Epidural intracranial abscesses and multiple bone metastases caused by disseminated Mycobacterium avium complex infection: illustrative case

Yu Nomura Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Ai Mizukami Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Kota Ueno Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Ryota Watanabe Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Shohei Kinoshita Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Nozomi Fujiwara Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Kiyohide Kakuta Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Takahiro Morita Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Kenichiro Asano Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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Atsushi Saito Department of Neurosurgery, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

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BACKGROUND

Mycobacterium avium complex (MAC) generally causes localized pulmonary infections in immunocompromised hosts, but rarely in other organs and tissues, which is called disseminated MAC infection.

OBSERVATIONS

The authors herein present a 48-year-old male patient with disseminated MAC infectious lesions in the lungs and on the cranial, vertebral, femoral, and pelvic bones, a normal CD4 count, and immunopositivity for the interferon-ɤ (IFN-ɤ) neutralization antibody. Cranial lesions were multiple osteolytic lesions associated with abscesses in the cranial bones. The patient initially received conservative treatment with multiple antibiotics; however, cranial lesions worsened. Therefore, multiple cranial lesions were removed via osteoplastic craniectomy and the postoperative course was uneventful. Pathological findings revealed MAC infection. The patient was discharged without recurrence or complications.

LESSONS

Multiple cranial MAC dissemination with immunopositivity for the IFN-ɤ antibody is rare. The authors herein present the clinical course of a rare surgical case of MAC dissemination with a literature review.

ABBREVIATIONS

CT = computed tomography; HIV = human immunodeficiency virus; IFN-ɤ = interferon-ɤ; IL-12 = interleukin-12; MAC = Mycobacterium avium complex; MR = magnetic resonance

BACKGROUND

Mycobacterium avium complex (MAC) generally causes localized pulmonary infections in immunocompromised hosts, but rarely in other organs and tissues, which is called disseminated MAC infection.

OBSERVATIONS

The authors herein present a 48-year-old male patient with disseminated MAC infectious lesions in the lungs and on the cranial, vertebral, femoral, and pelvic bones, a normal CD4 count, and immunopositivity for the interferon-ɤ (IFN-ɤ) neutralization antibody. Cranial lesions were multiple osteolytic lesions associated with abscesses in the cranial bones. The patient initially received conservative treatment with multiple antibiotics; however, cranial lesions worsened. Therefore, multiple cranial lesions were removed via osteoplastic craniectomy and the postoperative course was uneventful. Pathological findings revealed MAC infection. The patient was discharged without recurrence or complications.

LESSONS

Multiple cranial MAC dissemination with immunopositivity for the IFN-ɤ antibody is rare. The authors herein present the clinical course of a rare surgical case of MAC dissemination with a literature review.

ABBREVIATIONS

CT = computed tomography; HIV = human immunodeficiency virus; IFN-ɤ = interferon-ɤ; IL-12 = interleukin-12; MAC = Mycobacterium avium complex; MR = magnetic resonance

Infection with nontuberculous mycobacteria, typically Mycobacterium avium complex (MAC), predominantly occurs in the right middle lobe or lingual lobe of the lungs in nonsmoking, middle-aged females,1,2 and other locations of this disease, particularly the disseminated form of MAC in patients without human immunodeficiency virus (HIV), are rare.3,4 Underlying patient features, such as the reduced production of interferon-ɤ (IFN-ɤ) by T cells and natural killer cells, increase susceptibility to mycobacterial infection, indicating a newly acquired immunocompromised status.1,5 Disseminated MAC infection also occurs in immunocompromised patients or patients with preexisting conditions and intracranial and cranial bony infections are rare.6 Koya et al. reported that patients who were immunopositive for anti-IFN-ɤ antibodies were more likely to show the dissemination of MAC into bony and cartilaginous lesions and be resistant to multiple antibiotic agents.1,7 However, the precise infectious mechanisms and clinical features of MAC dissemination with immunopositivity for the IFN-ɤ neutralizing antibody remain unknown.

