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The role of surgery in the management of pulmonary monosporosis
The role of surgery in the management of pulmonary monosporosis A collective review Nine cases of pulmonary monosporosis treated in the Missouri State Chest Hospital over a period of 19 years (1956 to 1975) were reviewed. Nine other cases from the literature are summarized. Ten of these 18 patients underwent resectional operations with two operative deaths, one from respiratory insufficiency and the other from a bronchopleural fistula and massive hemorrhage. The rest of the patients had an uneventful recovery. The indications for resectional surgery are re-established for suitable cases. The underlying disease is the major determinant of the outcome of the surgery. Other modes of treatment are also discussed. Based on the analysis of these 18 cases, a guideline for the management of pulmonary monosporosis is proposed.
J. Y. Jung, M.D., Rafael Salas, M.D., Carl H. Almond, M.D., Salim Saab, M.D., and Roberto Reyna, M.D., Columbia, Mo.
IT ulmonary monosporosis is a rare pulmonary fungal infection. The fungus, Monosporium apiospernum, is most often isolated from the pathological lesion of cutaneous and subcutaneous tissue of the foot— maduromycosis. Deep mycotic infection other than lung has also been recognized, such as otomycosis,1 septicemia,2 meningitis,3 and endophthalmitis.4 Primary pulmonary infection has been reported off and on in the last two decades, mostly in the form of single case reports. The purpose of this communication is to present our experience with nine cases diagnosed and treated at the Missouri State Chest Hospital. Review of the literature is also made in order to summarize the over-all experience and attempt to formulate guidelines of management. Clinical data Between December, 1956, and August, 1975, nine cases of pulmonary monosporosis were diagnosed at From the Department of Thoracic and Cardiovascular Surgery, University of Missouri Medical Center, and the Department of Surgery, Missouri State Chest Hospital. Received for publication June 30, 1976. Accepted for publication July 23, 1976. Address for reprints: Carl H. Almond, M.D., Professor and Chief of Thoracic and Cardiovascular Surgery, University of Missouri Medical Center, Columbia, Mo. 65201.
the Missouri State Chest Hospital. The first three cases were reported previously by Reddy and associates5 from this institution in 1969. Since then, six additional cases were identified. The criteria for diagnosis were: (1) Repeated isolation of the fungus, M. apiospermum, in the sputum cultures. In order to avoid the contaminant, precaution was taken in the collection of sputum and in the subsequent isolation in the laboratory. Arbitrarily, at least four positive cultures per patient were considered to be significant to be included in this report. Our laboratory has recovered M. apiospermum from sputum in many patients on one or two occasions. Because of its questionable significance, they are not included in this series. (2) Identification and growth of the fungus from the excised surgical specimen. (3) Positive cultures and growth from the specimen obtained from the bronchial washing or selective brushing from the pulmonary lesions through the fiberoptic bronchoscope. (4) Evidence of tissue invasion in tissue sections. There were five men and four women, a ratio of 1.25:1; their ages ranged from 52 to 81 years. Of interest, all nine patients were long-time rural residents. Eight of them were either farmers or farmers' wives. One patient was a baker who had worked in a small-town bakery. All patients underwent complete evaluation. This included tuberculin skin tests, skin test 139
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1 4 0 Jung et al.
Table I. Summary of nine cases of pulmonary monosporosis (Missouri State Chest Hospital) Case No. Age Sex
Profession
Symptoms
Wife of Fever, chills, farmer productive cough Wife of Productive cough farmer
X-ray findings
Sputum culture
1 1956
52
F
2 1963
77
F
3 62 1967
M
64 4 1969
M
73 5 1969
M
6 1969
60
F
Baker
7 1971
67
F
Monosporium Farmer's Hemoptysis, LLL infiltrate bronch - (+) x 4 wife fever, chills iectasis
8
60
M
Farmer
Chest pain, hemoptysis
Honeycomb, LU lobe
9 81 1975
M
Farmer
Mild cough
LLL infiltrate
Monosporium Cylindrical bronchi(+) ectasis, RUL Monosporium Infiltrate both apices x4(+)
Monosporium Plumber, Hemoptysis, Extensive farmer weight loss, infiltrate (+) weakness and bronchi ectasis cavities, fungus ball X 2, rt. lung Farmer Weakness, Rt. hilar Monosporium chest pain, mass (+) wt. loss Farmer Chest pain, Rt. complete Monosporium hemoptysis opacity, (+) LLL infil.
