M U S C U L O S K E

M u s c u l o s k e l e t a l I m a g i n g • P i c t o r i a l E s s ay Lacout et al. CT and MRI of Spinal Neuroarthropathy Musculoskeletal Imaging Pictorial Essay

CT and MRI of Spinal Neuroarthropathy Alexis Lacout 1 Caroline Lebreton Dominique Mompoint Samia Mokhtari Christian A. Vallée Robert Y. Carlier Lacout A, Lebreton C, Mompoint D, Mokhtari S, Vallée CA, Carlier RY

OBJECTIVE. The objective of this article is to describe the different stages of spinal neuroarthropathy as assessed by CT and MRI and to discuss their contribution to the management of affected patients. CONCLUSION. Early-stage findings consisted of inflammatory changes involving adjacent vertebral endplates and mimicking degenerative disk disease with inflammation. Subsequently, progression of the lesions led to complete destruction of the intervertebral joint. Knowledge of the initial features of spinal neuroarthropathy may allow earlier treatment, which may improve outcomes.

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pinal neuroarthropathy, also known as Charcot spine, is a destructive process that occurs when neurologic damage causes loss of the protective proprioceptive reflexes. In this article, we describe the different stages of spinal neuroarthropathy as assessed by CT and MRI, and we discuss the contribution of these imaging techniques to the management of affected patients. Materials and Methods Keywords: Charcot spine, CT, MRI, spinal cord lesions, spinal neuroarthropathy DOI:10.2214/AJR.09.2268 Received December 18, 2008; accepted after revision June 18, 2009. 1

All authors: Department of Radiology, Hôpital Raymond Poincaré, Assistance Publique-Hôpitaux de Paris, Université Paris Ile-de-France Ouest, 104 Blvd. Raymond Poincaré, 92380 Garches, France. Address correspondence to A. Lacout.

CME This article is available for CME credit. See www.arrs.org for more information. WEB This is a Web exclusive article. AJR 2009; 193:W505–W514 0361–803X/09/1936–W505 © American Roentgen Ray Society

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Over a 4-year period, approximately 220 patients with severe neurologic impairments due to spinal cord injury were admitted to our unit for initial rehabilitation. During the same period, 800 patients were referred to our unit for evaluation and treatment of impairments from older spinal cord lesions. Among these patients, we identified 10 who had spinal neuroarthropathy and included them in a retrospective study. Our institutional review board approved the study. We reviewed the medical records, including the imaging studies, of the patients with spinal neuroarthropathy. In all these patients, clinical and radiologic examinations were performed at symptom onset and, when possible, later in the course of the disease. Most patients underwent radiography as well as CT and MRI of the lumbar spine. When reviewing the imaging studies, we directed special attention to the detection of destructive lesions, sclerosis, new bone formation, vacuum phenomena within disks, and intervertebral collections. We recorded the site of each lesion (e.g.,

diskovertebral unit or facet joints). Percutaneous needle biopsy for bacteriologic and pathologic studies was performed when infection was suspected. Whenever possible, we evaluated the clinical and radiologic outcomes after treatment.

Results We identified 10 patients with spinal neuroarthropathy (Table 1). The underlying diagnosis was traumatic paraplegia in seven patients, Guillain-Barré syndrome in one patient, transverse myelitis in one patient, and Friedreich’s ataxia in one patient. Presenting symptoms consisted of lumbar pain in six patients, worsening of the neurologic deficit in three, and kyphosis or instability in three. One patient had a fever related to infection of an intervertebral collection. The patient with Friedreich’s ataxia lost the ability to walk at 41 years old and experienced the first symptoms of spinal neuroarthropathy at 47 years old. In the other patients, the symptoms developed several years after the injury (mean, 19 years; range, 5–40 years). The initial CT and MRI studies showed inflammatory changes of the vertebral endplates in three patients (patients 1, 2, and 6). On MRI, the affected endplates generated high signal on the T2-weighted and STIR sequences as well as on the gadolinium-enhanced T1-weighted sequence. Bone erosions were also visible in these three patients. In the other seven patients, destruction and sclerosis of the diskovertebral unit

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5 (Fig. 5)

