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Previous Volume 329:1231-1236 October 21, 1993 Number 17 Next

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ABSTRACT

Background and Methods Few cases of overwhelming pulmonary blastomycosis associated with the adult respiratory distress syndrome have been reported. We describe 10 patients with this condition who were treated at one center in Wisconsin.

Results All 10 patients presented with fever, cough, and dyspnea; radiographic evidence of diffuse pulmonary infiltrates; and marked impairment of oxygenation. The mean alveolar-arterial oxygen gradient was 616 mm Hg. Six of the patients had no underlying disease associated with altered immunity, and two had no recent exposure to environmental reservoirs of Blastomyces dermatitidis. In all 10 patients, large numbers of broad-based budding yeasts were seen on microscopical examination of tracheal secretions. All patients were treated with intravenous amphotericin B (0.7 to 1.0 mg per kilogram per day). Of the five survivors, four received full doses of amphotericin B in the first 24 hours, and four required mechanical ventilatory support for 7 to 151 days. Long-term follow-up of three survivors showed good recovery of pulmonary function.

Conclusions Overwhelming infection with B. dermatitidis can cause diffuse pneumonitis and the adult respiratory distress syndrome, even in immunocompetent hosts. With prompt diagnosis by microscopical examination of tracheal secretions, intensive therapy with amphotericin B, and ventilatory support, good recovery of pulmonary function is possible.

Pulmonary blastomycosis characteristically causes an acute or chronic pneumonitis, in most cases with focal radiographic pulmonary infiltrates that occasionally cavitate^5,6. Disseminated granulomatous pulmonary infection causing severe impairment of gas exchange and a clinical and radiographic picture of the adult respiratory distress syndrome, although rare, has been reported with infection with Coccidioides immitis,^7,8 Histoplasma capsulatum,⁹ and Mycobacterium tuberculosis,^10,11 primarily in immunocompromised patients. Since 1983, we have treated 10 patients with overwhelming pulmonary blastomycosis associated with the adult respiratory distress syndrome. All the patients lived in Wisconsin or the Upper Peninsula of Michigan. Five of these patients survived after prompt diagnosis, immediate and intensive therapy with intravenous amphotericin B, and prolonged intensive care. We reviewed reports of 15 additional patients described in the literature,^{1,4,12,13,14,15,16,17,18,19,20,21} 3 of whom survived.

We describe the clinical and pathophysiologic findings in our 10 patients, including the results of long-term follow-up with pulmonary-function testing in 3 of the survivors, review the previously reported cases, and suggest an approach to the diagnosis and management of this syndrome.

Case Report

A 57-year-old man who had been in excellent health sustained a work-related contusion of his right elbow in February 1983; it was associated with persistent pain and swelling, but there were no abnormalities on radiographic examination. Ten days later, a nonproductive cough, chills, and fever (temperature as high as 39 °C) developed. Three days later, because of progressive dyspnea, the patient was admitted to a local hospital. A chest radiograph revealed diffuse pulmonary infiltrates. The white-cell count was 13,800 per cubic millimeter, with 79 percent segmented forms and 1 percent band forms. Despite treatment with antibiotics for presumed bacterial pneumonia, the patient's condition deteriorated, and on the fourth hospital day the partial pressure of arterial oxygen, with an inspired oxygen fraction (FIO₂) of 1.0 by non-rebreathing mask, was 57 mm Hg and the partial pressure of arterial carbon dioxide was 40 mm Hg. The patient was intubated and transferred to the University of Wisconsin Center for Trauma and Life Support.

