Clinical Significance of Pseudallescheria boydii: A Review of 10 Years' Experience

LOIS B. TRAVIS, M.D. , Resident in Pathology*; GLENN D. ROBERTS, Ph.D., Section of Clinical Microbiology, Department of Laboratory Medicine; WALTER R. WILSON, M.D. , Section of Clinical Microbiology, Department of Laboratory Medicine and Division of Infectious Diseases

Pseudallescheria boydii is a recognized cause of mycetoma, a chronic fungal disease that usually affects the extremities. Isolated case reports have also implicated P. boydii in infections of other sites. We report the first large series (83 isolates) of P. boydii in 46 patients, including the second report of P. boydii brain abscess and disseminated infection in a noncompromised host. Between 1974 and 1984 at our institution, P. boydii was cultured from a variety of sites: respiratory tract, 36; soft tissue, 25; bone, 9; gastric aspirate, 4; maxillary sinus, 2; wound, 2; urine, 2; brain abscess, 1; ear, 1; and toenail, 1. Pulmonary colonization proved to be the most common form of pseudallescheriasis of the lung (34 of 36 cultures in this category); 28 of the 32 patients with pulmonary infections had received immunosuppressive therapy or had an underlying disorder. The importance of isolation of P. boydii from bone and soft tissue is supported in this series because all 9 cultures from bone and 21 of 25 cultures from soft tissue were associated with infection. Of 10 cases of infection, 5 were osteomyelitis and 2 were infected wounds; in addition, maxillary sinusitis, disseminated infection, and a lung abscess occurred in 1 patient each.

Pseudallescheria boydii was first recovered from the ear of a child with chronic otitisexterna.1 Since the report of that first case, it has been implicated in infections of many other anatomic sites. This organism has been identified in specimens from pulmonary cavities2 5 and in patients with necrotizing pneumonia,6,7 pulmonary infiltrates,8

asymptomatic coin lesions,9 pleural f luid,10 and pulmo­nary sarcoidosis." In addition, P. boydii has caused sinusit is, , 2 '1 8 corneal infections,19"22 endophthal-mitis,23'24 parotitis,3 skin infections,25 arthritis,23'26"28 os­teomyelitis,26'29 brain and thyroid abscesses,6'23'30'33 en­docarditis,34,35 chronic otitisexterna,36'37 chronic prosta-titis,38 and disseminated infections.23'39'43

P. boydii is also a cause of mycetoma, a chronic, suppurative fungal infection usually of the extremities. Mycetoma occurs more commonly in rural than in urban areas and more frequently in men than in women, per­haps because of the usually greater outdoor activity of men and the occurrence of P. boydii in nature. The organism has been isolated from soi l ,4 4 4 6 poultry and cattle manure,47 polluted streams,48 and coastal waters.49

*Mayo Graduate School of Medicine, Rochester, Minnesota.

Address reprint requests to Dr. G. D. Roberts, Section of Clinical Microbiology, Mayo Clinic, Rochester, M N 55905.

Pseudallescheria infections other than mycetoma are usually associated with immunosuppressive therapy, ma­lignant lesions, or other underlying disorders.

The purposes of this report are to describe the impor­tance of P. boydii recovered from clinical specimens and to review our experience with clinically significant P. boydii infections.

MATERIAL AND METHODS All specimens submitted for culture were inoculated onto inhibitory mold agar; brain-heart infusion agar that con­tained 10% sheep blood, 5 μg/ml of gentamicin, and 16 μg/ml of chloramphenicol; brain-heart infusion agar that contained 10% sheep blood, 5 μg/ml of gentamicin, 16 μg/ml of chloramphenicol, and 500 μg/ml of cyclo-heximide; and Sabouraud's 2% dextrose agar. Cultures were incubated at 30°C for 30 days. Previously reported methods were used to identify isolates of P. boydii on the basis of morphologic features.50

