Pediatr Radiol DOI 10.1007/s00247-011-2340-8
PICTORIAL ESSAY
Skull base osteomyelitis and potential cerebrovascular complications in children Mariasavina Severino & Sidath Liyanage & Vas Novelli & Beth Cheesborough & Dawn Saunders & Roxana Gunny & Andrea Rossi
Received: 9 September 2011 / Revised: 24 November 2011 / Accepted: 5 December 2011 # Springer-Verlag 2012
Abstract Skull base osteomyelitis is an aggressive, lifethreatening infection that can be challenging to diagnose and treat. It occurs predominantly in elderly immunocompromised patients, but it has also been reported in children with normal immunological status. Typical skul base osteomyelitis arises as a complication to ear infection mainly involving the temporal bone and is usually caused by Pseudomonas aeruginosa. Atypical or central skul base osteomyelitis originates from paranasal infections, is primarily centred on the clivus and is usually caused by Aspergillus, Pseudomonas, Salmonella or Staphylococcus species. Potential complications include retropharyngeal abscesses, cranial neuropathies, meningitis, intracranial abscesses, sinovenous thrombosis, and carotid artery involvement with or without ischemic infarcts. The purpose of this pictorial essay is to illustrate the spectrum of imaging findings and potential complications of skul base osteomyelitis. Keywords Skull base osteomyelitis . Intracranial vascular complications . Lemierre syndrome
M. Severino : A. Rossi (*) Neuroradiology Department, G. Gaslini Children’s Hospital, Largo G. Gaslini 5, 16147 Genoa, Italy e-mail:
[email protected] S. Liyanage : D. Saunders : R. Gunny Radiology Department, Great Ormond Street Hospital, London, UK V. Novelli : B. Cheesborough Paediatric Infectious Disease, Great Ormond Street Hospital, London, UK
Introduction Skull base osteomyelitis is a rare, severe inflammation of the bones and soft tissues at the base of the skull that requires prompt diagnosis and aggressive management [1]. It predominantly occurs in diabetic or immunocompromised adults and in the elderly but has also been reported in both immunocompromised and immunocompetent children, with high morbidity and mortality [1, 2]. The clinical diagnosis is often delayed and mainly relies on imaging. Skul base osteomyelitis can be either typical, usually involving the temporal or occipital bones, or atypical/central, usually involving the clivus. Typical skul base osteomyelitis, also called malignant external otitis, is usually initiated by a soft-tissue infection of the external auditory canal, which spreads via the fissures of Santorini and the tympanomastoid suture to involve the temporal bone and skull base [2]. Typical skul base osteomyelitis may also complicate acute otitis media and mastoiditis in children, due to secondary extension of the infectious process within the temporal bone and intracranial compartments through preformed pathways (such as round and oval windows, endolymphatic sac, cochlear aqueduct, etc.), bone erosion, thrombophlebitis and haematogenous seeding. Pseudomonas aeruginosa is the most common pathogen [3]. Patients frequently present with painful otorrhoea and a swollen external auditory canal [4]. Atypical or central skul base osteomyelitis usually originates from a paranasal infection, such as sphenoidal or ethmoidal sinusitis, without associated external otitis [5]. The infection migrates via the Haversian system of the compact bone to access the skull base, where it causes osteitis and osteomyelitis. Various organisms have been implicated, including Aspergillus, Fusobacterium necrophorum, Pseudomonas, Salmonella, Streptococcus and Staphylococcus species [5, 6]. Central skul base osteomyelitis has
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been reported more frequently in children with immunodeficiency (such as anaemia, malnutrition, diabetes or leukopenia) but has also been described in patients with normal immune function [6, 7]. The clinical diagnosis is often difficult due to lack of specific symptoms. In children, skul base osteomyelitis frequently presents with a more severe and acute clinical picture than in adults, but the clinical course is usually shorter and the mortality is lower due to fewer comorbidities [1]. Presenting features may include otorrhoea, otalgia, hearing loss, focal itching and swelling, sinusitis, difficult swallowing and fever [2–5]. Patients often complain of neck pain and sometimes neck stiffness. However, children initially may present with headache as the only symptom, and classic signs of infection may be absent in immunocompromised patients. Cranial neuropathies usually occur later, mimicking symptoms of a posterior fossa tumour [8, 9]. Skul base osteomyelitis may be complicated by sinovenous thrombosis, meningitis, abscesses and ischaemic infarcts. The constellation of these potential complications has been named Lemierre syndrome (LS) [10, 11]. As described by André Lemierre in 1936, “postanginal septicaemia” typically affects otherwise healthy adolescents and