Otogenic skull base osteomyelitis caused by invasive fungal infection
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1 Otogenic skull base osteomyelitis caused by invasive fungal infection MICHAEL R. MENACHOF, MD, and ROBERT K. JACKLER, MD, San Francisco, California O to g e n ic sku!l base osteomyelitis (SBO) is classically described as an infection of the external auditory canal that invades the base of the skull, often resulting in progressive cranial nerve palsies. This is a disease primarily of elderly persons with diabetes and is associated with substantial morbidity and mortality. The infectious organism in the majority of cases is Pseudom onas aeruginosa. We have recently encountered two atypical cases of otogenic SBO that were caused by the fungus Aspergillus. CASE REPORTS Case 1. A 46-year-old woman with a longstanding history of chronic middle ear infection underwent induction chemotherapy for acute myelogenous leukemia. Two weeks later, at a time when she was severely leukopenic (WBC = 100), severe otalgia and purulent otorrhea developed. Several days later, a rapid onset complete facial palsy developed. Evaluation, including gallium, technetium, and CT scans, revealed osteomyelitis of the skull base, extending from the mastoid to the lateral wall of the sphenoid sinus. Repeated cultures of the ear drainage failed to yield a bacterial pathogen. A s pergillus flavus was noted, but this was thought to be a contaminant. An empirical trial of antipseudomonal therapy was begun. Several weeks later, despite high-dose intravenous tobramycin and ticarcillin, otalgia and otorrhea persisted. Mastoidectomy was undertaken, primarily to secure tissue for diagnostic purposes. Surgical findings included necrosis of the tympanic membrane remnant and both the middle ear and mastoid mucosa. The mastoid bone was softened and avascular. On histopathologic examination, numerous septated, branching fungal hyphae, consistent with aspergillus, were From the Department of Otolaryngology-Head and Neck Surgery, University of Califomia-San Francisco. Presented at the Annual Meeting of the American Academy of Otolaryngology-Head and Neck Surgery, Washington, D.C., Sept , Submitted for publication Jan. 13, 1989; revision received May 8, 1989; accepted May Reprint requests: Robert K. Jackler, MD, Department of Otolaryngology- Head and Neck Surgery, University of California, San Francisco, 350 Parnassus Ave, Suite 210, San Francisco, CA /4/13841 seen infiltrating both the osseous and soft tissue components of the specimen. A prolonged course of amphotericin B resulted in a dry and pain-free ear. The woman s complete facial palsy persisted through the time of her death from leukemia 13 months after her initial presentation. Case 2. An 82-year-old man had undergone bilateral radical mastoidectomies in the 1940s after a blast injury. He had experienced intermittent painless otorrhea for many years. During a particularly severe and painful exacerbation of his chronic otitis media, an acute facial palsy developed. CT, gallium, and technetium scans were performed, but revealed no evidence of skull base osteomyelitis. Culture of the ear drainage revealed A spergillus fu m ig a tu s and no bacterial pathogens. After several days of empirical antipseudomonal and grampositive antibiotic coverage, he was discharged on a regimen of oral antibiotics. Severe otalgia and intermittent otorrhea persisted despite treatment with repeated oral and ototopical antibiotics. Three months after presentation, gallium, technetium, and CT scans were repeated. Once again, no evidence of osteomyelitis was noted. The retrospective diagnosis of Ramsay Hunt syndrome complicated by post-herpetic neuralgia was considered. During frequent follow-up visits, his pain and discharge increased and diminished over the ensuing months. Repeated ear cultures were negative. Three months after his second series of scans, he manifested a 10-day history of voice change. Examination revealed paralysis of the glossopharyngeus, vagus, accessory, and hypoglossal nerves. At this time, both gallium and technetium scans were markedly positive, with uptake involving the entire posterolateral skull base ipsilateral to the cranial palsies (Fig. 1, A and B ). CT scan revealed extensive bony destruction in the region of the jugular and hypoglossal foramina (Fig. 2, A and B ). Intravenous antipseudomonal antibiotics were reinstituted, with partial resolution of otalgia and otorrhea. Three weeks into this hospitalization, the patient died of a myocardial infarction. Cultures of the otorrhea obtained on admission were initially negative; however, 1 week post mortem, growth of A spergillus fu m ig a tu s was evident. Autopsy revealed basilar meningitis and extensive osteomyelitis of the skull base. Histopathologic examination demonstrated the branching, septate fungal hyphae, typical of aspergillus species, both in the bone and soft tissue components of the skull base (Fig. 3). Gram stain revealed no other infecting organisms. DISCUSSION Deep ear pain, purulent otorrhea, and progressive cranial nerve palsies herald the onset o f otogenic skull 285
2 286 Case Reports O to laryn g o lo g y- Head and Neck Surgery H I T E = G R ft Y = BLftCf Fig.1. Case 2. A, Combined gallium and techetium scan of the head and neck region; lateral view. Arrows denote the area of intense uptake in the temporal bone. B, Combined gallium and technetium scan of the head and neck region; anteroposterior view. Arrows indicate the intense uptake in the temporal bone. base osteomyelitis (SB O ).1 The typical clinical setting is m alignant external otitis, in which infection gains access to the skull base via the floor of the external auditory canal.2-3 This scenario is most common in elderly persons with diabetes and is almost always caused by Pseudom onas aeruginosa. Unlike most otologic infections, pseudom onas SBO evolves through anterograde thrombophlebitis and marrow infection rather than involvem ent of the mucosally lined pneumatic spaces of the temporal bone.4
3 Volume 102 Number 3 March 1990 Case Reports 287 Fig. 2. Case 2. A, Computerized tomography scan of the right temporal bone before the development of skull base osteomyelitis. Note the smooth calcified margins of the jugular foramen (JF) and carotid canal (C). B, Computerized tomography scan in the same patient after the development of skull base osteomyelitis. Note the extensive osseous erosion in the region of the jugular foramen (JF) and carotid canal (C). Combining our two cases with those in the literature, there are now six cases of aspergillus SBO available for study.5'8 There are a number of important differences between fungal SBO and that caused by bacterial pathogens. In four of the six reported cases, the disease originated from the middle ear or mastoid, rather than the ear canal. Longstanding chronic otitis media was present in each of these cases. Immunocomprom ise associated with leukem ia was also prevalent in these patients. Two had acute myelogenous leukem ia associated with marked granulocytopenia and a third had chronic lymphocytic leukemia. The rem aining three patients had no dem onstrable imm une impairment, although all were of advanced age. None of the six patients reported to date had diabetes m ellitus. Invasive aspergillus infections have been increasingly recognized as important clinicopathologic entities, especially in im m unocom prom ised patients.9 There are nearly 30 aspergillus species known to cause invasive infection in man. The most common type is Aspergillus fum igatus, as was seen in four of the six otogenic SBO patients. There are several factors that predispose a patient to invasive aspergillosis: (1) immunodeficiency caused by system ic illness, cytotoxic drug therapy, or
4 288 Case Reports O tolaryngology- Head and Neck Surgery Fig. 3. Histopathologic appearance of infected tissue obtained at mastoidectomy in Case 2. Note the numerous septate branching fungal hyphae within the bony portion of the specimen (black arrows). advanced age; (2) a local point o f entry for the fungus; and,(3) disruption of normal bacterial flora by antim i crobial therapy. Four of the six patients with SBO appear to have been colonized with aspergillus in the middle ear and mastoid resulting from chronic otitis media. W hen immune deterioration occurred, the opportunistic fungus gained access to the adjacent bone marrow and intravascular spaces. Preceding the onset of SBO, each o f the six