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Friedreich’s ataxia

Traumatic paraplegia (T4 ASIA A)

Paraplegia, Guillain-Barré syndrome (T4 ASIA C)

Traumatic paraplegia (T4 ASIA A), lumbar arthrodesis, L5–S1 not fixed

Paraplegia secondary to an aortic dissection (T4 ASIA A)

Traumatic paraplegia L1

Traumatic paraplegia (T10 ASIA A)

Traumatic paraplegia (T10 ASIA A)

Paraplegia due to transverse myelitis (T6 ASIA A)

Traumatic paraplegia (T9 ASIA A)

Neurologic Impairment (Classification)

Birth (loss of march at 41 y)

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47

6

44

18

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45

27

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Age at Impairment (y)

Increased lumbar pain

Fever (infection of a lumbar collection)

Kyphosis, increased motor deficit

Positional lumbar pain, increased urinary dysfunction

Lumbar pain

Increased urinary dysfunction

Lumbar pain

Positional lumbar pain

Increased lumbar pain, kyphosis

Kyphosis, instability

Symptoms

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37

57

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65

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Age at Presentation (y)

L4–L5, L5–S1

L4–L5

L2–L3, L4–L5

L5–S1

L3–L4, L4–L5, L5–S1

L1–L2

L4–L5

L3–L4

L2–L3

L5–S1

Localization

Destruction and sclerosis, posterior joint involvement, intervertebral collection

Destruction and sclerosis, new bone formation, posterior joint involvement, infected collection, discal vacuum

Destruction and sclerosis, new bone formation, posterior joint involvement, discal vacuum

Destruction and sclerosis, new bone formation, posterior joint involvement, intervertebral collection

Destruction and sclerosis, new bone formation, posterior joint involvement, intervertebral collection

Destruction and sclerosis, new bone formation, posterior joint involvement, intervertebral collection

Destruction and sclerosis, new bone formation, posterior joint involvement

Destruction and sclerosis, new bone formation, posterior joint involvement, intervertebral collection

Bony erosions and sclerosis, inflammation of the vertebral endplates, posterior joint involvement

Bony erosions and sclerosis, inflammation of the vertebral endplates, rare erosions of the posterior joints

Initial Imaging Findings

Note—For classification of neurologic impairment, T = thoracic cord, ASIA = American Spinal Injury Association impairment classification, L = lumbosacral.

Sex

Patient No.

TABLE 1:  CT and MRI Findings of Axial Involvement in Patients With Charcot Spine

Arthrodesis planned

Drainage of the infected collection

Stability (3 mo later), arthrodesis (26 mo later)

L5–S1 arthrodesis (7 mo later), L1–L2 involvement (17 mo after arthrodesis)

No surgical treatment planned

No surgical treatment planned

Increase of destruction, increase of sclerosis, vertebral collection (33 mo later), mobility; no surgical treatment planned

Arthrodesis planed

Destruction, increase of sclerosis, new bone formation, discal vacuum (15 mo later)

Destruction, increase of sclerosis, posterior joint involvement (9 mo later); arthrodesis planned