Between March 1974 and January 1984 in the Clinical Mycology Laboratory at our institution, 83 isolates of P. boydii were recovered from 46 patients (Table 1). The clinical significance of a positive culture was determined by reviewing the medical records of these patients. P. boydii caused a clinically significant infection in 10

Mayo Clin Proc 60:531-537, 1985 531

532 PSLUDALLLSCHERIA BOYDII Mayo Clin Proc, August 1985, Vol 60

Table 1.—Recovery of Pseudallescheria boydii From Clinical Specimens

Source

Respiratory tract Soft tissue Bone Gastric aspirate Sinus (maxillary) Wound Urine Brain abscess External auditory canal Toenail

No. of isolates

36 25

9 4 2 2 2 1 1 1

No. of patients*

32 7 5 3 2 2 1 1 1 1

No. with underlying

disorder or immuno-suppressive

therapy

28 0 0 2 1 1 0 0 0 0

Clinical significance of isolates

(no. of patients)

Coloni­zation

30 2 0 3 1 0 0 0 1 1

Infectiont

2 5 5 0 1 2 1 1 0 0

*P. boydii was recovered from 46 patients; several patients had multiple cultures or recovery from multiple sites (or both).

tOverall, 10 patients had clinically significant infections; 4 patients had either multiple sites or multiple cultures positive (see Table 2 for details).

patients, and tissue specimens were available for review in 5 of them (cases 3 through 7). Methenamine silver-stained sections of tissue from four patients (cases 3, 4, 6, and 7) had fungal elements consistent with those of P. boydii (Fig. 1). Fungi were not seen in the tissue speci­mens of one patient (case 5); however, this patient had 18 positive P. boydii cultures from bone or soft tissue during a 6-month period.

CULTURE RESULTS The time from submission of the 83 cultures to identifica­tion of P. boydii ranged from 2 to 30 days (median, 10 days). Of these specimens, 36 (43%) were from the respiratory tract, 25 (30%) from soft tissue, 9 (11 %) from bone, and 13 (16%) from other sites (Table 1). Of the 36

Fig. 1. Appearance of Pseudallescheria boydii on tissue section. (Methenamine silver stain; x 500.)

cultures (from 32 patients) from the respiratory tract, 34 (94%) represented colonization and 2 (6%) were clini­cally significant (Table 2). Of the 30 patients with col­onization, 26 (87%) had underlying pulmonary disease and 5 (17%) were receiving corticosteroid therapy; in all 30 patients, other fungal species were isolated con-comitantly with P. boydii. Of these 30 patients, 22 had follow-up examinations from Vi month to 9 years later (median, 2 years). Thirteen patients remained alive with­out P. boydii pulmonary disease, and nine died of causes unrelated to P. boydii infection.

All 9 cultures positive for P. boydii from bone and 21 of 25 cultures (84%) from soft tissue were associated with infection. The remaining four positive cultures from soft tissue represented colonization in two patients who had sustained trauma and had wounds contaminated with soil.

The four isolates of P. boydii recovered from gastric aspirates of three patients were considered contaminants or colonizers. P. boydii was also recovered from the sputum of two of these patients. A chest roentgenogram in one patient demonstrated pneumonitis, which was later confirmed as Haemophilus influenzae pneumonia; he has remained well for 6 years. In the other patient, who had diffuse large cell lymphoma and squamous cell carcinoma, tuberculosis developed, and P. boydii was recovered from two gastric aspirates and sputum speci­mens. This patient died after 6 months.

One of the maxillary sinus isolates and both wound isolates were responsible for infection. The isolates from urine and the brain abscess and one of the isolates from the respiratory tract were recovered from one of the patients (case 1). The P. boydii organisms recovered from

Mayo Clin Proc, August 1985, Vol 60 PSEUDALLESCHERIA BOYDII 533

Table 2.—Profile of Patients With Infection Caused by Pseudallescheria boydii*

Case

1

2

3

4

5

6

7

8

9

10

Age (yr) and

40

43

18

3

16

20

59

47

46

64

sex

M

M

M

M

M

M

F

M

F

M

Occupation

Farmer

Farmer

Farmer

Farmer

Cafeteria manager

Farmer

Nurse's aide

Positive P. boydii

A n , o , . ~ w cultures

trauma

Yes

Yes

Yes

Yes

Yes

Yes

N A t

No

No

No

Site(s) No.