patients had undergone antibiotic therapy that presum ably fostered fungal overgrowth. The body has two levels o f defense against aspergillus invasion.10 Polym orphonuclear leukocytes (PMN) appear to play a key role in protection against the mycelial form o f aspergillus. M acrophages are instrumental in preventing invasion by the condidial m orphology. M acrophages appear to constitute the primary barrier to penetration, with PM Ns a secondary m echanism. Both of these lines o f defense must be breached for invasion to occur. Corticosteroids may suppress the immune response to both the mycelial and condidial form s.11 At least four o f the six patients with fungal SBO had undergone corticosteroid therapy before the diagnosis o f invasive aspergillosis. The mechanism of neural paralysis with typical pseudomonas SBO appears to be a bacterial elaboration of a neurotoxin.12 A spergillus is also known to produce endotoxins, one of which appears to act upon neural tissue.13 The diagnosis of SBO in a patient with a com patible history and physical findings includes nuclear medicine scans as well as com puted tomography (CT). Gallium 67 citrate is actively taken up by white blood cells and is localized to areas o f inflam m ation.14 Technetium 99m methylene diphosphonate is concentrated in osteoblasts and will demonstrate the effects o f bony infection and repair. Infections of the ear canal, middle ear, and m astoid that are complicated by osteomyelitis will show significant uptake o f both gallium and technetium, whereas infections limited to soft tissue structures will predominantly accumulate gallium. CT scan provides the fine osseous detail needed to map the anatomic extent of S B O.15 Although technetium is a more sensitive detector of early osteomyelitis, it does not provide much anatomic detail. Once positive, both technetium and CT scans remain so for prolonged periods of time. Gallium scans, by contrast, revert to normal when acute inflammation has resolved. This makes sequential gallium scans useful in determining the endpoint o f antibiotic therapy. Magnetic resonance im aging m ay be useful in delineating involvement o f the soft tissues in the infratemporal fossa and nasopharynx.16 Identification of the etiologic agent in otogenic SBO may be difficult when the patient is using antibiotic eardrops. If the infecting organism has not previously been identified, all topical and systemic antibiotics are stopped for 2 days and deep ear culture is obtained. In most of the cases, this will permit identification o f the offending gram-negative bacillus. The mere presence of an aspergillus species on culture does not necessarily indicate a fungal SBO, because these organism s are ubiquitous in the ear. Suspicion should be heightened when either Aspergillus fum igatus or flavus is identified, as these have proved capable of causing fungal SBO. Aspergillus niger, which is the most com mon species isolated from the external auditory canal, has not been reported to cause SBO. The definitive diagnosis o f in
5 Vciume 102 Number 3 March 1990 Case Reports 289 vasive aspergillosis requires biopsy to dem onstrate the organism within the soft tissues or bone o f the skull base. The treatment of SBO requires prolonged antim icrobial therapy, often lasting for months. The selection of an arbitrary duration o f therapy, lasting (for example) 6 weeks, is discouraged. Sequential gallium scans should be obtained and therapy halted when substantial reduction or complete elimination o f activity has taken place. Scans are usually obtained at monthly intervals. Early cessation of therapy is associated with a high recurrence rate and greater morbidity and m ortality.17 The role of surgery in SBO is both diagnostic and, perhaps, therapeutic. In the patient with nondiagnostic cultures, mastoidectom y may provide material for culture and histologic analysis essential for accurate diagnosis and selection between antibiotic and antifungal therapy. Surgery may also be indicated when disease plateaus or progresses on appropriate antimicrobial therapy.18 The drug o f choice for invasive aspergillosis is am photericin B. Use o f this drug in high doses early in the course of invasive aspergillosis m ay be curative, even