Clinical Observation
Optic Neuropathy Caused by Propionibacterium acnes Pachymeningitis Ore-ofe O. Adesina, MD, Brian C. Stagg, MD, Kathleen B. Digre, MD, Bradley J. Katz, MD, PhD, Edward P. Quigley, MD, PhD, Cheryl A. Palmer, MD, Judith E. A. Warner, MD
Abstract: We describe a patient with vision loss from an optic neuropathy caused by Propionibacterium acnes pachymeningitis. The patient’s optic neuropathy was stabilized with appropriate antibiotic therapy. Journal of Neuro-Ophthalmology 2014;34:264–267 doi: 10.1097/WNO.0000000000000101 © 2014 by North American Neuro-Ophthalmology Society
P
achymeningitis is a rare cause of vision loss (1–3). We present a case of vision loss caused by Propionibacterium acnes pachymeningitis. To the best of our knowledge, this is the only such case reported in the literature.
CASE REPORT An 82-year-old man reported a 5-day history of visual field narrowing and “flattening” of colors in the vision of his right eye. His medical history was significant for a 10-year history of ANCA-negative hypereosinophilic Churg–Strauss disease, for which he had been taking prednisone 5 mg daily for 4 years. He also had hypertension, hyperlipidemia, chronic allergic sinusitis, nasal polyposis, and eosinophilic fasciitis confirmed by electromyography and muscle biopsy. He had experienced sequential episodes of nonarteritic anterior ischemic optic neuropathy, first in the left eye 20 years ago and in the right eye 4 months before the presentation. Departments of Ophthalmology (O-OOA, BCS, KBD, BJK, JEAW), Radiology (EPQ), Pathology (CAP), and Neurology (KBD, BJK, JEAW), University of Utah, Salt Lake City, Utah. Supported in part by an unrestricted grant to the Department of Ophthalmology & Visual Sciences from Research to Prevent Blindness, Inc, New York, NY. The authors report no conflicts of interest. Address correspondence to Ore-ofe O. Adesina, MD, Cizik Eye Clinic, 6400 Fannin 18th Floor, Houston, TX 77030; E-mail: oreofe@ gmail.com
264
Family history was unremarkable and review of systems was positive for intermittent left-sided hearing impairment and nonfocal tongue weakness that he had been experiencing for the past 4 months without a definitive etiology. Visual acuity was 20/50 in the right eye, decreased from 20/40 at his last clinic visit 2 months previously. Vision in the left eye was 20/100 and stable. Pupils were reactive with a 1.9 log unit left relative afferent pupillary defect. Automated perimetry showed a new inferior arcuate defect in the right eye and an inferior altitudinal defect in the left eye that was unchanged from previous examination (Fig. 1). Ophthalmoscopy showed bilateral optic disc pallor. The patient was prescribed prednisone 80 mg/d. A temporal artery biopsy showed no signs of inflammation. Magnetic resonance imaging (MRI) of the brain and orbits demonstrated diffuse, smooth pachymeningeal enhancement involving the orbital apices and intracanalicular optic nerve sheaths (Fig. 2). These imaging findings were not present on an MRI performed 4 years before. Laboratory studies including complete blood count, metabolic profile, erythrocyte sedimentation rate, C-reactive protein, syphilis serologies (RPR and VDRL), anticytoplasmic antibody, antinuclear antibody, angiotensin-converting enzyme, and anticardiolipin antibodies were normal except an elevated serum IgE that was unchanged from his baseline. Lumbar puncture revealed an opening pressure of 14 cm H2O with a protein level of 96 mg/dL (normal: 15–45 mg/dL). CSF otherwise showed normal indices, and no infectious organisms were cultured. The patient was given 1 g of intravenous (IV) methylprednisolone daily for 3 days without a change in his vision. A dural biopsy was obtained. Intraoperatively, a milky thickened arachnoid was noted, and features of chronic meningeal inflammation were seen histologically (Fig. 3). Dural tissue culture grew P. acnes, and the patient was treated with oral doxycycline 100 mg twice daily. Two days later, he developed fever and swelling at the surgical site. Adesina et al: J Neuro-Ophthalmol 2014; 34: 264-267
Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.