None
RUL infiltrate
Associated lesion
Treatment
Culture of surgical specimen
Follow-up
RU lobectomy Positive Living and well, for mono last seen in 1968 sporium COPD, chronic None Left hospital — A.M.A., last bronchitis seen in 1968, living and well Continues to be Tbc. far adv., Rt. pneumoPositive nectomy for mono positive in inactive sporium sputum after surgery but well in 1971 Tbc. inactive, RUL
Anaplastic ca. rt. lung
Thoracotomy, inoperable tumor Tbc. far adv., Amphotericin inactive; D.N B, sputum severe respir. became neg. insufficiency
Monosporium M. kansasii neg. infection
—
Died; no autopsy
—
Became positive for monosporium in 1971; died with respiratory failure RU lobectomy Positive M. intracellulare inf., for mono readmitted sporium Antibiotic for Last seen 1975, — good condition pseudomonas
Bronchiectasis LLL, pseudomonas infect. Monosporium T b c , L U L LU lobectomy Positive Sputum continues amphotericin for mono- ( + ) for mono(+); B sporium after TB (+) sporium surgery Geotrichum COPD, chronic Iodide, amLiving and well — (+); monobronchitis photericin B at present sporium (+)
for histoplasma and aspergillus, sputum smears for AFB, fungi, sputum cultures, and bronchoscopic examination. After 1973, selective brushing through the fiberoptic bronchoscope under fluoroscopic control was added to the diagnostic armamentarium. The latter technique was applied in Case 9 to obtain the positive cultures. Clinical symptoms were variable, from none to hemoptysis and general debilitation. Among them, hemoptysis is the most common presenting symptom (44.4 per cent). Other symptoms include productive cough, weight loss, fatigue, and dyspnea. PPD skin test was positive in all patients. Radiologic abnormalities of the lung ranged from pulmonary infiltrates to cavitary lesions containing fungus ball. In Cases 2,
6, and 9, only pulmonary infiltrates were demonstrated. Bronchiectasis was shown in Cases 1 and 7 by means of bronchogram. Case 4 displayed only the right hilar mass. Cases 3, 5, and 8 presented with multiple cavitary lesions. Fungus ball or mycetoma was found in the cavities in Cases 3 and 8. The lesion was located in the upper lobe in three cases: two in the right and one in the left. The left lower lobe was involved in three cases, the entire right lung in two. One patient had a right hilar mass which later proved to be an undifferentiated carcinoma on thoracotomy. Pleural effusion was present in one patient (Case 3). In the first six cases, the fungus was isolated repeatedly from sputum cultures. In Case 8, the first isolation was obtained from the culture of left bronchial
Volume 73 Number 1 January, 1977
lavage fluid. Subsequently, the sputum culture became positive on nine occasions before surgical intervention. In Case 9, the first positive culture was made from the material obtained by means of selective brushing of the left lower lobe infiltrate. Geotrichum had been isolated from sputum on many occasions before the recovery of M. apiospermum in the last case. In Case 6, sputum cultures were all negative but for fungus. Right upper lobectomy was performed because of M. kansasii infection. M. apiospermum was isolated from the surgical specimen. All cases were associated with other pulmonary diseases. Two cases had chronic obstructive pulmonary disease and chronic bronchitis. Five cases were associated with tuberculosis or its sequelae—bronchiectasis or cavitary lesions. Undifferentiated carcinoma of the right lung was the coexisting condition on one occasion and bronchiectasis of undetermined etiology in another. The clinical features of our nine cases are summarized in Table I. Treatment and results Of the nine patients, five were managed surgically. Lobectomy was performed in three cases and pneumonectomy in one. Thoracotomy was done in one case because of undifferentiated carcinoma which was proved to be resectable. Four patients underwent resectional surgery and had an uneventful recovery without postoperative complications. Sputum cultures were positive on three consecutive occasions in Case 8 after a left upper lobectomy for a cavitary lesion containing a fungus ball. A course of amphotericin B treatment was instituted but sputum cultures continued to be positive. The patient remained clinically well without any symptoms. Three patients were managed medically (Cases 5,7, and 9). Two of these were treated with amphotericin B (Cases 5 and 9). Case 5 presented with multiple cavitary lesions with questionable mycetoma and pleural effusion; however, severe respiratory insufficiency made surgical intervention prohibitive. With amphotericin B treatment, the patient's condition improved initially. Sputum cultures became negative for monosporium. He was discharged for a short period, but returned to the hospital in early 1971. Sputum became positive for monosporium again. Meanwhile, infiltrates extended to the left upper lobe. In spite of another course of amphotericin B administration, the patient died because of profound respiratory failure. Despite adequate amphotericin B administration in Case 9, sputum cultures continued to be positive for fungus. No improvement of the left lower lobe infiltrate
Pulmonary monosporosis
1 41
was observed. Because of drug-induced anorexia, the antifungal drug was discontinued. He remains clinically stable at this time. In Case 7, the sputum culture became negative after adequate postural drainage and antibiotic therapy for concomitant pseudomonas infection. No antifungal drug was necessary. Case 3 left the hospital against medical advice. She was well, as stated by her private physician, 5 years after initial isolation of M. apiospermum from the sputum. No mode of treatment was given to this patient. Discussion In 1909, Tarozzi6 isolated an imperfect fungus from a Sardinian case of Madura foot which was named later by Aaccordo in 1911 as Monosporium apiospermum. In 1921, Boyd and Crutchfield isolated an ascomycete from a mycetoma of a human case.7 This isolate was recognized by Shear7 to be a new species of the genus Allescheria and given the name of Allescheria boydii.1 Emmons8 subsequently clarified the relationship between the two fungi. They were actually the same organism but in different phases of the life cycle. As demonstrated by Lupan and Cazin9 recently, in an animal experiment, the pathogenecity of the fungus appears to be strain-dependent and entirely unrelated to its sexual or asexual phase. A. boydii (sexual form) exhibits no different pathogenic potentials from M. apiospermum (asexual form). Susceptibility of the host to infection appears to be the major determinant factor in developing the disease. Epidemiologic investigation by Ajello6 established that M. apiospermum is ubiquitous in distribution and saprophytic in nature. Primary infection of the lung might be caused by inhalation of the spores, but it is not clear whether in the majority of the patients the course of infection is self-limited, inapparent, and benign, provided no underlying lung disease is present. Allergic bronchopulmonary phenomenon with untoward effect caused by this fungus, to our knowledge, has not been described. Pulmonary monosporosis with positive precipitin antibody was reported by Hainer, Ostrow, and Mackenzie10 recently. Routine use of this test in future cases might help to elucidate this speculation. Eleven cases of pulmonary monosporosis are reported in the literature. Two cases were described twice11' 12' 18' 20; therefore, nine cases were collected from the literature. Summary of these nine cases is shown in Table II. 10 " 20 These nine cases plus our nine cases form the basis of our analysis and subsequent conclusion.