We encountered a case of MAC dissemination with multiple osteolytic bone lesions (cranial and vertebral bones, ribs, pelvis, and limbs). Multimodal antibiotic treatment was ineffective against cranial bony lesions, and, thus, surgical resection was performed. We herein present the clinical course of MAC dissemination with immunopositivity for the IFN-ɤ antibody with a literature review.

Illustrative Case

A 48-year-old male patient with fever, back pain, and no neurological deficits presented to the hospital. Computed tomography (CT) showed multiple bone lesions in the cranial bones, vertebral bones (C4, T1, T2, and T8), pelvic bones, and femoral bone (Fig. 1A and B). Chest CT revealed a nodular lesion in the left lung and bronchial dilation (Fig. 1C and D). Therefore, the patient was referred to a respiratory physician. Fluorodeoxyglucose positron emission tomography showed increased uptake by the cranial bones, vertebral bones, ribs, and pelvic bones (Fig. 2A–D). Massive cranial lesions were biopsied. Hematoxylin and eosin staining of biopsy samples revealed granuloma, while mycobacterial staining showed mycobacterial-positive tissue. The patient had a normal CD4 count (1,078 × 103/μL), but was immunopositive for the IFN-ɤ antibody, which was examined at Kumamoto University. He was diagnosed with disseminated MAC infection. Head CT showed a low-density mass at the right frontal lesion that had eroded cranial bone (Fig. 3A and B). He was treated with rifampicin, ethambutol, kanamycin, amikacin, and sitafloxacin. Multiple cranial lesions worsened despite the attenuation of pulmonary lesions and femoral and pelvic bone lesions. Head CT and the bone window of head CT showed a new low-density mass at the midline of the frontal extracranial lesion that eroded cranial bone and reached the epidural space, but not the dura mater (Fig. 3C and D: head CT; Fig. 3E and F: the bone window of head CT). Enhanced magnetic resonance (MR) images revealed that the membrane of an abscess, cranial bone, and the dura mater, which was attached to the abscess, were enhanced, and cranial bone was eroded (Fig. 4A–C). MR diffusion-weighted images showed a high signal intensity in these lesions, suggesting abscesses (Fig. 4D).

FIG. 1.
FIG. 1.

CT of bone conditions showing vertebral bones (C4, T1, T2, and T8) that are fractured and compressed (white arrowheads in A and B). Chest CT showing lesions, a pulmonary infiltrative shadow, and bronchodilation in the left lower lung (black arrowheads in C and D), which is in accordance with the CT findings of MAC.

FIG. 2.
FIG. 2.

Fluorodeoxyglucose positron emission tomography of the present case showing increased uptake by multiple cranial bones, vertebral bones, rib bones, pelvic bones, the brain, kidneys, and liver (A and B). In the skull, increased uptake was noted at the front and left side of the head (C and D).

FIG. 3.
FIG. 3.

Head CT before the initiation of treatment showing a low-density mass at the extracranial right frontal bone lesion (white arrowheads in A: axial, B: sagittal) that eroded cranial bone (black arrowheads in A and B). Head CT 5 months after the initiation of treatment showing a new low-density mass at the extracranial anterior frontal bone (white arrowheads in C: axial, D: sagittal) that slightly eroded cranial bone (black arrowheads in C and D) and reached the epidural space, but not the dura mater. The bone window of head CT 5 months after the initiation of treatment showed eroded cranial bone (white arrowheads in E and F).

FIG. 4.
FIG. 4.

An enhanced MR image showing that the membrane of an abscess, cranial bone, and the dura mater at the left frontal bone that attached to the abscess were enhanced, and cranial bone was eroded (white arrowheads in A: axial, B: coronal; black arrowheads in A: axial, B: coronal, and C: sagittal). An MR diffusion-weighted image showing the hyperintensity of the abscess (white arrow, D).