Clinical Observation
FIG. 1. Automated visual fields. A. Four months before presentation, there is bilateral visual field loss due to previous episodes of nonarteritic anterior ischemic optic neuropathy. B. At presentation, the patient has developed a new inferior nerve fiber bundle defect in the right eye.
MRI revealed an abscess at the biopsy site and persistent diffuse pachymeningeal enhancement. The abscess was drained, and he was treated for 5 days with IV vancomycin and meropenem. Klebsiella oxytoca and P. acnes were cultured from the abscess. He was switched to ceftriaxone 2 g twice daily IV, metronidazole 500 mg 3 times daily orally, and discharged to home in stable condition to complete a 6-week course of antibiotic therapy. One month later, MRI showed decreased inflammation at the biopsy site and resolution of pachymeningeal enhancement. Throughout his hospital course and during 10 months of follow-up, the patient’s visual acuity and fields have remained stable.
DISCUSSION Pachymeningitis is an inflammatory thickening of the dura mater and is an uncommon cause of vision loss (4). Known causes of pachymeningitis include intracranial hypotension Adesina et al: J Neuro-Ophthalmol 2014; 34: 264-267
(5), idiopathic hypertrophic cranial pachymeningitis, central nervous system (CNS) infections, meningeal carcinomatosis, and autoimmune vasculitides including Churg–Strauss syndrome (6). The natural course and treatment of pachymeningitis depends on the underlying etiology. The optic nerves may be affected in the setting of infectious pachymeningitis (7) along with other cranial nerves at the skull base. Because pachymeningitis may be due to both infectious and autoimmune etiologies, we proceeded with dural biopsy in our patient to correctly identify the etiology and guide therapy. Although pachymeningitis can be caused by Churg– Strauss syndrome, the MRI findings in this disorder generally are more focal and isolated and usually discovered on initial presentation, before institution of immunosuppressive therapy (6). Our patient had been on chronic immunosuppressive therapy before presenting with vision loss and pachymeningitis. Additionally, the lack of an eosinophilic inflammatory cell infiltrate in the dural biopsy makes it less likely that Churg–Strauss was the cause of pachymeningitis. Our patient’s pachymeningeal enhancement persisted while on high-dose oral and IV steroids, also making a vasculitic cause less likely. Although there have been rare reports of Churg–Strauss–associated ischemic optic neuropathy, vision loss generally occurs early in the disease course, before treatment with immunosuppressive therapy (8,9). P. acnes is a slow-growing, anaerobic gram-positive bacillus that belongs to the human cutaneous propionibacteria. It is a saprophytic diphtheroid that is part of the normal flora of human skin, particularly the sebaceous glands. It is also an opportunistic agent that produces a number of virulence factors and is well known for its inflammatory and immunomodulatory properties (10). It is occasionally recognized as a contaminant of neurosurgical procedures and biopsies and is a known cause of postoperative CNS infections. Such infections generally are indolent, with a prolonged duration of symptoms before presentation, low to no attributable mortality, significant time lapse between the CNS procedure and presentation, and rarely causing fever or leukocytosis (11,12). There is only 1 report of pachymeningitis caused by P. acnes, and it did not result in an optic neuropathy (13). A 30-yearold woman developed recurrent headaches and recalcitrant partial motor seizures. MRI demonstrated thickening of the left fronto-parietal dura consistent with pachymeningitis, and anaerobic culture of dural biopsy grew P. acnes. One could argue that P. acnes was inoculated into the biopsy site of our patient at the time of the procedure. However, this species was the only organism isolated from the biopsy, and it seems logical that if it was a contaminant, other organisms would have been recovered as well. Granulation tissue–like microvascular proliferation with a mild chronic inflammatory cell component also was seen in the patient’s dural biopsy, histopathologic features consistent with a P. acnes infection. Neuroimaging evidence of pachymeningeal inflammation only resolved after broad-spectrum 265
Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.