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Table II. Summary of reported cases of pulmonary monosporosis
Year
Ref. No.
Age, sex Profession
Symptoms
1955 1958
11
56 M
Farmer
1960
13
26 F
Farmer's wife
1960
14
53 M
Gardener
Productive cough, bloodstreaked sputum, fever Cough, hemoptysis, pleurisy, pain Hemoptysis
1961
15
37 M
Farmer
Hemoptysis
1966
16
52 F 55 M
Unknown
Hemoptysis
Carpenter
Chest pain, wt. loss
1968
17
1969
19
38 F
Teacher
Coughing spell
1968 1969
18 20
50
Unknown
Productive cough
1974
15
52 F
Rural Hemoptysis, resident productive cough
X-ray findings
Associated lesion or underlying disease
Treatment Medical
Surgical
Result Residual space, hydro-pneumo thorax, died
Multiple cavities, Multiple lung both upper abscesses lobes
2-hydroxystilamide
RU &RM lobectomy
RUL cavity
None
RU lobectomy Recovered
Cavitary lesion, RUL
Cavities with Cavitary lesion fungus ball, tbc.LUL LUL Multiple thinSarcoidosis walled cavities up. lungs, bilat. Bronchogenic cyst Nodule, post. Cavitary tbc. seg., RUL Cavity with fungus ball, LUL
— ACTH and cortisone for sarcoid
Bisegmental resection, LUL None
Postop. pneumonia, recovered Profuse hemoptysis, died
Recovered Excision of nodule LU lobectomy Broncho-fistula, mass. hemorrhage, died Prominent lung Chronic bronchitis Nonspecific med. Recovered markings, treatment, prominent hila nystatin autovaccination Died 1968, Bil. up. lobe Cavitary bronchiec- Endocavitary instillation rt. heart cavities with tasis, ankylosis, spondylitis of 2% K.I many fungus failure balls in 1965 RUL cavity with Pulmonary abc. — fungus ball diabetes RU lobectomy Recovered
Pulmonary monosporosis is a saprophytic infection superimposed on patients with other chronic debilitating disease or whose body defenses have been depressed by drug therapy. Monosporium is most prone to complicate the pre-existing cavitary lesions (nine out of 18 patients), primarily tuberculous in origin. It was associated with bronchiectasis in three (16.6 per cent), chronic obstructive pulmonary disease and chronic bronchitis in two, carcinoma of the lung in one, multiple lung abscess in one, bronchogenic cyst in one, and chronic bronchitis in one. Another case was a case of long-standing pulmonary sarcoidosis treated with steroid, finally invaded by monosporosis; the patient died of massive hemoptysis. Intracavitary mycetoma, or fungus ball, was found in five cases (27 per cent). Characteristically, the lesion appeared as an intracavitary mass separated from the surrounding lung tissue by a crescent of air. Location of the mass in the cavity may
None
—
change with the position of the patient. All these fungus balls are located in the upper lobe. One patient had more than one cavity containing fungus balls. When the appearance on the planigram is not typical, tomogram is usually confirmative. These findings are quite similar to those formed by aspergillosis. The characteristic picture of the fungus ball has been cited frequently since the first description by Deve21 in 1938. Repeated positive sputum cultures of this fungus are of utmost importance in making the diagnosis, but the possibility of contamination should always be kept in mind. Isolation of the organism from the surgical or autopsy specimen serves as a sole confirmative evidence. Symptoms are not distinct and of no diagnostic value. (The high incidence of hemoptysis—52 per cent—is important regarding the decision for treatment.) Repeated isolation of the fungus from the sputum of a patient with cavitary lesion should alert the
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physician to the possibility of pulmonary monosporosis. Precipitin antibody test was found positive in one case. Its significance in establishing the diagnosis needs further evaluation. If the patient presented only with pulmonary infiltrate, or bronchitis, along with positive sputum cultures, probably he would do well with or without antifungal drug administration. As illustrated in our patients, amphotericin B did not alter the prognosis, even though the sputum culture became negative temporarily in one case. Preoperative and postoperative coverage with amphotericin B seems not to be necessary. Disseminated monosporosis has not been observed in the primary form or in the postoperative period. Positive sputum after adequate resection of a pulmonary lesion causes no particular concern. The patients usually do well, as illustrated by our Case 8 and the case of Hainer, Ostrow, and Mackenzie10 in the collected series. Other modalities of supportive treatment are listed in Table II. So it is fair to say, until more effective antifungal drugs are available, the experience with amphotericin B or other modalities of medical management has not been uniformly encouraging. The threat of massive hemoptysis constitutes the major indication for surgical intervention, especially in the case with cavitary lesion containing mycetoma. Those cases usually have a history of, or present with hemoptysis (55 per cent). Experiences also have been gained from the management of aspergillosis with a similar clinical picture. Other indications for surgery are: Treating the underlying diseases, and when the nature of the lesion is uncertain, especially when carcinoma cannot be ruled out. In these 18 patients, 11 (61.1 per cent) underwent surgical treatment. One patient had thoracotomy without resection. The latter was found to have carcinoma which was unresectable. The patient finally died of advanced neoplastic disease. Ten patients had resectional surgery; two of these died postoperatively. One case reported by Tong and associates12 was complicated by postoperative hydropneumothorax and inadequate expansion of the right lower lobe after right upper and middle lobectomy. The patient died because of respiratory insufficiency. The other patient17 underwent a left upper lobectomy with technical difficulty because of dense adhesions and required rib resection. The patient developed a bronchopleural fistula on the twelfth postoperative day, followed by sudden massive intrathoracic hemorrhage on the next day, and died. The other eight patients had rather uneventful recoveries. Thus, postoperative space problems and bronchopleural fistulas constitute the major complications. The outcome of the operation de-