Follow-Up

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CT and MRI of Spinal Neuroarthropathy were seen (Figs. 1–8). Newly formed bone was visible in eight patients (Figs. 2–8). The facet joints were consistently involved (Figs. 3 and 5). In seven patients, we found an intervertebral collection, which was infected in one patient (Figs. 3, 4, 6, and 7). Vacuum phenomena within a disk were noted in three patients (Figs. 2 and 8). The lesions were located near the lumbosacral junction (L4–L5 or L5–S1) in seven patients and near the thoracolumbar junction (L1–L2) in two patients. Dynamic standard radiographs showed vertebral mobility in one patient (Fig. 4). Follow-up CT or MRI was performed in five patients. There was no change in one patient after 3 months. In three patients, the mean interval between the two evaluations was 19 months (range, 9–33 months) and worsening of the destructive lesions was noted. The remaining patient was treated with arthrodesis, after which spinal neuroarthropathy lesions developed above and below the fixation (L1–L2 and L5–S1) (Fig. 7). Discussion Spinal neuroarthropathy, or Charcot spine, is a process of progressive aseptic destruction of the spine that can complicate a variety of neurologic disorders associated with loss of proprioception and pain sensation, such as tabes dorsalis [1, 2], traumatic brain or spinal cord injury [3], diabetes mellitus [2], and congenital insensitivity to pain [4]. The destructive process involves the disk, adjacent vertebral bodies, and facet joints [5, 6]. Pain and position sense play a key role in joint protection by avoiding joint overuse associated with microtrauma [7]. When pro­ prioception and pain sensation are lost, repeated microtrauma to the joint occurs, leading to joint damage. Thus, neuroarthropathy develops only in mobile joints [7]. The joint damage caused by microtrauma further increases joint mobility, thus creating a vicious circle. In most of our patients, the neuroarthropathic lesions developed at spinal levels characterized by considerable mobility—that is, near the thoracolumbar or lumbosacral junction or just above and below an orthopedic fixation. Vacuum phenomena within the disk, present in three of our patients, indicate mobility of the affected spinal level. In patients with neurologic impairment due to spinal cord injury or disease, symptoms that may prompt imaging studies of the spine consist of increasing spasticity, autonomic hyperreflexivity, increasing pain during transfers, and spinal instability. However, the clin-

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ical diagnosis is difficult and often delayed because the classical symptoms are lacking. The radiologist should carefully examine each diskovertebral unit for changes suggesting spinal neuroarthropathy, especially at the thoracolumbar and lumbosacral junctions. We identified two stages in the development of spinal neuroarthropathy (Fig. 9). Initially, nonspecific inflammatory changes were visible in two adjacent endplates. These changes may mistakenly suggest disk degeneration with inflammation. However, neuroarthropathy should be considered in patients who have neurologic conditions associated with loss of proprioception and pain sensation. Vacuum phenomena in the disk or facet joints may be present. This finding may indicate exaggerated local mobility as the precipitating factor of the neuroarthropathy. In patients with later-stage spinal neuroarthropathy, destruction of the diskovertebral unit and facet joints was apparent. Concomitant bone sclerosis and new bone formation were noted. These findings were consistent with earlier data [5, 6]. Neuroarthropathy may be difficult to distinguish from infection [5]. Furthermore, infection may complicate neuroarthropathy [8, 9], although the primary process is aseptic. In a study comparing 19 patients with proven disk space infection and 14 patients with spinal neuroarthropathy investigated by CT or MRI, the best discriminators were intradiscal vacuum phenomena, osseous debris, facet joint involvement, joint disorganization (spondylolisthesis and dislocations), and signal patterns on T2-weighted and gadolinium-enhanced T1-weighted MRI sequences [5]. In neuroarthropathy, the vertebral bodies usually generate high-intensity signal on T2-weighted and gadolinium-enhanced T1weighted sequences, whereas the signal abnormalities are usually confined to the endplates in infection [5]. The disks usually exhibit rim enhancement in neuroarthropathy and diffuse high signal in infection [5]. However, no sign is entirely specific for neuroarthropathy [5]. Percutaneous biopsy with bacteriologic examination, which was performed in one of our patients, may be required. Another important differential diagnosis is primary or metastatic vertebral tumor [6]. The clinical picture often suggests a malignancy, and histologic examination of a percutaneous biopsy specimen can establish the diagnosis. The treatment of spinal neuroarthropathy relies on immobilization of the affected spi-