Clinical Observation
FIG. 2. Brain magnetic resonance imaging. Initial postcontrast T1 axial (A) and coronal (B) scans show dural enhancement in the middle cranial fossa adjacent to both orbital apices (arrows) and thickening of the optic nerve sheaths of the intracanalicular optic nerves (arrowheads). After treatment, there is resolution of dural enhancement in both the contrasted T1 axial (C) and coronal (D) images (D was obtained with spoiled gradient-recalled sequences and the dural appearance is normal for this technique).
antibiotic therapy, and this clinical course is most consistent with an infectious etiology. It is important to recognize that isolation of P. acnes may indicate a pathologic infection and that this organism is not always a contaminant or saprophyte. Given the clinical and microbiological findings, our case represents a unique presentation of an optic neuropathy in the setting of P. acnes pachymeningitis and illustrates the importance of considering this organism in the differential diagnosis of pachymeningeal enhancement.
REFERENCES
FIG. 3. Dural biopsy shows granulation tissue–like proliferation with a mild chronic inflammatory cell component (hematoxylin and eosin, ·40).
266
1. Bonnin N, Chiambaretta F, Ulla M, Taith F, Chabert E, Claise B, Bacin F. Toxoplasmic pachymeningitis with visual field impairment in a single-eyed patient and a literature review. Oman J Ophthalmol. 2012;5:46–50. 2. Chan JW. Acute monocular visual loss in carcinomatous hypertrophic pachymeningitis mimicking giant cell arteritis. J Clin Rheumatol. 2006;12:30–31. 3. Tariq R, Ahmed R. Tuberculous hypertrophic pachymeningitis presenting as visual blurring and headaches. J Pak Med Assoc. 2012;62:966–968. 4. Weir NU, Collie D, McIllwaine GG, Lueck CJ. Idiopathic hypertrophic chronic pachymeningitis presenting with acute visual loss. Eye (Lond). 1999;13:384–387. Adesina et al: J Neuro-Ophthalmol 2014; 34: 264-267
Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.
Clinical Observation 5. Ferrante E, Riva M, Gatti A, Brioschi A, Marazzi R, Donato MF, Riva M. Intracranial hypotension syndrome: neuroimaging in five spontaneous cases and etiopathogenetic corrections. Clin Neurol Neurosurg. 1998;100:33–39. 6. Tokumaru AM, Obata T, Kohyama S, Kaji T, Okizuka H, Suzuki K, Kusano S. Intracranial meningeal involvement in Churg-Strauss syndrome. AJNR Am J Neuroradiol. 2002;23: 221–224. 7. Girkin CA, Perry JD, Miller NR, Reich SG. Pachymeningitis with multiple cranial neuropathies and unilateral optic neuropathy secondary to Pseudomonas aeruginosa: case report and review. J Neuroophthalmol. 1998;18:196–200. 8. Acheson JF, Cockerell OC, Bentley CR, Sanders MD. ChurgStrauss vasculitis presenting with severe visual loss due to bilateral sequential optic neuropathy. Br J Ophthalmol. 1993; 77:118–119.
Adesina et al: J Neuro-Ophthalmol 2014; 34: 264-267
9. Vallet AE, Didelot A, Guebre-Egziabher F, Bernard M, Mauguiere F. Initial neuro-ophthalmological manifestations in Churg-Strauss syndrome. BMJ Case Rep. 2010;12:2010. 10. Perry AL, Lambert PA. Propionibacterium acnes. Lett Appl Microbiol. 2006;42:185–188. 11. McClelland S III, Hall WA. Postoperative central nervous system infection: incidence and associated factors in 2111 neurosurgical procedures. Clin Infect Dis. 2007;45:55–59. 12. Nisbet M, Briggs S, Ellis-Pegler R, Thomas M, Holland D. Propionibacterium acnes: an under-appreciated cause of postneurosurgical infection. J Antimicrob Chemother. 2007;60: 1097–1103. 13. Nishioka R, Nakajima S, Morimoto Y, Hosoai H, Nakamura H. Hypertrophic cranial pachymeningitis with propionibacterium acnes detected by dural biopsy. Rinsho Shinkeigaku. 1995; 35:526–530.