Pulmonary monosporosis
1 43
pends largely on the magnitude and extent of the underlying disease. In most of the cases, this can be managed successfully. Four cases operated upon by us presented no postoperative complication. If the patient with fungus ball in the cavitary lesion carries a prohibitive surgical risk, that patient may be a candidate for endocavitary instillation treatment with 2 per cent potassium iodide, as described by Adelson and Malcolm.18 The result depends on the presence of communication between cavity and bronchial tree, but the long-term outcome is not clear. The fungus ball may recur at any time; as evidenced by Adelson's case later reported by Rosen, Adelson, and Borleigh.20 In conclusion, we suggest the following guidelines for the management of pulmonary monosporosis. 1. Medical treatment with the antifungal drug amphotericin B is not uniformly satisfactory. 2. Conservative watchful management is justifiable in symptomless, noncavitary, nonbronchiectatic patients. No disseminated case has been observed. 3. Endocavity instillation of an antifungal drug may be helpful in selected poor surgical risk patients, but the long-term outcome is not clear. 4. Resectional surgery is satisfactory in the goodrisk patient. Death and complications depend on underlying pathology rather than monosporosis infection. 5. Resectional surgery is the treatment of choice: (a) for a localized cavitary lesion with or without mycetoma; (b) for cases in which resection is indicated for the treatment of the underlying pathology; (c) to establish definite diagnosis in order to avoid missing early treatable disease, such as carcinoma. 6. Preoperative and postoperative antifungal drug coverage is not necessary. REFERENCES 1 Belding, D. L., and Umanzio, C. B.: A New Species of the Genus Monosporium Associated With Chronic Otomycosis, Am. J. Pathol. 11: 856, 1935. 2 Zaffino, A.: Forma sigolore di mycosi cutanea de Monosporium apiospermum a sviluppo clinicamete setticemo: Considerazioui diagnotiche deduzioni mediocolegal, G. Ital. Med. Milit. 86: 636, 1938, cited in Conant, N. F., Smith, D. T., Baker, R. D., Callaway, J. L., and Martin, D. S.: Manual of Clinical Mycology, ed. 2, Philadelphia, 1954, W. B. Saunders Company. 3 Benham, R. W., and George, L. K.: Allescheria boydii, Causative Agent in a Case of Meningitis, J. Invest. Dermatol. 10: 99, 1948. 4 Glassman, M. I., Henkind, P., and Alture-Weber, E.: Monosporium apiospermum Endophthalmitis, Am. J. Ophthalmol. 76: 821, 1973. 5 Reddy, P. C , Christianson, C. S., Gorelick, D. F., and
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6
7
8 9 10 11 12
13
14
Jung et al.
Larsh, H. W.: Pulmonary Monosporosis: An Uncommon Pulmonary Mycotic Infection, Thorax 24: 722, 1969. Tarozzi: cited in Ajello, L.: The Isolation of Allescheria boydii shear, an Etiologic Agent of Mycetomas, From Soil, Am. J. Trop. Med. Hyg. 1: 227, 1952. Shear, C. L.: Life history of an Undescribed Ascomycete Isolated From a Granular Mycetoma of Man, Mycologia 14: 239, 1922. Emmons, C. W.: Allescheria boydii and Monosporium spiospermum, Mycologia 36: 188, 1944. Lupan, D. M., and Cazin, J., Jr.: Pathogenicity of Allescheria boydii for Mice, Infect. Immunol. 8: 743, 1973. Hainer, J. W., Ostrow, J. M., and Mackenzie, D. W. R.: Pulmonary Monosporosis: Report of a Case With Precipitating Antibody, Chest. 66: 601, 1974. Creitz, J., and Harris, M. W.: Isolation of Allescheria boydii From Sputum, Am. Rev. Tuberc. 71: 126, 1955. Tong, J. L., Valentine, E. H., Durrance, J. W., Wilson, G. M., and Fischer, O. A.: Pulmonary Infection with Allescheria boydii. Report of a Fatal Case, Am. Rev. Tuberc. 78: 604, 1958. Scharyj, J., Levene, N., and Gordon, H.: Primary Pulmonary Infection With Monosporium apiospermum, J. Infect. Dis. 106: 141, 1960. Stocekel, H., and Ermer, C : Ein Fall von Monosporium—Mycetom der Lunge: Beitr. Klin. Tuberc. 122: 30, 1960.
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15 Travis, R. E., Ulruch, E. W., and Phillips, S.: Pulmonary Allescheria boydii, Ann. Intern. Med. 54: 141, 1961. 16 Louria, D. B., Lieberman, P. H., Collins, H. S., and Blevins, A.: Pulmonary Mycetoma Due to Allescheria boydii, Arch. Intern. Med. 117: 748, 1960. 17 Aury, P. M., Hocquet, P., Simard, C , Tuchaiz, E., and Cocaud, J.: Allescheriase pulmonaire (mycetome a Allescheria boydii), J. Franc. Med. Chir. Thorac. 33: 425, 1968. 18 Adelson, H. T., and Malcolm, J. A.: Endocavitary Treatment of Pulmonary Mycetomas, Am. Rev. Respir. Dis. 98: 87, 1968. 19 Ariewtsch, A. M., Stepaniszew, S. G., and Tiufilina, O. W.: Ein Fall des durch Monosporium apiospermum hervagerufenen lungen Myzetoms, Mycopathol. Mycol. Appl. 37: 171, 196. 20 Rosen, P., Adelson, H. T., and Borleigh, E.: Bronchiectasis Complicated by the Presence of Monosporium apiospermum and Aspergillus fumigatus. Am. J. Clin. Pathol. 52: 183, 1969. 21 Deve, F.: Une nouvelle forme anatomoradiologique de mycose pulmonaire primitive-le megamycetome intrabronchiectasique, Arch. Med. Chir. Appar. Respir. 13: 337, 1938.