Urine Sputum

Brain abscess

Bone

Bone

Bone Soft

tissue Bone

Soft tissue

Bone

Soft tissue

Respiratory

Maxillary sinus

Wound

Wound

2 1

1 1

1

3

3 3

15

1

3 1

1

1

1

Other organisms present

None Pseudomonas

aeruginosa

None Group D strep­

tococci

None

None

None P. maltophilia,

Enterobacter agglomerans, P. aeruginosa

Scopulariopsis species, group D streptococci, viridans strep­tococci, Bacillus species, Staphylococcus epidermidis

None

None None

Citrobacter freundii

S. epidermidis

Proteus mirabilis

Diagnosis

Disseminated pseudall-escheriasis

Osteomyelitis

Osteomyelitis

Osteomyelitis

Osteomyelitis

Osteomyelitis

Lung abscess

Sinusitis

Infected lumbar wound

Infected axillofemoral graft

Treatment

Miconazole

Surgical resection, miconazole, ketoconazole

Clotrimazole, below-knee amputation

Incision and drainage

Amputation

Amputation

Surgical procedure

Surgical procedure

Debridement

Surgical procedure

Outcome

Died

No evidence of recurrence

Cure

Cure

Cure

No evidence of recurrence

Cure

Cure

No evidence of recurrence

No evidence of recurrence

Duration of fol low-up

4 mo

22 mo

5 y r

7 y r

38 mo

8 mo

18 mo

22 mo

15 mo

9 mo

•None of these patients had received corticosteroid therapy; one patient (case 10) had diabetes mellitus. +NA = not applicable.

the external auditory canal and a toenai l were considered colonizers.

REPORT OF CASES

The 10 cases of c l in ica l ly signif icant P. boydii infect ion

are summarized in Table 2. Add i t iona l detai led in forma­

tion is provided for six of these cases.

Case 1.—A healthy 40-year-old farmer fell into a hog manure pit and was discovered 45 minutes later. He had aspirated animal fecal material and was unresponsive. Shortly after he was hospital ized elsewhere and intubated, acute respiratory distress syndrome developed as a result of aspiration pneumoni t is . Dur ing the next 6 days, his condit ion improved, and he was extubated and transferred f rom the intensive care uni t . O n e week later, lethargy and

534 PSEUDALLESCHERIA BOYDII Mayo Clin Proc, August 1985, Vol 60

confusion developed; an initial computed tomographic scan of the head reportedly showed normal f indings. Sev­eral days later, a repeat tomographic study showed bif ront-al cerebral abscesses, which appeared enlarged on subse­quent studies. Twenty-six days after the initial event, P. boydii was recovered f rom a frontal brain abscess, which had been drained through a bur hole.

The patient was transferred to our medical center; on admission, a computed tomogram of the head showed multiple brain abscesses (Fig. 2). A chest roentgenogram revealed infiltrates in the right lung base and left mid lung field and b lunt ing of the left costophrenic angle by f lu id (Fig. 3). Endotracheal cultures yielded Pseudomonas aer-uginosa and P. boydii. Two ur ine cultures yielded P. boydii only; b lood cultures were negative.

Fig. 2 (case 1). Computed tomogram of head, showing multiple brain abscesses.

Therapy wi th dexamethasone sodium phosphate (Deca-dron) , ch lo ramphen ico l , and intravenously and intra-thecally administered miconazole was ini t iated. Because of potential contaminat ion of the ventricular f lu id wi th P. boydii, an Ommaya reservoir was not inserted. After 1 week of therapy, the patient was transferred to a hospital in his hometown at the request of his family. A l though the aforementioned therapeutic regimen was cont inued, the patient died approximately 3 months later.

