecting organism. Two recent studies have examined low-dose (50 mg per day) fluconazole prophylaxis in heterogeneous groups of patients with malignant conditions.14 , 15 In both, the frequency of superficial fungal infections was reduced by fluconazole therapy. Our study conclusively shows that preventive therapy is effective in reducing the incidence of systemic mycoses in severely immunosuppressed patients. Although orally administered ketoconazole is also active against candida species, it was ineffective as prophylaxis in the setting of bone marrow transplantation.16 One previous study suggested that intravenous miconazole could reduce fungemia among patients with neutropenia.17 This smaller study had a short duration of treatment and a low incidence of fungal sepsis among study subjects, and did not find that miconazole had any effect on fungal colonization. In addition, miconazole may be associated with more frequent side effects.18
Fluconazole was well tolerated by the patients in our study, despite their acute illnesses and the administration of a number of other medications. We were particularly concerned about potential liver toxicity because of both the known effect of the chemically related imidazole ketoconazole19 and two possible instances of severe fluconazole hepatotoxicity reported to the manufacturer. As described, abnormal results of liver-function tests were very common in both the fluconazole and placebo groups and are known to occur in the majority of patients undergoing bone marrow transplantation.20 Major contributing factors most likely include graft-versus-host and venoocclusive liver disease as well as the effects of chemotherapy, other medications, and transfusions. When we compared either the overall incidence of abnormal results of liver-function tests or the incidence of more severe abnormalities in liver function, there were no differences between the fluconazole and placebo groups. However, the mean increase in the alanine aminotransferase level was greater with fluconazole than with placebo, a difference that suggests that fluconazole may affect the liver but in a way that is of uncertain clinical importance. Although we detected no excess in the incidence of severely abnormal results of liver-function tests among our fluconazole-treated patients, given the high background incidence of hepatic dysfunction, a low incidence of severe hepatotoxicity due to fluconazole would have been difficult to identify.
One source of concern about the use of any prophylactic antimicrobial agent is the potential for the selection or development of resistant organisms during therapy. Unfortunately, in vitro sensitivity testing of fungal isolates is not well standardized, and results do not always correlate with in vivo activity.21 For this reason, there was no systematic attempt to examine the susceptibility of fungal isolates to fluconazole, either before or after prophylactic therapy. We observed no excess of infections with resistant fungal species among fluconazole recipients. However, it should be mentioned that the average total duration of prophylaxis and follow-up was less than 40 days, and this may not have allowed the recognition of all such infections. Our studies of colonizing fungi isolated before and after prophylaxis showed a tendency toward the increased recovery of C. krusei during therapy with fluconazole. In addition, all three episodes of candidemia that we observed in patients receiving fluconazole were due to this species. The potential importance of these observations is underscored by a recent case report of C. krusei fungemia in a patient with neutropenia who was receiving fluconazole22 and by the reported increase of C. krusei colonization and infection that coincided with the adoption of fluconazole therapy at one transplantation center.23 However, the number of patients who became colonized or infected with C. krusei during our study was not significantly greater among patients receiving fluconazole than among those receiving placebo. Thus, there was no suggestion that fluconazole therapy actually led to C. krusei infections. The incidence of colonization with T. glabrata increased during the study in both groups. Although C. krusei and T. glabrata are not common causes of invasive fungal infections, the persistent colonization observed in fluconazole-treated patients is of potential concern and needs further study so that we can determine whether patients receiving longer-term fluconazole therapy or in other hospital environments may be at increased risk for such infections, particularly as fluconazole becomes more widely used.
The empirical use of amphotericin B, although common in both the fluconazole and placebo groups, was begun earlier and slightly more often among placebo patients. Because of the great excess of colonization with yeast among placebo recipients, such culture data, which were often available to the clinicians, may have been a factor in the earlier use of amphotericin B among patients receiving placebo. The reduction of systemic mycoses with fluconazole prophylaxis suggests that the early aggressive use of amphotericin B for persistent fevers in the neutropenic host should now be reevaluated in patients treated prophylactically with fluconazole. Although the aggressive empirical use of amphotericin B for persistent fevers in patients with neutropenia who are receiving antibacterial agents has been justified by the high incidence of fungemia in these patients,24 , 25 many such infections may now be prevented by treatment with fluconazole. Therefore, it may now be possible to test approaches in which, in the absence of fungal colonization or of clinical or pathological changes specifically suggestive of fungal infection, the empirical use of amphotericin B for neutropenic fevers is delayed or greatly reduced. This would spare patients considerable Clinical and renal toxic effects caused by amphotericin. Finally, the dose of fluconazole that we used, 400 mg daily, is greater than the dose of 100 to 200 mg that has been reported to be effective in treating serious candidal infections.5 This relatively high dose was chosen both because of the severe immunosuppression of this patient population and in the hope that it might offer some protection against aspergillus. This dose was well tolerated. However, given the low incidence of aspergillus infection during the study, we cannot comment on whether fluconazole affects the incidence of aspergillosis. Lower doses of fluconazole might be as efficacious as the dose studied, but higher doses might be more effective in preventing colonization or infection due to relatively resistant fungal organisms. We have yet to determine the optimal timing or duration of prophylaxis. Since infections with fluconazole-resistant fungi such as aspergillus, mucorales, and C. krusei will remain a problem in transplant recipients, continued clinical vigilance is required. The development of agents similar to fluconazole with respect to its reproducible bioavailability and safety, but with enhanced spectrums of antifungal activity, remains a priority. Our findings show that fluconazole protects against systemic infections by the most common fungal pathogens and support its use for routine prophylaxis in bone marrow transplantation.