The surgical resection of enlarged cranial lesions was performed with right frontal osteoplastic craniectomy. Milky abscesses were observed at the extracranial lesion that eroded cranial bone. During craniotomy, we noted that a milky liquid abscess had spread in the epidural space. The partially thickened abscess had adhered to the dura mater. We removed two pieces of galea tissues eroded by the milky abscess as well as eroded bony tissues that were red and purple in color. A pathological examination of these tissue specimens showed coagulative necrosis, epithelial granulomas, inflammatory cells, and multinuclear giant cells, which suggested nontuberculous mycobacterial infection (Fig. 5A and B). A bacterial culture revealed M. intracellulare in the subcutaneous abscess. Rifampicin, ethambutol, clarithromycin, amikacin, and sitafloxacin were administered for 1 week after surgery and were followed by rifabutin and clarithromycin until discharge. No recurrence has been detected and back pain was attenuated.

FIG. 5.
FIG. 5.

A: Pathological findings of a biopsy specimen of galea tissue showing coagulative necrosis (white arrow), epithelial granulomas (black arrow), and inflammatory cells (white arrow) (hematoxylin and eosin staining). B: A specimen of decalcified bony tissue showing coagulative necrosis (white arrow), epithelial granulomas (black arrowheads), and inflammatory cells (white arrowheads), which are specific to the pathogen of nontuberculous mycobacterial infection (hematoxylin and eosin staining).

Discussion

Observations

MAC includes two important human pathogens, M. avium and M. intracellulare. MAC organisms are ubiquitous in the environment and have been identified in typical reservoirs of soil, water, and animals.8 There are no documented cases of the horizontal transmission of nontuberculous mycobacteria infections,9 and manifestations of human disease most commonly occur after the acquisition of a bacterial inoculum via inhalation or ingestion.8,10 MAC was rare until 1982 when it was found to be associated with HIV infection. Due to increased awareness, the number of case reports of MAC infection markedly increased, particularly in developed countries with a decreasing incidence of M. tuberculosis infection.6,11 The presentation of MAC varies and depends on the level of immunity in an individual. Isolated pulmonary infection is the most common form in an immunocompetent individual.9 In contrast, focal lymphadenitis and disseminated MAC are common forms of MAC infection in HIV-positive individuals.12,13 Patients with a CD4 count <50 U/L are at an increased risk of disseminated infections due to MAC, whereas those with higher total CD4 counts are more likely to have M. tuberculosis infection.14,15 Disseminated MAC infection may mimic disseminated histoplasmosis and difficulties are sometimes associated with distinguishing between both conditions in patients residing in endemic areas.16,17 Factors present in both disease conditions that were identified in our patient included severe immunosuppression, nonspecific symptoms, elevated alkaline phosphatase, lactate dehydrogenase, and aspartate aminotransferase, cytopenia (particularly thrombocytopenia), and markedly elevated ferritin.18 The early detection of MAC infection and initiation of appropriate antimicrobial regimens are associated with prolonged survival.19 The diagnosis of MAC infection in the absence of immunodeficiency and predisposing conditions is more likely to be delayed and have a high recurrence rate.6

The disseminated form of MAC in patients without HIV is rare.1,3 The first step in the treatment of nontuberculous infection is overcoming the innate antimicrobial response provided by macrophages and IFN-ɤ.20 Most of these cases are accompanied by immune deficiencies associated with the regulation of the interleukin-12 (IL-12)–IFN-ɤ circuit.1 Recent studies reported the presence of high titers of IFN-ɤ neutralization antibodies in patients diagnosed with disseminated mycobacterial or other infections; these antibodies exert high-affinity inhibitory effects.4,21 Browne et al.22 detected high titers of IFN-ɤ neutralization antibodies in 42 of 52 patients with disseminated, rapidly, or slowly growing nontuberculous mycobacterial infection. The presence of anti-IFN-ɤ autoantibodies demonstrated their blockade of human IFN-ɤ binding, their inhibitory effects on IFN-ɤ signal transduction, such as signal transducers and activators of transcription-1 phosphorylation, and their suppression of the downstream biological effects of IFN-ɤ binding, including IL-12 or tumor necrosis factor-α production.23 Patients who were immunopositive for anti-IFN-ɤ antibodies were more likely to show the dissemination of MAC into bony and cartilaginous lesions and resistance to multiantibiotic agents.1 A recent study revealed that a new treatment strategy with the CD20 monoclonal antibody, rituximab, which inhibits the production of IFN, was effective against MAC with immunopositivity for IFN-ɤ.24