Physical examination revealed no skin lesions, but the right elbow was swollen; no adventitious sounds were noted on auscultation of the chest, and there was no splenomegaly. Diffuse pulmonary infiltrates were seen on a chest radiograph (Figure 1A). A pulmonary-artery catheter was inserted and revealed a pulmonary-artery occlusive pressure of 10 mm Hg. On the second hospital day, large numbers of broad-based budding yeast forms were identified on a wet mount of tracheal secretions (Figure 2). Treatment was begun with intravenous amphotericin B at a dose of 100 mg (1 mg per kilogram of body weight) during the first 24 hours and daily thereafter, intravenous ketoconazole at a daily dose of 400 mg, and rifampin at a daily dose of 600 mg, administered by nasogastric tube. Ketoconazole and rifampin were discontinued after one week. Although yeast forms were detectable microscopically in the tracheal secretions until the 38th day of therapy, B. dermatitidis could not be recovered in culture after the 15th day. Fluid aspirated from the patient's elbow also grew B. dermatitidis in culture.

View larger version (47K): [in this window] [in a new window]   Figure 1. Chest Radiograph of Patient 1 on the First Day of Therapy (Panel A) and Two Years Later (Panel B).

 

View larger version (123K): [in this window] [in a new window]   Figure 2. Tracheal Secretions from Patient 1 (Panel A) and Tissue Obtained by Open-Lung Biopsy from Patient 2 (Panel B). In Panel A, a wet mount of tracheal secretions shows numerous large, broad-based, budding yeasts characteristic of B. dermatitidis (x400). In Panel B, the alveoli are packed with B. dermatitidis organisms (Gomori-methenamine silver, x200).

 
The patient received a total dose of 3000 mg of amphotericin B intravenously and required continuous positive-pressure mechanical ventilatory support for 50 days. His three-month hospital course was complicated by episodes of pneumothorax, intrapleural hemorrhage, Klebsiella pneumoniae bacteremia, acalculous cholecystitis, acute renal failure requiring hemodialysis, and the generalized polyneuropathy of the critically ill. The patient ultimately made a complete neurologic recovery, and his renal function returned to normal. He was sent home on the 75th day of hospitalization, and 4 months later returned to work full-time as a foreman in a locomotive-manufacturing plant.

Pulmonary-function testing one year after hospital discharge showed resolution of a severe restrictive defect, with normal diffusion capacity and lung volumes; exercise testing two years later showed no oxyhemoglobin desaturation after 9.5 minutes of cycling at 169 W. A chest radiograph obtained at this time showed residual scarring (Figure 1B). The patient worked full-time for seven more years before retiring in 1991.

Methods

The records of all patients with culture-documented pulmonary blastomycosis who had been hospitalized in our center since 1960 were reviewed. Ten patients, all of whom had been treated by one or more of the authors since 1983, presented with a clinical picture consistent with overwhelming pulmonary infection and radiographic findings of diffuse pulmonary infiltrates, but without evidence of congestive heart failure. All 10 patients had a partial pressure of arterial oxygen of 60 mm Hg or less with an FIO₂ of more than 0.50. Hemodynamic monitoring with a flow-directed, balloon-tipped pulmonary-artery catheter was used in the early care of nine patients. Eight of the nine had a pulmonary-artery occlusive pressure of 12 mm Hg or less, consistent with the presence of noncardiogenic pulmonary edema. All patients met the clinical criteria for the adult respiratory distress syndrome²².

Pulmonary function was tested in the early recovery period in all five surviving patients, and long-term follow-up studies were performed in three patients, one to four years after recovery from their illness. Autopsies were performed in four of the five patients who died.

Results

Clinical Features of the Patients

The clinical features of the 10 patients treated at the University of Wisconsin Center for Health Sciences are summarized in Table 1. There were four women and six men, ranging from 33 to 70 years of age. The average duration of illness before hospitalization was 25 days (range, 4 to 90), and the average length of time from initial hospitalization to the diagnosis of blastomycosis was 8 days (range, 2 to 13). Two of the patients had had no recent exposure to a plausible outdoor reservoir of B. dermatitidis; these cases are thought to represent reactivated latent infections.

View this table: [in this window] [in a new window]   Table 1. Summary of Clinical Data for 10 Patients with Overwhelming Blastomycosis Associated with the Adult Respiratory Distress Syndrome.

