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Musculoskeletal Imaging • Original Research

Lee et al.
MRI of Candida Spondylitis

Musculoskeletal Imaging
Original Research
Downloaded from www.ajronline.org by 36.81.41.167 on 08/10/21 from IP address 36.81.41.167. Copyright ARRS. For personal use only; all rights reserved

Candida Spondylitis: Comparison


of MRI Findings With Bacterial and
Tuberculous Causes
Sheen-Woo Lee1 OBJECTIVE. Candida spondylitis is relatively uncommon and is usually encountered
Sang Hoon Lee2 as an opportunistic infection. We analyzed the MRI characteristics of biopsy-proven cases
Hye Won Chung2 of Candida spondylitis, and compared the findings with bacterial or tuberculous spondylitis.
Min Jee Kim 3 MATERIALS AND METHODS. The study included patients with infectious spondyli-
Min Jeong Seo 4 tis who underwent MRI and biopsy from 1998 to 2011 (60 patients; mean age 56 ± 18 years).
MR images were analyzed with respect to the number of involved vertebrae, contrast en-
Myung Jin Shin2
hancement pattern, signal intensity of spinal inflammatory masses on T2-weighted imaging,
Lee SW, Lee SH, Chung HW, Kim MJ, Seo MJ, paraspinal abscess size, intervertebral disk destruction, subligamentous spread, and skip le-
Shin MJ sions. The Fisher exact test and analysis of variance were used for statistical analysis.
RESULTS. There were 10 cases of Candida spondylitis, and 29 and 21 cases of bacterial and
tuberculous spondylitis, respectively. On MRI, disk destruction was seen in 50%, 93%, and 30%
of Candida, bacterial, and tuberculous cases, respectively. Subligamentous spread of infection
was noted in 22%, 10%, and 85%. Paraspinal inflammatory masses were seen in 100%, 100%,
and 76%, and abscesses in 100%, 66%, and 90%, of Candida, bacterial, and tuberculous cases,
respectively. Paraspinal inflammatory masses contained low T2 signal intensity portions in 80%,
21%, and 67%, and skip lesions were seen in 0%, 10%, and 14%, respectively. Small abscesses
were noted in 100%, 76%, and 35% of Candida, bacteria, and tuberculosis infections, respec-
tively. Candida involved 2.3 ± 0.4 vertebrae compared with 2.3 ± 0.9 and 3.0 ± 1.7 in bacterial
and tuberculous, respectively. Differences in the three groups were statistically significant (p <
Keywords: Candida, fungus, infectious spondylitis, MRI, 0.05) except for the number of involved vertebrae, and skip lesions.
opportunistic infection CONCLUSION. Candida spondylitis can be suspected when infectious lesions contain
low-signal spinal inflammatory masses on T2-weighted imaging, small paraspinal abscesses,
DOI:10.2214/AJR.12.10344 and in immunocompromised patients.
Received November 20, 2012; accepted after revision

T
February 1, 2013. he risk of fungal infection is istics of biopsy-proven cases of Candida in-
closely related with the immuno- fection are analyzed and compared with those
Presented at the 2008 annual meeting of the Radiological compromised state [1]. Although of the other more common causes of infec-
Society of North America.
the CT and MRI findings of pyo- tious spondylitis. Our objective was to iden-
1
Department of Radiology, Gachon University Gil Medical genic or tuberculous spondylitis are well tify the MRI characteristics of Candida spon-
Center, Inchoen, Korea. known, those of fungal spondylitis are not dylitis, and thus aid in its diagnosis.
well characterized in the literature [2]. Fun-
2
Department of Radiology, Asan Medical Center, gal spondylitis is difficult to diagnose clini- Materials and Methods
University of Ulsan College of Medicine, 388-1 Pungnap-2
dong, Songpa-gu, Seoul, Korea. Address correspondence
cally or pathologically, and thus, treatment is With approval from our institutional review board,
to S. H. Lee (shlee@amc.seoul.kr). commonly delayed [1]. we retrospectively studied 352 patients who were
Fungal spondylitis occurs primarily as an admitted into our institute for infectious spondylitis
3
Department of Radiology, Seoul Medical Center, Seoul, opportunistic infection [1], and Candida and from 1998 to 2011. Medical records were reviewed
Korea.
Aspergillus species are the most common and clinical data and histopathologic findings were
4
Department of Radiology, Seoul Veteran’s Hospital, causative fungal organisms. Few cases of Can- investigated. The inclusion criteria were as follows:
Seoul, Korea. dida spondylitis have been reported and little prebiopsy MRI, including T1- and T2-weighted sag-
is known of its MRI characteristics. Further- ittal and axial imaging and contrast-enhanced stud-
AJR 2013; 201:872–877
more, no study has systematically compared ies; CT-guided percutaneous needle biopsy or open
0361–803X/13/2014–872 the imaging characteristics of Candida spon- surgical biopsy of the infected spine area; and a pos-
dylitis and those of bacterial and tuberculous itive pathogen yield by the biopsy. Patients whose
© American Roentgen Ray Society spondylitis. In this article, the MRI character- medical record was unavailable; those without MRI;