is caused by primary oropharyngeal infection resulting in internal jugular vein (IJV) thrombophlebitis, leading to anaerobic septicaemia and metastatic septic embolisation. The most common organism cultured is Fusobacterium necrophorum, an anaerobic bacterium [10]. Symptoms usually start with a sore throat for 4–5 days and then, as the parapharyngeal space infection progresses, patients become pyrexial and generally unwell. Cervical lymphadenopathy may be present and, as IJV thrombophlebitis develops, there may be a tender swelling at the angle of the jaw or anterior to the sternomastoid muscle. Finally, symptoms of haematogenous spread of infection to the lungs, muscles and other softtissue, liver, spleen, kidneys and central nervous system may develop. Nowadays the spectrum of LS has been widened to include primary foci other than the oropharynx, such as sinusitis, otitis, mastoiditis, dental infections and skul base osteomyelitis, and less common organisms such as other anaerobic and aerobic bacteria and fungal species [12]. The incidence and mortality of LS markedly decreased in the postantibiotic era. However, during the past decade there has been a resurgence of the condition, which may reflect a decrease in antibiotic therapy for communityacquired pharyngitis. The current mortality associated with LS remains relatively high (4–12%) [11]. Treatment consists of a prolonged course (usually 8– 12 weeks) of intravenous antibiotics [4, 5]. Adjuvant hyperbaric oxygen therapy has proved effective in the treatment of advanced skul base osteomyelitis [4]. Surgery is reserved primarily for debridement of necrotic bone and inflammatory tissue, biopsy and culture [13]. The role of
anticoagulation in the management of cerebrovascular complications in children remains debated because of its sporadic use and lack of controlled studies [14].
Imaging findings in typical and central skul base osteomyelitis Different imaging modalities may be helpful in assessing children with skul base osteomyelitis, although MRI is probably the most important owing to superior soft-tissue discrimination around the skull base and better depiction of bone marrow abnormalities. CT may sometimes be normal, especially if performed early. Technetium-99 single-photon emission CT (SPECT) and gallium-67 SPECT may be useful when CT/MRI findings are inconclusive or for monitoring the course of the disease [15]. Non-enhanced CT usually shows opacification of the middle ear cavities in typical skul base osteomyelitis, and of paranasal sinuses (particularly the sphenoid sinus and posterior ethmoid cells) in central skul base osteomyelitis. Bone erosion is an important sign that should be carefully sought on bone window, although it may be absent in the early stages [15]. In typical skul base osteomyelitis, bone erosion usually involves the walls of the external auditory canal, mastoid cells and occipital bone (Figs. 1 and 2), while central skul base osteomyelitis erosion predominantly involves the walls of sphenoid sinus and the clivus (Fig. 3). Interestingly, CT may reveal gas bubbles within the marrow spaces of the skull base bones and within the surrounding softtissues, implying the presence of gas-forming organisms (Figs. 4 and 5). Brain MRI usually demonstrates signal changes of the skull base bone marrow with loss of cortical margins and contrast enhancement of the affected regions (Figs. 1 and 2). Diffuse infiltration and enhancement of soft-tissues along the superficial and deep fascial planes around the skull base is frequently associated, extending posteriorly to abut the carotid arteries and obliterating the skull base foramina [16]. This typically corresponds with the clinical features of lower cranial neuropathies; in particular, stylomastoid foramen involvement can lead to facial nerve paralysis, jugular foramen involvement can lead to paralysis of the glossopharyngeal, vagus or accessory nerves, and hypoglossal canal involvement can lead to paralysis of the hypoglossal nerve (Figs. 1 and 4) [4]. On postcontrast studies, fat saturation is necessary to accurately assess skull base enhancement, soft-tissue infiltration and foraminal involvement. After contrast medium administration, fluid collections may be noted in the soft tissue around the skull base and within the involved bone segments. These areas may present
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Fig. 1 Typical skul base osteomyelitis in a 6.5-year-old boy presenting with severe otalgia, otorrhoea and right facial palsy. Staphylococcus cohnii was isolated from drained pus. a Axial contrast-enhanced T1weighted image with fat saturation shows diffuse infiltration and enhancement of the right external auditory canal and retroauricular softtissues associated with a small fluid collection (black arrowhead). There is inflammatory tissue in the mastoid air cells accompanied by dural thickening (white arrowhead) and posterior fossa empyema (open arrow). Note enhancing thrombus within the sigmoid sinus (black arrow).