267
Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.
Optic Neuropathy Caused by Propionibacterium acnes Pachymeningitis Ore-ofe O. Adesina, MD, Brian C. Stagg, MD, Kathleen B. Digre, MD, Bradley J. Katz, MD, PhD, Edward P. Quigley, MD, PhD, Cheryl A. Palmer, MD, Judith E. A. Warner, MD
Abstract: We describe a patient with vision loss from an optic neuropathy caused by Propionibacterium acnes pachymeningitis. The patient’s optic neuropathy was stabilized with appropriate antibiotic therapy. Journal of Neuro-Ophthalmology 2014;34:264–267 doi: 10.1097/WNO.0000000000000101 © 2014 by North American Neuro-Ophthalmology Society
P
achymeningitis is a rare cause of vision loss (1–3). We present a case of vision loss caused by Propionibacterium acnes pachymeningitis. To the best of our knowledge, this is the only such case reported in the literature.
CASE REPORT An 82-year-old man reported a 5-day history of visual field narrowing and “flattening” of colors in the vision of his right eye. His medical history was significant for a 10-year history of ANCA-negative hypereosinophilic Churg–Strauss disease, for which he had been taking prednisone 5 mg daily for 4 years. He also had hypertension, hyperlipidemia, chronic allergic sinusitis, nasal polyposis, and eosinophilic fasciitis confirmed by electromyography and muscle biopsy. He had experienced sequential episodes of nonarteritic anterior ischemic optic neuropathy, first in the left eye 20 years ago and in the right eye 4 months before the presentation. Departments of Ophthalmology (O-OOA, BCS, KBD, BJK, JEAW), Radiology (EPQ), Pathology (CAP), and Neurology (KBD, BJK, JEAW), University of Utah, Salt Lake City, Utah. Supported in part by an unrestricted grant to the Department of Ophthalmology & Visual Sciences from Research to Prevent Blindness, Inc, New York, NY. The authors report no conflicts of interest. Address correspondence to Ore-ofe O. Adesina, MD, Cizik Eye Clinic, 6400 Fannin 18th Floor, Houston, TX 77030; E-mail: oreofe@ gmail.com
264
Family history was unremarkable and review of systems was positive for intermittent left-sided hearing impairment and nonfocal tongue weakness that he had been experiencing for the past 4 months without a definitive etiology. Visual acuity was 20/50 in the right eye, decreased from 20/40 at his last clinic visit 2 months previously. Vision in the left eye was 20/100 and stable. Pupils were reactive with a 1.9 log unit left relative afferent pupillary defect. Automated perimetry showed a new inferior arcuate defect in the right eye and an inferior altitudinal defect in the left eye that was unchanged from previous examination (Fig. 1). Ophthalmoscopy showed bilateral optic disc pallor. The patient was prescribed prednisone 80 mg/d. A temporal artery biopsy showed no signs of inflammation. Magnetic resonance imaging (MRI) of the brain and orbits demonstrated diffuse, smooth pachymeningeal enhancement involving the orbital apices and intracanalicular optic nerve sheaths (Fig. 2). These imaging findings were not present on an MRI performed 4 years before. Laboratory studies including complete blood count, metabolic profile, erythrocyte sedimentation rate, C-reactive protein, syphilis serologies (RPR and VDRL), anticytoplasmic antibody, antinuclear antibody, angiotensin-converting enzyme, and anticardiolipin antibodies were normal except an elevated serum IgE that was unchanged from his baseline. Lumbar puncture revealed an opening pressure of 14 cm H2O with a protein level of 96 mg/dL (normal: 15–45 mg/dL). CSF otherwise showed normal indices, and no infectious organisms were cultured. The patient was given 1 g of intravenous (IV) methylprednisolone daily for 3 days without a change in his vision. A dural biopsy was obtained. Intraoperatively, a milky thickened arachnoid was noted, and features of chronic meningeal inflammation were seen histologically (Fig. 3). Dural tissue culture grew P. acnes, and the patient was treated with oral doxycycline 100 mg twice daily. Two days later, he developed fever and swelling at the surgical site. Adesina et al: J Neuro-Ophthalmol 2014; 34: 264-267
Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.