Case 2.—After a healthy 43-year-old farmer stepped on a nail, he was treated w i th one intramuscular inject ion of

Fig. 3 (case 1). Chest roentgenogram, showing infiltrates in base of right lung and in left midlung field and blunting of left costophrenic angle because of fluid.

penicil l in C procaine, tetanus prophylaxis, and irrigation of the wound . Six weeks later, osteomyelit is was diagnosed. He was treated first w i th intravenously administered anti­biotics fo r4 days and then wi th orally administered cloxacil-l in , after which he was referred to our inst i tut ion.

The left four th and f i f th metatarsophalangeal joints were resected, and P. boydii was recovered f rom cultures of specimens obtained intraoperatively. Miconazole was ad­ministered intravenously for 14 days, fo l lowed by keto-conazole administered orally f o r4 months. The patient had no recurrence of infect ion dur ing 22 months of fo l low-up.

Case 7.—A healthy 59-year-old female cafeteria manager was referred to our medical center for evaluation of an asymptomatic lung nodule noted on routine chest roent-genography. Sputum cultures were negative. Histologie examinat ion of a pu lmonary specimen obta ined f rom wedge resection of the posterior segment of the right upper lobe disclosed an inf lammatory abscess, which yielded a pure cul ture of P. boydii. No antifungal therapy was administered, and infect ion d id not recur dur ing an 18-month fo l low-up per iod.

Case 8.—A 47-year-old farmer w i th no known underly ing disease had a 5-year history of right supraorbital head­aches. He had been treated elsewhere wi th antibiotics and antrat i r r igat ion for s inusi t is , but the symptoms had persisted.

Subsequently, a Caldwell-Luc procedure and intranasal antrostomy were performed at our inst i tut ion. Cultures of specimens obtained intraoperatively yielded P. boydii and Citrobacter freundii. The patient received neither antibiot­ics nor antifungal therapy, and sinusitis did not recur dur­ing a 22-month fo l low-up interval.

Case 9.—A healthy 46-year-old female nurse's aide had undergone a partial hemilaminectomy elsewhere 3 weeks before being transferred to our clinic for treatment of a subsequent wound infect ion. Cultures of specimens ob­tained dur ing debr idement yielded P. boydii and Staphylo-coccus epidermidis. The patient received no antifungal

Mayo Clin Proc, August 1985, Vol 60 PSiUÜALLLSCHLMA UOYDII 5.J5

therapy; the infection did not recur during 15 months of follow-up.

Case 10.—In a 64-year-old man with insulin-dependent diabetes, an axillofemoral graft became infected 9 months after a surgical procedure had been performed elsewhere. The infected graft was resected at our institution, and cultures of the graft yielded P. boydii and Proteus mirabilis. The involved extremity was revascularized by placement of a graft in an extra-anatomic position through uninfected tissue planes. No evidence of recurrence of infection was noted at follow-up 9 months later.

DISCUSSION Only 10 previous reports have described substantiated P. boydii in fec t ion of the centra l nervous sys­tem. ''·«'-! ! ' ! , ,-42-' i l- ' ; i In one of these cases, meningitis had resulted from contamination of the cerebrospinal fluid during spinal anesthesia.5' Granulomatous meningitis occurred in a second, presumably healthy, patient.''2 The third case of P. boydii infection was associated with pansinusitis in a woman with diabetes.Si Brain abscesses were diagnosed in the remaining seven patients, six of whom had received immunosuppressive therapy for se­vere underlying illnesses.0, !C)"i2'!l)'42 The seventh patient had aspirated river water and mud in a diving accident. Seven weeks later, P. boydii was recovered from brain abscess cultures and from cultures of the river water. Although the patient was treated with miconazole, death ensued 4 months after the accident."