J. Y. Jung, M.D., Rafael Salas, M.D., Carl H. Almond, M.D., Salim Saab, M.D., and Roberto Reyna, M.D., Columbia, Mo.
IT ulmonary monosporosis is a rare pulmonary fungal infection. The fungus, Monosporium apiospernum, is most often isolated from the pathological lesion of cutaneous and subcutaneous tissue of the foot— maduromycosis. Deep mycotic infection other than lung has also been recognized, such as otomycosis,1 septicemia,2 meningitis,3 and endophthalmitis.4 Primary pulmonary infection has been reported off and on in the last two decades, mostly in the form of single case reports. The purpose of this communication is to present our experience with nine cases diagnosed and treated at the Missouri State Chest Hospital. Review of the literature is also made in order to summarize the over-all experience and attempt to formulate guidelines of management. Clinical data Between December, 1956, and August, 1975, nine cases of pulmonary monosporosis were diagnosed at From the Department of Thoracic and Cardiovascular Surgery, University of Missouri Medical Center, and the Department of Surgery, Missouri State Chest Hospital. Received for publication June 30, 1976. Accepted for publication July 23, 1976. Address for reprints: Carl H. Almond, M.D., Professor and Chief of Thoracic and Cardiovascular Surgery, University of Missouri Medical Center, Columbia, Mo. 65201.
the Missouri State Chest Hospital. The first three cases were reported previously by Reddy and associates5 from this institution in 1969. Since then, six additional cases were identified. The criteria for diagnosis were: (1) Repeated isolation of the fungus, M. apiospermum, in the sputum cultures. In order to avoid the contaminant, precaution was taken in the collection of sputum and in the subsequent isolation in the laboratory. Arbitrarily, at least four positive cultures per patient were considered to be significant to be included in this report. Our laboratory has recovered M. apiospermum from sputum in many patients on one or two occasions. Because of its questionable significance, they are not included in this series. (2) Identification and growth of the fungus from the excised surgical specimen. (3) Positive cultures and growth from the specimen obtained from the bronchial washing or selective brushing from the pulmonary lesions through the fiberoptic bronchoscope. (4) Evidence of tissue invasion in tissue sections. There were five men and four women, a ratio of 1.25:1; their ages ranged from 52 to 81 years. Of interest, all nine patients were long-time rural residents. Eight of them were either farmers or farmers' wives. One patient was a baker who had worked in a small-town bakery. All patients underwent complete evaluation. This included tuberculin skin tests, skin test 139
The Journal of Thoracic and Cardiovascular Surgery
1 4 0 Jung et al.
Table I. Summary of nine cases of pulmonary monosporosis (Missouri State Chest Hospital) Case No. Age Sex
Profession
Symptoms
Wife of Fever, chills, farmer productive cough Wife of Productive cough farmer
X-ray findings
Sputum culture
1 1956
52
F
2 1963
77
F
3 62 1967
M
64 4 1969
M
73 5 1969
M
6 1969
60
F
Baker
7 1971
67
F
Monosporium Farmer's Hemoptysis, LLL infiltrate bronch - (+) x 4 wife fever, chills iectasis
8
60
M
Farmer
Chest pain, hemoptysis
Honeycomb, LU lobe
9 81 1975
M
Farmer
Mild cough
LLL infiltrate
Monosporium Cylindrical bronchi(+) ectasis, RUL Monosporium Infiltrate both apices x4(+)
Monosporium Plumber, Hemoptysis, Extensive farmer weight loss, infiltrate (+) weakness and bronchi ectasis cavities, fungus ball X 2, rt. lung Farmer Weakness, Rt. hilar Monosporium chest pain, mass (+) wt. loss Farmer Chest pain, Rt. complete Monosporium hemoptysis opacity, (+) LLL infil.