in some imm unosuppressed patients.9 The usual dosage for am photericin B or invasive aspergillus infections is three gram s, adm inistered as a daily dose ov er many weeks. The optim al total dosage and duration of therapy necessary for com plete resolution of aspergillus SBO is not known. Azotem ia is a serious and potentially fatal side effect o f am photericin B therapy. A rising creatinine level in one of our patients required reduction to 60 mg three times per week. It was not until this patient received a total of 4.6 grams of amphotericin B that her gallium scan cooled o f f and her therapy was term inated. O f the six patients treated for fungal SBO, three have sustained prolonged remission after am photericin therapy. The im provem ent in immunologic function that occurs with cessation of chemotherapy may well play a role in these recoveries. CONCLUSIONS 1. Aspergillus infection of the ear may cause invasive osteomyelitis o f the skull base, accom panied by progressive cranial nerve palsies. 2. These infections tend to arise in im m unocom promised and/or elderly patients. Unlike pseudomonas infections, there is no strong association with diabetes mellitus. 3. While most otogenic skull base osteom yelitis arises from infection o f the external auditory canal, aspergillus tends to invade via the middle ear or mastoid, usually in the setting of longstanding chronic otitis media. 4. Because aspergillus is ubiquitous in the ear, biopsy o f infected tissues is necessary to establish the diagnosis o f invasive fungal infection. 5. Biopsy of skull base tissues to identify the presence of an invasive fungus is indicated when bacterial cultures o f ear drainage are negative or when disease progresses on system ic antipseudom onal therapy. REFERENCES 1. Chandler JR, Grobman L, Quencer R, et al. Osteomyelitis of the base of the skull. Laryngoscope 1986;96: Chandler JR. Malignant external otitis: further considerations. Ann Otol Rhinol Laryngol 1977;86: Chandler JR. Malignant external otitis. Laryngoscope 1968; 78: Nadol JB Jr. Histopathology of pseudomonas osteomyelitis of the temporal bone starting as malignant external otitis. Am J Otolaryngol 1980;1: Cunningham M, Yu V, Turner J. Necrotizing otitis externa due to Aspergillus in an immunocompromised patient. Arch Otolaryngol Head Neck Surg 1988;114: Stanley R, McCaffrey TV, Weiland L. Fungal mastoiditis in the immunocompromised host. Arch Otolaryngol Head Neck Surg 1988;114: Petrak R, Pottage J, Levin S. Invasive external otitis caused by Aspergillus fumigatus in an immunocompromised patient. J Infect Dis 1985;151: Bickley L, Betts R, Parkins C. Atypical invasive external otitis from Aspergillus. Arch Otolaryngol Head Neck Surg 1988; 114: Rinaldi MG. Invasive aspergillosis. Rev Infect Dis 1983;5: Schaffner A, Douglas H, Braude A. Selective protection against conidia by mononuclear and against mycelia by polymorphonuclear phagocytes in resistance to Aspergillus: observations on these two lines of defense in vivo and in vitro with human and mouse phagocytes. J Clin Invest 1982;69: Diamond RD. Inhibition of monocyte-mediated damage to fungal hyphae by steroid hormones. J Infect Dis 1983; 147: Chandler JR. Pathogenesis and treatment of facial paralysis due to malignant external otitis. Ann Otol Rhinol Larynbol 1972;81: Fadulu S. Experimental Aspergillosis: role of endotoxin in pathogenesis and neurologic manifestations of Aspergillosis. In: Iwata K, ed. Recent advances in medical and veterinary mycology. Baltimore: University Park Press, 1975: Garty I, Rosen G, Holdstein Y. The radionuclide diagnosis, evaluation, and follow-up of malignant otitis media (MEO). J Laryngol Otol 1985;99: Gold S, Som PM, Lucente FE, et al. Radiographic findings in progressive necrotizing malignant external otitis. Laryngoscope 1984;94: Gherini SG. Brackmann DE. Bradley WG. Magnetic resonance imaging and computerized tomography in malignant external otitis. Laryngoscope 1986;96: Lucente FE, Parisier SC, Som PM. Complications of the treatment of malignant external otitis. Laryngoscope 1983;93: Raines JM, Schildler RA. The surgical management of recalcitrant malignant external otitis. Laryngoscope 1980;90:
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