nal levels. Surgery typically consists of reduction of the deformities, posterolateral spinal fusion with hooks and pedicular screws, and posterior lumbar interbody fusion [10, 11]. The resulting shift in mechanical loading to other levels, together with mobility just above or below the internal fixation, may lead to the development of neuroarthropathy at other spinal sites [12]. This complication occurred in one of our patients. An early diagnosis may help to improve the management of spinal neuroarthropathy because early treatment at the stage of isolated inflammation might prevent the development of destructive lesions. We suggest that MRI may be the most sensitive investigation for detecting early-stage spinal neuroarthropathy. In conclusion, the early stages of spinal neuroarthropathy may mimic inflammatory disk degeneration. Thus, MRI shows high signal from the vertebral endplates on T2weighted, STIR, and gadolinium-enhanced T1-weighted sequences, as well as bone erosions. CT and MRI may allow an earlier diagnosis, thereby improving treatment efficacy. Radiologists should be familiar with the imaging findings, particularly those present at the early stage. References 1. Allali F, Rahmouni R, Hajjaj-Hassouni N. Tabetic arthropathy: a report of 43 cases. Clin Rheumatol 2006; 25:858–860 2. Race MC, Keppler JP, Grant AE. Diabetic Charcot spine as cauda equina syndrome: an unusual presentation. Arch Phys Med Rehabil 1985; 66: 463–465 3. Mohit AA, Mirza S, James J, Goodkin R. Charcot arthropathy in relation to autonomic dysreflexia in spinal cord injury: case report and review of the literature. J Neurosurg Spine 2005; 2:476–480 4. Sliwa JA, Rippe D, Do V. Charcot spine in a person with congenital insensitivity to pain with anhydrosis: a case report of re-diagnosis. Arch Phys Med Rehabil 2008; 89:568–571 5. Wagner SC, Schweitzer ME, Morrison WB, Przybylski GJ, Parker L. Can imaging findings help differentiate spinal neuropathic arthropathy from disc space infection? Initial experience. Radiology 2000; 214:693–699 6. Park YH, Taylor JA, Szollar SM, Resnick D. Imaging findings in spinal neuroarthropathy. Spine 1994; 19:1499–1504 7. Crim JR, Bassett LW, Gold RH, et al. Spinal neuroarthropathy after traumatic paraplegia. AJNR 1988; 9:359–362 8. Suda Y, Saito M, Shioda M, Kato H, Shibasaki K.

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agishi M. Surgical treatment of Charcot spine. J Spinal Disord Tech 2007; 20:85–88 11. Arnold PM, Baek PN, Stillerman CB, Rice SG, Mueller WM. Surgical management of lumbar neuropathic spinal arthropathy (Charcot joint) af-

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ter traumatic thoracic paraplegia: report of two cases. J Spinal Disord 1995; 8:357–362 12. McBride GG, Greenberg D. Treatment of Charcot spinal arthropathy following traumatic paraplegia. J Spinal Disord 1991; 4:212–220

Fig. 1—40-year-old man in whom L5–S1 spinal neuroarthropathy developed 11 years after traumatic paraplegia (thoracic cord 9, American Spinal Injury Association impairment classification A [T9 ASIA A]). A and B, Sagittal fat-saturated fast spin-echo T1weighted image after gadolinium injection (A) and CT scan with coronal reformation (B) show disk space narrowing, erosions, and slight endplate enhancement. These findings mimic degenerative disk disease with inflammatory changes (arrowheads). C and D, Sagittal fat-saturated fast spin-echo T2-weighted image (C) and CT scan with sagittal reformation (D) obtained 9 months after A and B show progression to complete destruction of diskovertebral unit with bone fragmentation and sclerosis (arrows).

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CT and MRI of Spinal Neuroarthropathy

Fig. 2—34-year-old man in whom L2–L3 spinal neuroarthropathy developed 7 years after traumatic paraplegia (thoracic cord 6, American Spinal Injury Association impairment classification A [T6 ASIA A]). A and B, CT scan with sagittal reformation (A) and sagittal fat-saturated fast spin-echo T1-weighted image after gadolinium injection (B) show erosions, sclerosis, and slight endplate enhancement (arrows). These findings mimic degenerative disk disease with inflammatory changes. C and D, CT scan with sagittal reformation (C) and coronal STIR image (D) obtained 15 months after A and B show destruction of diskovertebral unit (thin arrows) with vacuum phenomenon within disk and new bone formation (thick arrows, D).

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Fig. 3—65-year-old woman with L3–L4 spinal neuroarthropathy 20 years after traumatic paraplegia (thoracic cord 10, American Spinal Injury Association impairment classification A [T10 ASIA A]). A and B, CT scans with coronal (A) and axial (B) reformations show complete destruction of diskovertebral unit and zygapophyseal joints, with abundant osseous debris extending beyond vertebral body (arrows) and intervertebral collection (arrowheads). C, CT scan with volumetric reformation shows complete destruction of L3 and L4 with osseous fragmentation (arrow).