None
RUL infiltrate
Associated lesion
Treatment
Culture of surgical specimen
Follow-up
RU lobectomy Positive Living and well, for mono last seen in 1968 sporium COPD, chronic None Left hospital — A.M.A., last bronchitis seen in 1968, living and well Continues to be Tbc. far adv., Rt. pneumoPositive nectomy for mono positive in inactive sporium sputum after surgery but well in 1971 Tbc. inactive, RUL
Anaplastic ca. rt. lung
Thoracotomy, inoperable tumor Tbc. far adv., Amphotericin inactive; D.N B, sputum severe respir. became neg. insufficiency
Monosporium M. kansasii neg. infection
—
Died; no autopsy
—
Became positive for monosporium in 1971; died with respiratory failure RU lobectomy Positive M. intracellulare inf., for mono readmitted sporium Antibiotic for Last seen 1975, — good condition pseudomonas
Bronchiectasis LLL, pseudomonas infect. Monosporium T b c , L U L LU lobectomy Positive Sputum continues amphotericin for mono- ( + ) for mono(+); B sporium after TB (+) sporium surgery Geotrichum COPD, chronic Iodide, amLiving and well — (+); monobronchitis photericin B at present sporium (+)
for histoplasma and aspergillus, sputum smears for AFB, fungi, sputum cultures, and bronchoscopic examination. After 1973, selective brushing through the fiberoptic bronchoscope under fluoroscopic control was added to the diagnostic armamentarium. The latter technique was applied in Case 9 to obtain the positive cultures. Clinical symptoms were variable, from none to hemoptysis and general debilitation. Among them, hemoptysis is the most common presenting symptom (44.4 per cent). Other symptoms include productive cough, weight loss, fatigue, and dyspnea. PPD skin test was positive in all patients. Radiologic abnormalities of the lung ranged from pulmonary infiltrates to cavitary lesions containing fungus ball. In Cases 2,
6, and 9, only pulmonary infiltrates were demonstrated. Bronchiectasis was shown in Cases 1 and 7 by means of bronchogram. Case 4 displayed only the right hilar mass. Cases 3, 5, and 8 presented with multiple cavitary lesions. Fungus ball or mycetoma was found in the cavities in Cases 3 and 8. The lesion was located in the upper lobe in three cases: two in the right and one in the left. The left lower lobe was involved in three cases, the entire right lung in two. One patient had a right hilar mass which later proved to be an undifferentiated carcinoma on thoracotomy. Pleural effusion was present in one patient (Case 3). In the first six cases, the fungus was isolated repeatedly from sputum cultures. In Case 8, the first isolation was obtained from the culture of left bronchial
Volume 73 Number 1 January, 1977
lavage fluid. Subsequently, the sputum culture became positive on nine occasions before surgical intervention. In Case 9, the first positive culture was made from the material obtained by means of selective brushing of the left lower lobe infiltrate. Geotrichum had been isolated from sputum on many occasions before the recovery of M. apiospermum in the last case. In Case 6, sputum cultures were all negative but for fungus. Right upper lobectomy was performed because of M. kansasii infection. M. apiospermum was isolated from the surgical specimen. All cases were associated with other pulmonary diseases. Two cases had chronic obstructive pulmonary disease and chronic bronchitis. Five cases were associated with tuberculosis or its sequelae—bronchiectasis or cavitary lesions. Undifferentiated carcinoma of the right lung was the coexisting condition on one occasion and bronchiectasis of undetermined etiology in another. The clinical features of our nine cases are summarized in Table I. Treatment and results Of the nine patients, five were managed surgically. Lobectomy was performed in three cases and pneumonectomy in one. Thoracotomy was done in one case because of undifferentiated carcinoma which was proved to be resectable. Four patients underwent resectional surgery and had an uneventful recovery without postoperative complications. Sputum cultures were positive on three consecutive occasions in Case 8 after a left upper lobectomy for a cavitary lesion containing a fungus ball. A course of amphotericin B treatment was instituted but sputum cultures continued to be positive. The patient remained clinically well without any symptoms. Three patients were managed medically (Cases 5,7, and 9). Two of these were treated with amphotericin B (Cases 5 and 9). Case 5 presented with multiple cavitary lesions with questionable mycetoma and pleural effusion; however, severe respiratory insufficiency made surgical intervention prohibitive. With amphotericin B treatment, the patient's condition improved initially. Sputum cultures became negative for monosporium. He was discharged for a short period, but returned to the hospital in early 1971. Sputum became positive for monosporium again. Meanwhile, infiltrates extended to the left upper lobe. In spite of another course of amphotericin B administration, the patient died because of profound respiratory failure. Despite adequate amphotericin B administration in Case 9, sputum cultures continued to be positive for fungus. No improvement of the left lower lobe infiltrate
Pulmonary monosporosis
1 41
was observed. Because of drug-induced anorexia, the antifungal drug was discontinued. He remains clinically stable at this time. In Case 7, the sputum culture became negative after adequate postural drainage and antibiotic therapy for concomitant pseudomonas infection. No antifungal drug was necessary. Case 3 left the hospital against medical advice. She was well, as stated by her private physician, 5 years after initial isolation of M. apiospermum from the sputum. No mode of treatment was given to this patient. Discussion In 1909, Tarozzi6 isolated an imperfect fungus from a Sardinian case of Madura foot which was named later by Aaccordo in 1911 as Monosporium apiospermum. In 1921, Boyd and Crutchfield isolated an ascomycete from a mycetoma of a human case.7 This isolate was recognized by Shear7 to be a new species of the genus Allescheria and given the name of Allescheria boydii.1 Emmons8 subsequently clarified the relationship between the two fungi. They were actually the same organism but in different phases of the life cycle. As demonstrated by Lupan and Cazin9 recently, in an animal experiment, the pathogenecity of the fungus appears to be strain-dependent and entirely unrelated to its sexual or asexual phase. A. boydii (sexual form) exhibits no different pathogenic potentials from M. apiospermum (asexual form). Susceptibility of the host to infection appears to be the major determinant factor in developing the disease. Epidemiologic investigation by Ajello6 established that M. apiospermum is ubiquitous in distribution and saprophytic in nature. Primary infection of the lung might be caused by inhalation of the spores, but it is not clear whether in the majority of the patients the course of infection is self-limited, inapparent, and benign, provided no underlying lung disease is present. Allergic bronchopulmonary phenomenon with untoward effect caused by this fungus, to our knowledge, has not been described. Pulmonary monosporosis with positive precipitin antibody was reported by Hainer, Ostrow, and Mackenzie10 recently. Routine use of this test in future cases might help to elucidate this speculation. Eleven cases of pulmonary monosporosis are reported in the literature. Two cases were described twice11' 12' 18' 20; therefore, nine cases were collected from the literature. Summary of these nine cases is shown in Table II. 10 " 20 These nine cases plus our nine cases form the basis of our analysis and subsequent conclusion.
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1 4 2 Jung et al.
Table II. Summary of reported cases of pulmonary monosporosis
Year
Ref. No.