Coronal T2-weighted image (b) and contrast-enhanced T1-weighted image with fat saturation (c) show intracranial spread of the infection through venous channels, and bone erosions (arrowheads). d The posterior fossa collection (arrow) has high signal on a diffusion-weighted image B=1000. e Reduced apparent diffusion coefficients are demonstrated (arrow) consistent with purulent content. f CT with bone window and coronal reconstruction demonstrates multiple areas of temporal bone erosion (arrowheads). g Phase-contrast MR venography reveals absent flow in the right sigmoid sinus and internal jugular vein (arrow)
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Fig. 2 Typical skul base osteomyelitis in an 8-year-old girl presenting with occipital soft-tissue swelling, fever and pain. CT with bone window and coronal reconstruction (a) and 3-D reconstructions (b) show thickening of the occipital bone with multiple erosions (arrowheads) and loss of cortical margins associated with enlargement of the inferior part of the lambdoid suture (arrow). c Coronal T2-weighted image with
fat saturation clearly depicts expansion and signal changes of the occipital and parietal bone marrow (arrowheads). d Coronal contrast-enhanced T1-weighted image with fat saturation reveals enhancement of the affected bone segments and soft-tissues around the skull base. Note intracranial spread of the infection through the enlarged right lambdoid suture (arrow) and enhancement of posterior fossa dura (arrowheads)
high signal on diffusion-weighted imaging (DWI) and associated decreased apparent diffusion coefficient (ADC), consistent with abscess formation [17]. Purulent
collections are typically located within the clivus (Fig. 4) [18, 19] or in the parapharyngeal spaces (Figs. 3 and 6) in central skul base osteomyelitis, and in the
Fig. 3 Central skul base osteomyelitis in a 6-year-old girl presenting with sore throat and fever. Fusobacterium necrophorum was isolated from drained pus. a CT with bone window and sagittal reconstruction shows opacification of the sphenoid sinus and erosion of the inferior clivus cortex (arrow). Sagittal (b) and coronal (c) contrast-enhanced
T1-weighted images show abnormal clival enhancement (white arrow) associated with an abscess (black arrow) extending laterally in the parapharyngeal spaces (arrowheads). Note the enhancing inflammatory tissue within the sphenoid sinus (asterisk)
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Fig. 4 Central skul base osteomyelitis in a 15-year-old girl presenting with intermittent fever and sore throat followed by neck pain, speech difficulties and right 12th nerve palsy. Group A beta haemolytic Streptococcus was grown on a throat swab. a Axial contrastenhanced CT shows thrombosis of the right sigmoid sinus and internal jugular vein (arrowheads). Gas loculations are present in the clival marrow space (black arrows) and within the right carotid sheath along the internal carotid artery (white arrow), which is markedly narrowed (black open arrow). Corresponding axial T2-weighted (b) and contrast-enhanced T1-weighted (c) images reveal extensive signal changes within the clivus (white empty arrow) associated with an
abscess in the left retropharyngeal space (black arrow) Both internal carotid arteries are encased and narrowed by the inflammatory tissue (black arrowheads). Note the enhancing thrombus occluding the right sigmoid sinus and internal jugular vein (thick white arrow). Following 2 months of antibiotic and anticoagulation therapy, an axial T2weighted image (d) shows that the inflammatory process at the skull base has partially resolved with persistent right sigmoid sinus thrombosis (black arrow) and formation of a small fluid collection within the left clivus (white arrow). There is high signal on diffusion-weighted imaging B=1000 (e, arrow) and reduced apparent diffusion coefficients values (f, arrow)
infratemporal fossa or retroauricular region (Fig. 1) in typical skul base osteomyelitis.