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Fig. 4—58-year-old man in whom L4–L5 spinal neuroarthropathy developed 27 years after traumatic paraplegia (thoracic cord 10, American Spinal Injury Association impairment classification A [T10 ASIA A]). A and B, CT scans with sagittal (A) and axial (B) reformations show destruction (arrowheads), sclerosis (thin arrows), and new bone formation (thick arrows, A). C, CT scan with sagittal reformation obtained 33 months after A and B shows increased destruction of diskovertebral unit and central vertebral collection (star). D, Lateral dynamic radiograph of lumbar spine shows posterior and inferior displacement of L5 (star) between S1 (thin arrow) and L4 (thick arrow).

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CT and MRI of Spinal Neuroarthropathy

Fig. 5—58-year-old man in whom L1–L2 spinal neuroarthropathy developed 40 years after traumatic paraplegia (lumbosacral cord [L1]). A and B, Sagittal fast spin-echo T1-weighted (A) and coronal fast spin-echo T2-weighted (B) images show complete destruction of diskovertebral unit, intervertebral collection (star), and formation of abundant new bone (arrows, B). C and D, Lateral (C) and anteroposterior (D) radiographs of lumbar spine show anterior and lateral new bone formation in diskovertebral unit (thick arrows) and zygapophyseal joints (thin arrow, C).

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Fig. 6—57-year-old man with L3–L4, L4–L5, and L5–S1 spinal neuroarthropathy 13 years after aortic dissection responsible for paraplegia (thoracic cord 4, American Spinal Injury Association impairment classification A [T4 ASIA A]). A and B, Coronal reformation (A) and sagittal STIR (B) CT scans show lesions of L3–L4, L4–L5, and L5–S1 (thin arrows, B). At L3–L4, note intervertebral collection (star, B) and abundance of new bone (thick arrows, A). At L4–L5 and L5–S1, lesions are less severe and consist of disk space narrowing and endplate erosions (arrowheads, A). C, Anteroposterior radiograph of lumbar spine shows lateral new bone formation (arrows).

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Fig. 7—37-year-old man in whom L5–S1 spinal neuroarthropathy developed 29 years after traumatic paraplegia (thoracic cord 4, American Spinal Injury Association impairment classification A [T4 ASIA A]). A–C, Sagittal fast spin-echo T1-weighted (A) and sagittal (B) and coronal (C) fast spin-echo T2-weighted images show destruction of L5–S1 diskovertebral unit (arrow, A and B) and intervertebral collection (stars). Lesions developed just below orthopedic fixation. (Fig. 7 continues on next page)

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Fig. 7 (continued)—37-year-old man in whom L5–S1 spinal neuroarthropathy developed 29 years after traumatic paraplegia (thoracic cord 4, American Spinal Injury Association impairment classification A [T4 ASIA A]). D and E, CT scans with sagittal (D) and axial (E) reformations show destruction, intervertebral collection (stars), and abundant osseous debris extending beyond vertebral body (arrowheads) and into spinal canal. This patient underwent orthopedic fixation 7 months later. F, CT scan with coronal reformation obtained 17 months after surgery shows orthopedic fixation at L5–S1 (arrow) and development of L1–L2 lesions just above orthopedic fixation (arrowhead).

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Fig. 8—52-year-old woman in whom L2–L3 and L4– L5 spinal neuroarthropathy developed 5 years after Guillain-Barré syndrome responsible for paraplegia (thoracic cord 4, American Spinal Injury Association impairment classification C [T4 ASIA C]). A and B, Coronal fat-saturated fast spin-echo T1weighted image after gadolinium injection (A) and CT scan with coronal reformation (B) show destruction (thin white arrow, A), new bone formation (thick arrows), sclerosis, vacuum phenomena in disk (black arrows), and L2–L3 enhancement.

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Vertebral collection

Inflammatory signal on MRI

Changes best depicted on CT

Stages of the disease

Changes best depicted on MRI

Destruction, fragmentation, new bone formation

Bony erosions

Fig. 9—Graphic shows stages of development of spinal neuroarthropathy.

F O R YO U R I N F O R M AT I O N

This article is available for CME credit. See www.arrs.org for more information.

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