Age, sex Profession
Symptoms
1955 1958
11
56 M
Farmer
1960
13
26 F
Farmer's wife
1960
14
53 M
Gardener
Productive cough, bloodstreaked sputum, fever Cough, hemoptysis, pleurisy, pain Hemoptysis
1961
15
37 M
Farmer
Hemoptysis
1966
16
52 F 55 M
Unknown
Hemoptysis
Carpenter
Chest pain, wt. loss
1968
17
1969
19
38 F
Teacher
Coughing spell
1968 1969
18 20
50
Unknown
Productive cough
1974
15
52 F
Rural Hemoptysis, resident productive cough
X-ray findings
Associated lesion or underlying disease
Treatment Medical
Surgical
Result Residual space, hydro-pneumo thorax, died
Multiple cavities, Multiple lung both upper abscesses lobes
2-hydroxystilamide
RU &RM lobectomy
RUL cavity
None
RU lobectomy Recovered
Cavitary lesion, RUL
Cavities with Cavitary lesion fungus ball, tbc.LUL LUL Multiple thinSarcoidosis walled cavities up. lungs, bilat. Bronchogenic cyst Nodule, post. Cavitary tbc. seg., RUL Cavity with fungus ball, LUL
— ACTH and cortisone for sarcoid
Bisegmental resection, LUL None
Postop. pneumonia, recovered Profuse hemoptysis, died
Recovered Excision of nodule LU lobectomy Broncho-fistula, mass. hemorrhage, died Prominent lung Chronic bronchitis Nonspecific med. Recovered markings, treatment, prominent hila nystatin autovaccination Died 1968, Bil. up. lobe Cavitary bronchiec- Endocavitary instillation rt. heart cavities with tasis, ankylosis, spondylitis of 2% K.I many fungus failure balls in 1965 RUL cavity with Pulmonary abc. — fungus ball diabetes RU lobectomy Recovered
Pulmonary monosporosis is a saprophytic infection superimposed on patients with other chronic debilitating disease or whose body defenses have been depressed by drug therapy. Monosporium is most prone to complicate the pre-existing cavitary lesions (nine out of 18 patients), primarily tuberculous in origin. It was associated with bronchiectasis in three (16.6 per cent), chronic obstructive pulmonary disease and chronic bronchitis in two, carcinoma of the lung in one, multiple lung abscess in one, bronchogenic cyst in one, and chronic bronchitis in one. Another case was a case of long-standing pulmonary sarcoidosis treated with steroid, finally invaded by monosporosis; the patient died of massive hemoptysis. Intracavitary mycetoma, or fungus ball, was found in five cases (27 per cent). Characteristically, the lesion appeared as an intracavitary mass separated from the surrounding lung tissue by a crescent of air. Location of the mass in the cavity may
None
—
change with the position of the patient. All these fungus balls are located in the upper lobe. One patient had more than one cavity containing fungus balls. When the appearance on the planigram is not typical, tomogram is usually confirmative. These findings are quite similar to those formed by aspergillosis. The characteristic picture of the fungus ball has been cited frequently since the first description by Deve21 in 1938. Repeated positive sputum cultures of this fungus are of utmost importance in making the diagnosis, but the possibility of contamination should always be kept in mind. Isolation of the organism from the surgical or autopsy specimen serves as a sole confirmative evidence. Symptoms are not distinct and of no diagnostic value. (The high incidence of hemoptysis—52 per cent—is important regarding the decision for treatment.) Repeated isolation of the fungus from the sputum of a patient with cavitary lesion should alert the
Volume 73 Number 1 January, 1977
physician to the possibility of pulmonary monosporosis. Precipitin antibody test was found positive in one case. Its significance in establishing the diagnosis needs further evaluation. If the patient presented only with pulmonary infiltrate, or bronchitis, along with positive sputum cultures, probably he would do well with or without antifungal drug administration. As illustrated in our patients, amphotericin B did not alter the prognosis, even though the sputum culture became negative temporarily in one case. Preoperative and postoperative coverage with amphotericin B seems not to be necessary. Disseminated monosporosis has not been observed in the primary form or in the postoperative period. Positive sputum after adequate resection of a pulmonary lesion causes no particular concern. The patients usually do well, as illustrated by our Case 8 and the case of Hainer, Ostrow, and Mackenzie10 in the collected series. Other modalities of supportive treatment are listed in Table II. So it is fair to say, until more effective antifungal drugs are available, the experience with amphotericin B or other modalities of medical management has not been uniformly encouraging. The threat of massive hemoptysis constitutes the major indication for surgical intervention, especially in the case with cavitary lesion containing mycetoma. Those cases usually have a history of, or present with hemoptysis (55 per cent). Experiences also have been gained from the management of aspergillosis with a similar clinical picture. Other indications for surgery are: Treating the underlying diseases, and when the nature of the lesion is uncertain, especially when carcinoma cannot be ruled out. In these 18 patients, 11 (61.1 per cent) underwent surgical treatment. One patient had thoracotomy without resection. The latter was found to have carcinoma which was unresectable. The patient finally died of advanced neoplastic disease. Ten patients had resectional surgery; two of these died postoperatively. One case reported by Tong and associates12 was complicated by postoperative hydropneumothorax and inadequate expansion of the right lower lobe after right upper and middle lobectomy. The patient died because of respiratory insufficiency. The other patient17 underwent a left upper lobectomy with technical difficulty because of dense adhesions and required rib resection. The patient developed a bronchopleural fistula on the twelfth postoperative day, followed by sudden massive intrathoracic hemorrhage on the next day, and died. The other eight patients had rather uneventful recoveries. Thus, postoperative space problems and bronchopleural fistulas constitute the major complications. The outcome of the operation de-