 
All 10 patients presented with fever, cough, and dyspnea, associated with profound impairment of oxygenation (mean alveolar-arterial oxygen gradient, 616 mm Hg). Hemodynamic data and the results of arterial blood gas measurements are shown in Table 2. The diagnosis was made in six patients by examining a wet mount of tracheal secretions. The diagnosis was made by open-lung biopsy in two, bronchoalveolar lavage in one, and biopsy of a skin lesion in one; however, examination of wet mounts of sputum from each of these patients after the diagnosis of B. dermatitidis infection had been established showed numerous yeast forms. The white-cell count was elevated in nine patients; one patient who had undergone renal transplantation had leukopenia on initial presentation. Nine of the ten patients had a marked leftward shift in the differential count.

View this table: [in this window] [in a new window]   Table 2. Initial Hemodynamic Data for Nine Patients.

 
All patients were treated with intravenous amphotericin B in a daily dose of 0.7 to 1.0 mg per kilogram; four of the five survivors received a dose of 1.0 mg per kilogram within the first 24 hours of therapy. Nine patients required intubation and controlled mechanical ventilation with volume-controlled, time-cycled ventilators and positive end-expiratory pressures ranging from 5 to 17.5 cm of water. Because of very high peak airway pressures, all were paralyzed with neuromuscular-blocking agents, and low tidal volumes with high respiratory frequencies were employed to keep airway pressures as low as possible and minimize the risk of barotrauma. One patient received inspiratory-pressure support ventilation through a face mask. Pneumothorax developed in three patients during mechanical ventilation, and three patients had multiple nosocomial bacterial infections. In one patient who had been making a steady recovery from the B. dermatitidis infection, overwhelming Enterobacter aerogenes pneumonia developed, and he died on the 38th hospital day. Acalculous cholecystitis developed in two patients, one on the 54th day of hospitalization after the patient had been successfully weaned from mechanical ventilation; the patient died of rupture of a gangrenous gallbladder associated with intraabdominal hemorrhage.

The five surviving patients have been followed for 1 to 10 years; none have relapsed, and all were asymptomatic at the most recent examination. The results of follow-up pulmonary-function testing 9 to 55 months after the acute infection are shown in Table 3 for three survivors. In Patient 1, forced vital capacity and total lung capacity were within the normal range 9 months after his illness, and this pattern was preserved 41 months after recovery; the diffusion capacity was slightly decreased at 9 months but was within the normal range at 41 months. Fifty-five months after the infection, Patient 2 had reduced vital capacity and total lung capacity (64 percent of predicted values) and subnormal diffusion capacity (74 percent of predicted values), all of which correlated with the persistence of extensive destructive changes and interstitial markings on chest radiographs obtained during convalescence. In Patient 10, lung volume and diffusion capacity were normal 11 months later. None of the three patients tested had resting hypoxemia or oxyhemoglobin desaturation during vigorous exercise.

View this table: [in this window] [in a new window]   Table 3. Follow-up Pulmonary-Function Testing in Three Survivors of Overwhelming Pulmonary Blastomycosis with the Adult Respiratory Distress Syndrome.

 
Roentgenographic Features

In 7 of the 10 patients, diffuse, bilateral, interstitial alveolar infiltrates were seen at the outset (Figure 1); in 3 patients, diffuse infiltrates appeared shortly after admission to the hospital. One patient had a pleural effusion early in his illness, before the initiation of mechanical ventilation. In the survivors, the generalized infiltration cleared, but focal areas of interstitial fibrosis were evident up to five years later (Figure 1B).

Pathological Findings

Postmortem lung tissue was available from four of the five patients who died, and open-lung-biopsy specimens were available from one survivor and one nonsurvivor. The gross and microscopical findings in each case were similar: dense consolidation of the parenchyma was associated with numerous small, firm, yellow nodules scattered throughout the lobes. Microscopically, alveolar spaces were packed with large numbers of characteristic large, broad-based, budding yeasts, with relatively minimal infiltration by inflammatory cells (Figure 2B); hyaline membranes consistent with the presence of adult respiratory distress syndrome were also seen. All lung specimens yielded B. dermatitidis in culture, and cultures of blood and spleen obtained at autopsy from two patients were also positive; B. dermatitidis grew from a culture of liver tissue from one patient.