Intracranial MAC lesions are challenging to diagnose, requiring tissue sampling. Lane-Donovan et al.25 reported a case of multiple brain abscesses caused by MAC in a review of 51 cases in the literature. Although peripheral MAC infections are classically associated with granulomatous inflammation, similar histological changes are rarely identified in MAC intracranial infectious lesions.25 The majority of reported cases have been characterized by spindle cell pseudotumors, in which spindle-shaped histiocyte proliferation results in tumor-like lesions that contain mycobacteria. In a literature review on 51 cases of spindle cell pseudotumors, 26 (51%) had HIV and 24 (47%) had MAC infections.26 In reported cases of MAC brain abscesses in which tissue was obtained, acid fast bacteria cultures from brain biopsy samples frequently grew MAC, whereas cerebrospinal fluid cultures were negative or not reported, including ventricular fluid from a patient who developed hydrocephalus due to abscess blockage of the fourth ventricle.27,28 Lane-Donovan et al.25 effectively treated multiple MAC brain abscesses with antibiotic agents, concluded that its diagnosis may be challenging given variable radiographic and histological features, and proposed a universal broad-range polymerase chain reaction as an available complementary tool to increase diagnostic yield.

There is currently no well-established treatment strategy for MAC intracranial abscesses. The majority of cases are treated with a three-drug regimen of a macrolide (azithromycin or clarithromycin), ethambutol, and rifabutin, extrapolated from treatment guidelines for disseminated MAC.29 Macrolides and ethambutol are considered to reach sufficient cerebrospinal fluid concentrations only in the setting of meningeal inflammation, and it is important to note that many of these MAC brain abscesses were detected in the absence of meningitis.30 Furthermore, rifamycin concentrations may not achieve the minimum inhibitory concentration for some mycobacterial strains in the central nervous system.31 These concerns prompted us to intensify MAC therapy with moxifloxacin when cranial abscesses in the present case did not exhibit radiological improvement.32

Lessons

The present case had the following characteristic features. The patient showed immunopositivity for the IFN-ɤ neutralization antibody and multiple systemic lesions, such as in the lungs and other bony tissues. Furthermore, uptake by multiple cranial lesions on fluorodeoxyglucose positron emission tomography contributed to the correct diagnosis of MAC dissemination. In addition, conservative treatment with five types of antibiotic agents resulted in the remission of lung and other systemic bony lesions, such as the vertebral, pelvic, and femoral bones; however, it was not effective against cranial lesions. The clinical feature of resistance to multiantibiotic agents was consistent with previous findings on MAC with immunopositivity for the IFN-ɤ neutralization antibody. However, the pathological feature of the cranial dissemination of MAC with immunopositivity for the IFN-ɤ neutralization antibody, which originated from membranous ossification, was not in accordance with previous findings.1 The efficiency of antibiotic agents for the systemic bony dissemination of MAC in the vertebral, pelvic, and femoral bones differed. The mechanism of ossification and the pathological characteristics of MAC dissemination with immunopositivity for the IFN-ɤ neutralization antibody may be related. Although MAC dissemination into cranial lesions with immunopositivity for the IFN-ɤ neutralization antibody is rare, this diagnosis needs to be considered, particularly in patients with multiple osteolytic lesions that are not responsive to empirical antibiotic therapy and who have concomitant MAC disease in other parts of the body.

Acknowledgments

We wish to acknowledge Dr. Takuro Sakagami, Professor of the Department of Respiratory Medicine, The Faculty of Life Sciences, Kumamoto University, for his help with measuring immunopositivity for the interferon-ɤ neutralization antibody.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Saito, Nomura, Ueno, Asano. Acquisition of data: Nomura, Mizukami, Ueno, Watanabe, Fujiwara, Asano. Analysis and interpretation of data: Nomura, Ueno, Fujiwara, Asano. Drafting the article: Nomura, Ueno. Critically revising the article: Saito, Ueno, Kinoshita. Reviewed submitted version of manuscript: Nomura, Ueno, Morita. Approved the final version of the manuscript on behalf of all authors: Saito. Statistical analysis: Ueno. Administrative/technical/material support: Ueno. Study supervision: Ueno, Kakuta, Asano.