Clinical Observation
FIG. 1. Automated visual fields. A. Four months before presentation, there is bilateral visual field loss due to previous episodes of nonarteritic anterior ischemic optic neuropathy. B. At presentation, the patient has developed a new inferior nerve fiber bundle defect in the right eye.
MRI revealed an abscess at the biopsy site and persistent diffuse pachymeningeal enhancement. The abscess was drained, and he was treated for 5 days with IV vancomycin and meropenem. Klebsiella oxytoca and P. acnes were cultured from the abscess. He was switched to ceftriaxone 2 g twice daily IV, metronidazole 500 mg 3 times daily orally, and discharged to home in stable condition to complete a 6-week course of antibiotic therapy. One month later, MRI showed decreased inflammation at the biopsy site and resolution of pachymeningeal enhancement. Throughout his hospital course and during 10 months of follow-up, the patient’s visual acuity and fields have remained stable.
DISCUSSION Pachymeningitis is an inflammatory thickening of the dura mater and is an uncommon cause of vision loss (4). Known causes of pachymeningitis include intracranial hypotension Adesina et al: J Neuro-Ophthalmol 2014; 34: 264-267
(5), idiopathic hypertrophic cranial pachymeningitis, central nervous system (CNS) infections, meningeal carcinomatosis, and autoimmune vasculitides including Churg–Strauss syndrome (6). The natural course and treatment of pachymeningitis depends on the underlying etiology. The optic nerves may be affected in the setting of infectious pachymeningitis (7) along with other cranial nerves at the skull base. Because pachymeningitis may be due to both infectious and autoimmune etiologies, we proceeded with dural biopsy in our patient to correctly identify the etiology and guide therapy. Although pachymeningitis can be caused by Churg– Strauss syndrome, the MRI findings in this disorder generally are more focal and isolated and usually discovered on initial presentation, before institution of immunosuppressive therapy (6). Our patient had been on chronic immunosuppressive therapy before presenting with vision loss and pachymeningitis. Additionally, the lack of an eosinophilic inflammatory cell infiltrate in the dural biopsy makes it less likely that Churg–Strauss was the cause of pachymeningitis. Our patient’s pachymeningeal enhancement persisted while on high-dose oral and IV steroids, also making a vasculitic cause less likely. Although there have been rare reports of Churg–Strauss–associated ischemic optic neuropathy, vision loss generally occurs early in the disease course, before treatment with immunosuppressive therapy (8,9). P. acnes is a slow-growing, anaerobic gram-positive bacillus that belongs to the human cutaneous propionibacteria. It is a saprophytic diphtheroid that is part of the normal flora of human skin, particularly the sebaceous glands. It is also an opportunistic agent that produces a number of virulence factors and is well known for its inflammatory and immunomodulatory properties (10). It is occasionally recognized as a contaminant of neurosurgical procedures and biopsies and is a known cause of postoperative CNS infections. Such infections generally are indolent, with a prolonged duration of symptoms before presentation, low to no attributable mortality, significant time lapse between the CNS procedure and presentation, and rarely causing fever or leukocytosis (11,12). There is only 1 report of pachymeningitis caused by P. acnes, and it did not result in an optic neuropathy (13). A 30-yearold woman developed recurrent headaches and recalcitrant partial motor seizures. MRI demonstrated thickening of the left fronto-parietal dura consistent with pachymeningitis, and anaerobic culture of dural biopsy grew P. acnes. One could argue that P. acnes was inoculated into the biopsy site of our patient at the time of the procedure. However, this species was the only organism isolated from the biopsy, and it seems logical that if it was a contaminant, other organisms would have been recovered as well. Granulation tissue–like microvascular proliferation with a mild chronic inflammatory cell component also was seen in the patient’s dural biopsy, histopathologic features consistent with a P. acnes infection. Neuroimaging evidence of pachymeningeal inflammation only resolved after broad-spectrum 265
Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.