Supported by grants from Pfizer Central Research.
We are indebted to our patients and many other members of the bone marrow transplantation teams, including physicians, nurses, and other health care professionals at the various medical centers, without whose willing participation this study would not have been possible; to Barton and Polansky Associates for providing studywide auditing and quality-control monitoring; and to Beth Wetak for assistance in the preparation of the manuscript.
Source Information
From the University of Minnesota Hospital and Clinics. Minneapolis (J.L.G., D.W.); UCLA Medical Center, Los Angeles (D.J.W., W.G.H.); University of Oklahoma Health Sciences Center Hospital, Oklahoma City (R.A.G.); Harper Hospital, Wayne State University, Detroit (P.H.C.); Ohio State University Hospital, Columbus (B.F.); Rush–Presbyterian–St. Luke's Medical Center, Chicago (H.K.); Montefiore Hospital, University of Pittsburgh School of Medicine, Pittsburgh (R.K.S.); University of California at San Diego Medical Center, San Diego (T.C.S.); Foster G. McGaw Hospital, Loyola University, Maywood, Ill. (P.S.); University of Texas Health Science Center, San Antonio (D.J.F.); Washington University Medical Center, St. Louis (W.G.P.); Hospital of the University of Pennsylvania. Philadelphia (J.L.S.); Westchester County Medical Center, New York Medical College, Valhalla (H.H.); Cleveland Clinic, Cleveland (A.L.); Vanderbilt University, Nashville (S.N.W.); Temple University Comprehensive Cancer Center, Philadelphia (K.F.M.); University of Michigan Medical Center, Ann Arbor (S.M.S.); and Pfizer Central Research, Groton, Conn. (G.G., D.B.). Address reprint requests to Dr. Goodman at Box 250 Mayo Bldg., University of Minnesota School of Medicine, Minneapolis, MN 55455.
Appendix
The following are additional participants in the study: University of Minnesota Hospital and Clinics, Minneapolis: D. Hermann, M.D., B. Kringstad, R.N., J. Harkness, R.N., A. Erdtman, D. Curtis, and D. Luke, Pharm.D.; UCLA Medical Center, Los Angeles: R.E. Champlin, M.D., and N. Kaufman, R.N.; University of Oklahoma Health Sciences Center, Oklahoma City: R.B. Slease, M.D., R.A. Saez, M.D., N. Sylvester, R.N., and D. Mentzer, R.N.; Harper Hospital, Wayne State University, Detroit: C. Gatny, R.N.; Ohio State University Hospital, Columbus: P. Tutschka, M.D., E. Copelan, M.D., N. Kapoor, M.D., J. Russell, R.N., and J. Malone; Rush–Presbyterian–St. Luke's Medical Center, Chicago: C. Richman, M.D., R. Ghalie, M.D., S. Adler, M.D., A. Korenblit, M.D., and S. Manson, M.S.N.; Montefiore Hospital, University of Pittsburgh School of Medicine, Pittsburgh: C.S. Rosenfeld, M.D., R. Gibbons, R.N., and M. Lowry; University of California at San Diego Medical Center, San Diego: B. Newton, R.N.; Foster G. McGaw Hospital, Loyola University School of Medicine, Maywood, Ill.: D. Koch, B.S.N.; University of Texas Health Science Center, San Antonio: Y. Medina; Washington University Medical Center, St. Louis: G. Herzig, M.D., R. Brown, M.D., M.T. Langlois, R.N., T. Hall, Pharm.D, T.C. Bailey, M.D., and L. Pineiro, M.D.; Hospital of the University of Pennsylvania, Philadelphia: G. Talbot, M.D., P. Cassileth, M.D., E. Stadtmauer, M.D., J. Scholtz, Pharm.D., J. Ball, Pharm.D., and A. Graziani, Pharm.D.; Westchester County Medical Center, New York Medical College, Valhalla: E. Feldman, M.D., T. Ahmed, M.D., G. Forseter, R.N., and T. Pace-Pouw, R.N.; Cleveland Clinic, Cleveland: B. Bolwell, M.D., S. Andresen, D.O., J. Weick, M.D., and A. Murar, R.N.; Vanderbilt University, Nashville: J.P. Greer, M.D., M. Thomas, R.N., and L. Jackson, R.N.; Temple University Comprehensive Cancer Center, Philadelphia: T.M. Cropper, P.A.-C; University of Michigan Medical Center, Ann Arbor: G. Messerschmidt, M.D., K. Hammelef, R.N., P. Jacobson, Pharm.D., J. Birk, and J. Douville; and Pfizer Central Research, Groton, Conn.: J. Jacobson, M.B.A., J. Schalhoub, R.N., L. Conway, and P. Wolejko.
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