Pulmonary monosporosis
1 43
pends largely on the magnitude and extent of the underlying disease. In most of the cases, this can be managed successfully. Four cases operated upon by us presented no postoperative complication. If the patient with fungus ball in the cavitary lesion carries a prohibitive surgical risk, that patient may be a candidate for endocavitary instillation treatment with 2 per cent potassium iodide, as described by Adelson and Malcolm.18 The result depends on the presence of communication between cavity and bronchial tree, but the long-term outcome is not clear. The fungus ball may recur at any time; as evidenced by Adelson's case later reported by Rosen, Adelson, and Borleigh.20 In conclusion, we suggest the following guidelines for the management of pulmonary monosporosis. 1. Medical treatment with the antifungal drug amphotericin B is not uniformly satisfactory. 2. Conservative watchful management is justifiable in symptomless, noncavitary, nonbronchiectatic patients. No disseminated case has been observed. 3. Endocavity instillation of an antifungal drug may be helpful in selected poor surgical risk patients, but the long-term outcome is not clear. 4. Resectional surgery is satisfactory in the goodrisk patient. Death and complications depend on underlying pathology rather than monosporosis infection. 5. Resectional surgery is the treatment of choice: (a) for a localized cavitary lesion with or without mycetoma; (b) for cases in which resection is indicated for the treatment of the underlying pathology; (c) to establish definite diagnosis in order to avoid missing early treatable disease, such as carcinoma. 6. Preoperative and postoperative antifungal drug coverage is not necessary. REFERENCES 1 Belding, D. L., and Umanzio, C. B.: A New Species of the Genus Monosporium Associated With Chronic Otomycosis, Am. J. Pathol. 11: 856, 1935. 2 Zaffino, A.: Forma sigolore di mycosi cutanea de Monosporium apiospermum a sviluppo clinicamete setticemo: Considerazioui diagnotiche deduzioni mediocolegal, G. Ital. Med. Milit. 86: 636, 1938, cited in Conant, N. F., Smith, D. T., Baker, R. D., Callaway, J. L., and Martin, D. S.: Manual of Clinical Mycology, ed. 2, Philadelphia, 1954, W. B. Saunders Company. 3 Benham, R. W., and George, L. K.: Allescheria boydii, Causative Agent in a Case of Meningitis, J. Invest. Dermatol. 10: 99, 1948. 4 Glassman, M. I., Henkind, P., and Alture-Weber, E.: Monosporium apiospermum Endophthalmitis, Am. J. Ophthalmol. 76: 821, 1973. 5 Reddy, P. C , Christianson, C. S., Gorelick, D. F., and
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7
8 9 10 11 12
13
14
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Larsh, H. W.: Pulmonary Monosporosis: An Uncommon Pulmonary Mycotic Infection, Thorax 24: 722, 1969. Tarozzi: cited in Ajello, L.: The Isolation of Allescheria boydii shear, an Etiologic Agent of Mycetomas, From Soil, Am. J. Trop. Med. Hyg. 1: 227, 1952. Shear, C. L.: Life history of an Undescribed Ascomycete Isolated From a Granular Mycetoma of Man, Mycologia 14: 239, 1922. Emmons, C. W.: Allescheria boydii and Monosporium spiospermum, Mycologia 36: 188, 1944. Lupan, D. M., and Cazin, J., Jr.: Pathogenicity of Allescheria boydii for Mice, Infect. Immunol. 8: 743, 1973. Hainer, J. W., Ostrow, J. M., and Mackenzie, D. W. R.: Pulmonary Monosporosis: Report of a Case With Precipitating Antibody, Chest. 66: 601, 1974. Creitz, J., and Harris, M. W.: Isolation of Allescheria boydii From Sputum, Am. Rev. Tuberc. 71: 126, 1955. Tong, J. L., Valentine, E. H., Durrance, J. W., Wilson, G. M., and Fischer, O. A.: Pulmonary Infection with Allescheria boydii. Report of a Fatal Case, Am. Rev. Tuberc. 78: 604, 1958. Scharyj, J., Levene, N., and Gordon, H.: Primary Pulmonary Infection With Monosporium apiospermum, J. Infect. Dis. 106: 141, 1960. Stocekel, H., and Ermer, C : Ein Fall von Monosporium—Mycetom der Lunge: Beitr. Klin. Tuberc. 122: 30, 1960.
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15 Travis, R. E., Ulruch, E. W., and Phillips, S.: Pulmonary Allescheria boydii, Ann. Intern. Med. 54: 141, 1961. 16 Louria, D. B., Lieberman, P. H., Collins, H. S., and Blevins, A.: Pulmonary Mycetoma Due to Allescheria boydii, Arch. Intern. Med. 117: 748, 1960. 17 Aury, P. M., Hocquet, P., Simard, C , Tuchaiz, E., and Cocaud, J.: Allescheriase pulmonaire (mycetome a Allescheria boydii), J. Franc. Med. Chir. Thorac. 33: 425, 1968. 18 Adelson, H. T., and Malcolm, J. A.: Endocavitary Treatment of Pulmonary Mycetomas, Am. Rev. Respir. Dis. 98: 87, 1968. 19 Ariewtsch, A. M., Stepaniszew, S. G., and Tiufilina, O. W.: Ein Fall des durch Monosporium apiospermum hervagerufenen lungen Myzetoms, Mycopathol. Mycol. Appl. 37: 171, 196. 20 Rosen, P., Adelson, H. T., and Borleigh, E.: Bronchiectasis Complicated by the Presence of Monosporium apiospermum and Aspergillus fumigatus. Am. J. Clin. Pathol. 52: 183, 1969. 21 Deve, F.: Une nouvelle forme anatomoradiologique de mycose pulmonaire primitive-le megamycetome intrabronchiectasique, Arch. Med. Chir. Appar. Respir. 13: 337, 1938.