Similarities exist between this last-mentioned case and our case 1. Both patients were previously healthy and had accidents during which they aspirated vegetative material. Although initial computed tomograms of the head showed normal findings, cerebral abscesses be­came apparent later during the hospital course. Neither patient responded to miconazole therapy, and both died approximately 4 months after the accident.

Only one of the seven previously described patients with brain abscess survived.'2 The patient, a 3-year-old boy with acute lymphoblastic leukemia, was treated with surgical drainage and amphotericin B. The P. boydii recovered from this patient was resistant in vitro to am­photericin B, and the successful outcome was probably attributable to the surgical drainage. P. boydii frequently exh ib i t s in v i t r o res is tance to a m p h o t e r i c i n B w.u. i iMM.« f | u c y t o s J n e 2 i a n d chloramphenicol.56

Some isolates are m o d e r a t e l y suscep t i b l e to miconazole'2' l 4 ' 2 U 0 or ketoconazole.27 2H In patients with brain abscess, surgical drainage is probably more effec­tive than chemotherapy.

Case 2 (described in detail) is representative of our four other patients (cases 3 through 6) who had P. boydii osteomyelitis. All five patients were previously healthy

males, lived in rural areas (three were farmers), sustained traumatic injuries that caused contamination with soil or vegetative material, and underwent surgical debride-ment or amputation for infection with P. boydii. In one patient (case 3), previous treatment with debridement and two courses of clotrimazole during a 3-year period had been unsuccessful. Eventually, amputation of the involved extremity was necessary. Three of these patients (cases 4, 5, and 6) received no antifungal therapy. In previous reports,20'2'''r'7 four patients with P. boydii osteo­myelitis responded to surgical debridement (or resection) and miconazole therapy. A fifth patient did not respond to miconazole therapy; with ketoconazole therapy, his associated cutaneous fistulas healed, but findings on bone scans and radiographs were unchanged.SH A sixth patient responded to surgical resection and ketoconazole therapy.M The specific contribution of antifungal therapy to the outcome of these patients is difficult to assess. In selected cases, antifungal chemotherapy may be a useful adjunct to surgical debridement or amputation.

Most P. boydii isolates from pulmonary specimens are colonizers.'4 In a review of pulmonary pseudallescheria-sis, Jung and associates1'0 considered surgical resection the treatment of choice for patients with localized cavi­tary lesions. They concluded that preoperative and post­operative antifungal chemotherapy was unnecessary. Our patient with pulmonary involvement (case 7) un­derwent surgical resection without antifungal therapy and had no further evidence of infection during 18 monthsof follow-up. Galgiani and associates'" described five patients with pulmonary infections, two of whom were refractory to ketoconazole therapy and were subse­quently cured by surgical resection. (One of these pa­tients had a cavitary lesion.) The other three patients responded to ketoconazole therapy alone.

In three previous case repor ts , ' ' " ' 1 8 P. boydii sinusitis in otherwise healthy persons has been described. One patient with maxillary sinusitis recovered with surgical treatment only. '8 A second patient had sphenoidal sinus­itis with intracranial involvement and died despite sur­gical drainage and treatment with amphotericin B and miconazole."' The third patient, who had sphenoidal sinusitis, recovered after transseptal sphenoidotomy and miconazole therapy.1'' Our patient with maxillary sinus­itis recovered after debridement only.

Four cases of P. boydii sinusitis in immunocompro-mised patients have been reported.12 u , / Two patients with maxillary sinusitis were reportedly cured with sur­gical treatment o n l y . " 1 ' A third patient died despite therapy with amphotericin B, flucytosine, and chloram­phenicol.14 The fourth patient, who had maxillary, eth­moid, and sphenoid sinusitis, showed improvement on

536 PStUDALLESCHERIA BOYDII Mayo Clin Proc, August 1985, Vol 60

amphotericin B therapy but died 4 months later of under­lying disease.12

ACKNOWLEDGMENT We thank Roberta M. Kondert for secretarial assistance.

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