Summary of the Cases in the Literature

Table 4 summarizes the demographic, epidemiologic, and clinical findings in 25 patients with overwhelming pulmonary blastomycosis presenting with the adult respiratory distress syndrome described in the world literature since 1968,^{1,4,12,13,14,15,16,17,18,19,20,21} including our 10 patients. Other reports of patients with overwhelming pulmonary blastomycosis and the adult respiratory distress syndrome^23,24 provided insufficient data to be included in this review.

View this table: [in this window] [in a new window]   Table 4. Features of Overwhelming Pulmonary Blastomycosis Associated with the Adult Respiratory Distress Syndrome in 25 Patients Described in the Medical Literature.

 
This syndrome has been identified primarily in middle-aged patients (mean age, 49 years), with men afflicted only slightly more frequently than women (14 men vs. 11 women). Less than half the patients had serious underlying diseases (11 of 25, 44 percent), and only 7 (28 percent) were known to be immunocompromised. In at least four patients, overwhelming B. dermatitidis infection appeared to represent a reactivated latent infection. All 25 patients resided in areas in which blastomycosis is endemic or had recently visited such areas before the onset of their illness. B. dermatitidis infection was confirmed by culture in 23 of the 25 patients.

Most patients presented with fever (84 percent), cough (68 percent), or dyspnea (68 percent), and all had radiographic evidence of generalized pulmonary infiltration consistent with the presence of the adult respiratory distress syndrome. Although a premortem diagnosis was made by bronchoscopy or open-lung biopsy in 10 patients, in 20 of 21 patients (95 percent) whose sputum was reported to have been examined microscopically, large, broad-based, budding yeasts characteristic of B. dermatitidis were seen microscopically in a wet-mount preparation.

Only 8 of the 25 patients survived (32 percent) -- 5 of our series of 10 patients treated at the University of Wisconsin Center for Health Sciences since 1983 and 3 of 15 described previously^16,20,21. All survivors received at least 20 mg of intravenous amphotericin B per kilogram and a total dose of 2000 to 3000 mg; all received a daily maintenance dose of at least 0.7 mg per kilogram. Seven of the eight survivors required prolonged mechanical ventilatory support (mean, 40 days; range, 7 to 151).

Discussion

We describe 10 patients with culture-documented, overwhelming pulmonary blastomycosis who presented with the adult respiratory distress syndrome. The adult respiratory distress syndrome is a rare manifestation of granulomatous pulmonary infection, but does occur in patients with disseminated coccidioidomycosis,^7,8 histoplasmosis,⁹ and M. tuberculosis infection^10,11. Although a diffuse infiltrative pattern on chest radiographs is a rare manifestation of pulmonary coccidioidomycosis in immunocompetent patients, most patients with the acquired immunodeficiency syndrome (AIDS) who are infected by C. immitis have radiographic evidence of diffuse infiltrates and clinical evidence consistent with a diagnosis of the adult respiratory distress syndrome⁸. Recently, pulmonary blastomycosis in patients with AIDS has often been associated with a diffuse or miliary radiologic pattern²⁵.

Except for 3 cases reported between 1968 and 1976,^12,13,14 pulmonary blastomycosis as a cause of the adult respiratory distress syndrome has been described relatively recently; since 1979, there have been 12 reported cases^{1,4,15,16,17,18,19,20,21}. Stringent hemodynamic criteria for the adult respiratory distress syndrome were not provided in most of these case reports, but the patients were considered to have noncardiogenic pulmonary edema on clinical grounds. In more than half the reported patients, the diagnosis was not made until the patient was moribund^{1,4,12,13,14,15,16,17,19,20} or until autopsy^4,17,18. Our experience with 10 cases since 1983 -- all identified before death -- and these recent reports indicate that B. dermatitidis has the capacity to produce overwhelming pulmonary infection with widespread systemic dissemination, in both immunocompromised and immunocompetent patients.