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  • Collapse
  • Expand
  • FIG. 1.

    CT of bone conditions showing vertebral bones (C4, T1, T2, and T8) that are fractured and compressed (white arrowheads in A and B). Chest CT showing lesions, a pulmonary infiltrative shadow, and bronchodilation in the left lower lung (black arrowheads in C and D), which is in accordance with the CT findings of MAC.

  • FIG. 2.

    Fluorodeoxyglucose positron emission tomography of the present case showing increased uptake by multiple cranial bones, vertebral bones, rib bones, pelvic bones, the brain, kidneys, and liver (A and B). In the skull, increased uptake was noted at the front and left side of the head (C and D).

  • FIG. 3.

    Head CT before the initiation of treatment showing a low-density mass at the extracranial right frontal bone lesion (white arrowheads in A: axial, B: sagittal) that eroded cranial bone (black arrowheads in A and B). Head CT 5 months after the initiation of treatment showing a new low-density mass at the extracranial anterior frontal bone (white arrowheads in C: axial, D: sagittal) that slightly eroded cranial bone (black arrowheads in C and D) and reached the epidural space, but not the dura mater. The bone window of head CT 5 months after the initiation of treatment showed eroded cranial bone (white arrowheads in E and F).

  • FIG. 4.

    An enhanced MR image showing that the membrane of an abscess, cranial bone, and the dura mater at the left frontal bone that attached to the abscess were enhanced, and cranial bone was eroded (white arrowheads in A: axial, B: coronal; black arrowheads in A: axial, B: coronal, and C: sagittal). An MR diffusion-weighted image showing the hyperintensity of the abscess (white arrow, D).

  • FIG. 5.

    A: Pathological findings of a biopsy specimen of galea tissue showing coagulative necrosis (white arrow), epithelial granulomas (black arrow), and inflammatory cells (white arrow) (hematoxylin and eosin staining). B: A specimen of decalcified bony tissue showing coagulative necrosis (white arrow), epithelial granulomas (black arrowheads), and inflammatory cells (white arrowheads), which are specific to the pathogen of nontuberculous mycobacterial infection (hematoxylin and eosin staining).

  • 1

    Koya T, Tsubata C, Kagamu H, et al. Anti-interferon-gamma autoantibody in a patient with disseminated Mycobacterium avium complex. J Infect Chemother. 2009;15(2):118122.

  • 2

    Prince DS, Peterson DD, Steiner RM, et al. Infection with Mycobacterium avium complex in patients without predisposing conditions. N Engl J Med. 1989;321(13):863868.

  • 3

    Dorman SE, Picard C, Lammas D, et al. Clinical features of dominant and recessive interferon gamma receptor 1 deficiencies. Lancet. 2004;364(9451):21132121.

  • 4

    Döffinger R, Helbert MR, Barcenas-Morales G, et al. Autoantibodies to interferon-gamma in a patient with selective susceptibility to mycobacterial infection and organ-specific autoimmunity. Clin Infect Dis. 2004;38(1):e10e14.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Safdar A, White DA, Stover D, Armstrong D, Murray HW. Profound interferon gamma deficiency in patients with chronic pulmonary nontuberculous mycobacteriosis. Am J Med. 2002;113(9):756759.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    To K, Cao R, Yegiazaryan A, Owens J, Venketaraman V. General overview of nontuberculous mycobacteria opportunistic pathogens: Mycobacterium avium and Mycobacterium abscessus. J Clin Med. 2020;9(8):2541.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Kampitak T, Suwanpimolkul G, Browne S, Suankratay C. Anti-interferon-γ autoantibody and opportunistic infections: case series and review of the literature. Infection. 2011;39(1):6571.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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