Clinical Observation
FIG. 2. Brain magnetic resonance imaging. Initial postcontrast T1 axial (A) and coronal (B) scans show dural enhancement in the middle cranial fossa adjacent to both orbital apices (arrows) and thickening of the optic nerve sheaths of the intracanalicular optic nerves (arrowheads). After treatment, there is resolution of dural enhancement in both the contrasted T1 axial (C) and coronal (D) images (D was obtained with spoiled gradient-recalled sequences and the dural appearance is normal for this technique).
antibiotic therapy, and this clinical course is most consistent with an infectious etiology. It is important to recognize that isolation of P. acnes may indicate a pathologic infection and that this organism is not always a contaminant or saprophyte. Given the clinical and microbiological findings, our case represents a unique presentation of an optic neuropathy in the setting of P. acnes pachymeningitis and illustrates the importance of considering this organism in the differential diagnosis of pachymeningeal enhancement.
REFERENCES
FIG. 3. Dural biopsy shows granulation tissue–like proliferation with a mild chronic inflammatory cell component (hematoxylin and eosin, ·40).
266
1. Bonnin N, Chiambaretta F, Ulla M, Taith F, Chabert E, Claise B, Bacin F. Toxoplasmic pachymeningitis with visual field impairment in a single-eyed patient and a literature review. Oman J Ophthalmol. 2012;5:46–50. 2. Chan JW. Acute monocular visual loss in carcinomatous hypertrophic pachymeningitis mimicking giant cell arteritis. J Clin Rheumatol. 2006;12:30–31. 3. Tariq R, Ahmed R. Tuberculous hypertrophic pachymeningitis presenting as visual blurring and headaches. J Pak Med Assoc. 2012;62:966–968. 4. Weir NU, Collie D, McIllwaine GG, Lueck CJ. Idiopathic hypertrophic chronic pachymeningitis presenting with acute visual loss. Eye (Lond). 1999;13:384–387. Adesina et al: J Neuro-Ophthalmol 2014; 34: 264-267
Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.
Clinical Observation 5. Ferrante E, Riva M, Gatti A, Brioschi A, Marazzi R, Donato MF, Riva M. Intracranial hypotension syndrome: neuroimaging in five spontaneous cases and etiopathogenetic corrections. Clin Neurol Neurosurg. 1998;100:33–39. 6. Tokumaru AM, Obata T, Kohyama S, Kaji T, Okizuka H, Suzuki K, Kusano S. Intracranial meningeal involvement in Churg-Strauss syndrome. AJNR Am J Neuroradiol. 2002;23: 221–224. 7. Girkin CA, Perry JD, Miller NR, Reich SG. Pachymeningitis with multiple cranial neuropathies and unilateral optic neuropathy secondary to Pseudomonas aeruginosa: case report and review. J Neuroophthalmol. 1998;18:196–200. 8. Acheson JF, Cockerell OC, Bentley CR, Sanders MD. ChurgStrauss vasculitis presenting with severe visual loss due to bilateral sequential optic neuropathy. Br J Ophthalmol. 1993; 77:118–119.
Adesina et al: J Neuro-Ophthalmol 2014; 34: 264-267
9. Vallet AE, Didelot A, Guebre-Egziabher F, Bernard M, Mauguiere F. Initial neuro-ophthalmological manifestations in Churg-Strauss syndrome. BMJ Case Rep. 2010;12:2010. 10. Perry AL, Lambert PA. Propionibacterium acnes. Lett Appl Microbiol. 2006;42:185–188. 11. McClelland S III, Hall WA. Postoperative central nervous system infection: incidence and associated factors in 2111 neurosurgical procedures. Clin Infect Dis. 2007;45:55–59. 12. Nisbet M, Briggs S, Ellis-Pegler R, Thomas M, Holland D. Propionibacterium acnes: an under-appreciated cause of postneurosurgical infection. J Antimicrob Chemother. 2007;60: 1097–1103. 13. Nishioka R, Nakajima S, Morimoto Y, Hosoai H, Nakamura H. Hypertrophic cranial pachymeningitis with propionibacterium acnes detected by dural biopsy. Rinsho Shinkeigaku. 1995; 35:526–530.
267
Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.