B. dermatitidis is one of the most commonly identified pulmonary mycoses in the United States that requires systemic treatment with antifungal drugs. An epidemiologic study of blastomycosis in Wisconsin suggests that the incidence of this infection in our state has been increasing over the past two decades²⁶. Moreover, six outbreaks of acute pulmonary blastomycosis have been reported since 1972^{27,28,29,30,31,32,33} and three since 1980, all in Wisconsin, that have been linked epidemiologically and microbiologically to an environmental reservoir of B. dermatitidis^31,32,33. An analysis of the voluntary reporting of deaths due to blastomycosis to the Centers for Disease Control and Prevention, the recent reports in the literature,^{1,4,12,13,14,15,16,17,18,19,20,21} and our experience suggest that the incidence of overwhelming pulmonary blastomycosis with the adult respiratory distress syndrome is increasing nationwide.

Clearly, all cases of symptomatic pulmonary blastomycosis do not originate from acute infection produced by the inhalation of B. dermatitidis, and acute pulmonary infection may also derive from the reactivation of a latent infection^1,2,34,35. Two of our patients and two patients described previously had no exposure to potential reservoirs of B. dermatitidis, such as a wooded or swampy area,^32,33 in the years before becoming ill, and their illnesses are thought to represent reactivated infections.

The syndrome we report is indiscernible from overwhelming bacterial sepsis with the adult respiratory distress syndrome, but its cause can be easily established by microscopical examination of tracheal secretions. All our patients had large numbers of broad-based budding yeasts on microscopical examination (wet mounts) of aspirated tracheal secretions. For patients who do not have characteristic yeast forms in tracheal secretions, specimens obtained by bronchoscopic biopsy or bronchoalveolar lavage³⁶ would be very likely to contain the organism on microscopical examination with the use of appropriate stains (toluidine blue or Gomori-methenamine silver). Examination of lung tissue from 6 of our patients and 11 of the 15 patients described in the literature^{4,12,13,14,15,17,18,19,20} revealed diffuse pyogranulomatous inflammation with massive infiltration of alveolar spaces by large numbers of B. dermatitidis organisms (Figure 2B). Hyaline membranes and other histopathological changes characteristic of the adult respiratory distress syndrome were seen in lung specimens from our patients and in five patients described in previous reports^17,18,19,20.

The syndrome we describe mandates an aggressive approach to therapy, with the dose of amphotericin B increased as rapidly as possible -- within 24 to 48 hours -- to a daily maintenance dose of 0.7 to 1.0 mg per kilogram (or a maximum of 70 mg). Our sickest patient who survived (Patient 1), who weighed 110 kg, was given 100 mg within the first 24 hours after the diagnosis was made and received this dose for 30 consecutive days. Of the 25 patients, all 8 surviving patients^16,20,21 received at least 20 mg of intravenous amphotericin B per kilogram.

Four of our five patients who survived required prolonged continuous positive-pressure mechanical ventilation with positive end-expiratory pressure and the use of a Swan-Ganz catheter³⁷; they also required paralytic agents to optimize ventilation and reduce the risk of barotrauma. Nonetheless, life-threatening pneumothorax complicated the course in three patients, so strategies to minimize the risk of barotrauma associated with mechanical ventilation should be employed, such as using lower tidal volumes or pressure-controlled ventilation to minimize peak inspiratory pressures³⁸. Although this syndrome produces devastating acute physiologic impairment, survivors appear to have a good prognosis for the recovery of pulmonary function.

Source Information

From the Sections of Pulmonary and Critical Care Medicine (K.C.M.) and Infectious Diseases (E.J.M., D.G.M.), Department of Medicine, and the Center for Trauma and Life Support (K.C.M., D.G.M.), University of Wisconsin Medical School, Madison. Presented in part at the Annual Meeting of the American Thoracic Society, Las Vegas, May 11, 1988, and the 28th Interscience Conference on Antimicrobial Agents and Chemotherapy, Los Angeles, October 25, 1988.

Address reprint requests to Dr. Maki at the University of Wisconsin Hospitals and Clinics, H4/574, Madison, WI 53792.

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