intracranial abscess, cranial neuropathies, venous sinus thrombosis and carotid artery involvement with or without ischaemic infarcts. These must be recognised promptly to institute appropriate treatment. In typical skul base osteomyelitis, brain MRI may show intracranial spread of the infection through venous channels and sutures of the temporal and occipital bones, with extension along the dural sinuses and formation of posterior fossa empyemas (Fig. 1) [3]. In
Imaging of intracranial and cerebrovascular complications in skul base osteomyelitis Several potentially serious complications can arise as a result of skul base osteomyelitis, including meningitis,
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Fig. 5 Central skul base osteomyelitis in a 2.5-year-old boy presenting with fever, drowsiness, left eye swelling and nasal discharge. Coagulasenegative Staphylococcus, Moraxella catarrhalis and Corynebacterium species were isolated from sinus pus. a CT with bone window and coronal reconstruction demonstrates extensive gas loculations within the sphenoid bone. b Axial contrast-enhanced T1-weighted image reveals enhancing soft-tissue within both cavernous sinuses encasing the terminal internal carotid arteries which are extremely narrowed (arrowheads). Note leptomeningeal enhancement over the medulla and along the seventh and
eighth cranial nerves (arrows). c Axial diffusion-weighted image B=1000 after 1 week demonstrates acute bilateral cerebral watershed infarcts and several embolic infarcts in the territory of both middle and anterior cerebral arteries. d Intracranial time-of-flight MR angiography shows that both internal carotid arteries are occluded (arrows) and there is markedly reduced flow in the middle and anterior cerebral arteries (empty arrows), which are filled from the posterior circulation via patent posterior communicating arteries (arrowheads)
central skul base osteomyelitis, brain MRI may reveal intracranial spread of the infection with dural involvement beyond the cavernous sinuses and formation of petroclival abscess and small epidural empyemas at the craniovertebral junction (Fig. 6) [20, 21]. Soft-tissue involvement of the cavernous sinus may be present even without signs of sinus thrombosis. Epidural abscess of the cervical spine may explain some of central skul base osteomyelitis symptoms, such as neck stiffness and restricted movement, cervical lymphadenopathy and localised cervical soft-tissue inflammatory changes [9]. Additional brain parenchymal and leptomeningeal involvement may be noted with enhancement along the lower cranial nerves both in typical and central skul base osteomyelitis (Fig. 5) [8, 9]. Sinovenous thrombosis is a typical complication of skul base osteomyelitis that can be detected easily on postcontrast CT or MRI and on MR venography. This most
frequently affects the transverse-sigmoid sinus and IJV in typical skul base osteomyelitis (Fig. 1), and the IJV and cavernous sinuses in central skul base osteomyelitis (Figs. 4 and 6) [16, 22]. Clot formation is secondary to the contiguous inflammatory process and can propagate to other cerebral venous sinuses with possible occlusion and distal embolism. In particular, the close contiguity of the sigmoid sinus to the mastoid bone and of the cavernous sinus to the sphenoid sinus accounts for their frequent involvement in skul base osteomyelitis. Arterial complications of skul base osteomyelitis are less common and often overlooked. Unilateral or bilateral narrowing of the internal carotid arteries (ICA) may be detected both on CT and MR angiography. In central skul base osteomyelitis, infection and inflammation of the cavernous sinus easily extends to the carotid siphon, causing contiguous inflammatory arteritis. The ICAs usually appear encased by the inflammatory tissue and
Pediatr Radiol Fig. 6 Central skul base osteomyelitis in a 15-year-old boy presenting with sore throat, fever, neck stiffness, dysarthria and right sixth to 12th cranial nerve palsies. Pseudomonas aeruginosa was grown on a throat swab. Coronal (a) and sagittal (b) contrast-enhanced T1-weighted images show abnormal soft tissue in the cavernous sinuses (thin arrows) and cavernous sinus thrombosis associated with extreme narrowing of the cavernous segments of the internal carotid arteries. Inflammatory disease of the sphenoid sinus (open arrow) is accompanied by abnormal clival hypointensity (arrowhead) and inflammation of the skull-base soft tissues. There is thickening of the retroclival dura (white arrowhead) in association with a shallow spinal epidural collection (thick white arrow). Note cerebellar swelling with downward tonsillar herniation (t). Coronal (c) and sagittal (d) contrastenhanced T1-weighted images after 2 months of antibiotics demonstrate almost complete normalisation. In particular, the internal carotid artery narrowing has completely reversed (arrows)
demonstrate enhancement and thickening of the arterial wall consistent with inflammatory changes within the vessel wall (Fig. 4). Narrowing of ICA lumen may also occur in the petrous segment associated with petrositis [13] or in the extracranial segments associated with retropharyngeal abscess [23]. Finally, ICA stenosis may result from simple mass effect or spasm associated with the surrounding inflammatory process. ICA stenosis may be clinically silent, and may reverse on subsequent scans (Fig. 6) [23]. However, patients with central skul base osteomyelitis may develop cerebral infarcts secondary to critical ICA stenosis or septic emboli. In some cases, there is additional evidence of arterial watershed infarctions consistent with cerebral hypoperfusion due to bilateral ICA occlusion (Fig. 5) [24, 25].
Conclusion Skul base osteomyelitis is a serious infection that is potentially life-threatening if not promptly recognised
and treated. Early diagnosis can be challenging, especially in children as they commonly present with nonspecific symptoms, and relies mainly on imaging. It is therefore important for radiologists to be aware the CT and MRI findings of skul base osteomyelitis and its several potentially serious complications. In particular, vascular involvement should be actively scrutinised, and imaging protocols should be targeted to the intracranial and extracranial arterial and venous vasculature.
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