872 AJR:201, October 2013


MRI of Candida Spondylitis

or those with limited MR image quality, such as rim-enhancing component were categorized as ab- ment or prolonged hospitalization associated
shading artifact by spine coil or who had a negative scesses. Further analyses of the paraspinal inflam- with burst fracture or intestinal adhesion (Ta-
result on the direct biopsy, were excluded. The final matory mass and abscess were done in the follow- ble 1). On the other hand, 10% of the pyo-
study cohort consisted of 60 patients (23 women and ing manner. Paraspinal inflammatory lesions were genic spondylitis patients and none of the
37 men) of mean age 56 ± 18 years. analyzed and categorized as diffusely high or heter- tuberculous spondylitis patients had such
The MRI systems and pulse sequences used ogeneously low signal intensity compared with the conditions. Ten percent of the Candida spon-
were varied because some of the imaging stud- adjacent muscle on axial T2-weighted imaging. The dylitis patients had undergone a recent inva-
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ies were performed at outside institutions, but all abscess size was categorized into large or small ac- sive spinal procedure, such as, epidural in-
studies were performed using a 1.5-T magnet. Im- cording to whether the individual cavity exceeded jection or spine surgery, whereas 48% and
aging sequences included spin-echo T1-weighted, half of the diameter of the vertebral body. MR im- 5% of pyogenic and tuberculous spondylitis
T2-weighted without fat suppression, and gado- ages were also reviewed twice by a radiologist un- patients, respectively, had done so. The re-
linium-enhanced T1-weighted with or without fat aware of causative organisms. spective durations of symptoms were 21 ± 44
suppression. Imaging included axial and sagittal Statistical differences between the three patho- months (median, 4 months), 2.0 ± 2.0 months
planes in all cases. genically different spondylitis types were ana- (median, 1 month), and 14 ± 26 months (me-
Two musculoskeletal radiologists with 12 and lyzed using the Fisher exact test and analysis of dian, 5 months) in Candida and bacterial and
4 years of experience analyzed the MR images by variance. The correlation coefficient (R2) was cal- tuberculous spondylitis patients, respective-
consensus. The following MRI data were evaluat- culated to find out the possibility of association ly. Mean patient age was 60 years (45–73
ed for each patient: the locations of involved bones, between the low signal intensity on T2-weighted years) in the Candida spondylitis group, 60
number of involved vertebra, presence of interver- imaging and the symptom duration or the patient’s years (15–82 years) in the bacterial spondy-
tebral disk destruction, subligamentous spread of age. Analysis was performed using SPSS for Win- litis group, and 47 years (12–83 years) in the
inflammation, skip lesions, contrast enhancement dows, version 12.0. Statistical significance was ac- tuberculous spondylitis group.
pattern of the paraspinal soft-tissue lesion, signal cepted for p values of < 0.05. On MRI, intervertebral disk destruction was
intensity of the spinal inflammatory mass by T2- observed in 50%, 93%, and 30% of Candida,
weighted imaging, and paraspinal abscess size. Results bacterial, and tuberculous cases (Fig. 1), and
Intervertebral disk destruction was defined as There were 10 cases of Candida spondy- subligamentous spread of infection was noted
breach of the subchondral cortex by extension of the litis, 29 cases of bacterial spondylitis, and 21 in 22%, 10%, and 85% of Candida, bacterial,
infectious lesion through the endplate into the disk, cases of tuberculous spondylitis. The cervical and tuberculous cases, respectively. A skip le-
with loss of the disk height on sagittal images. Sub- spine was not involved in any patients with sion was present in 10% of pyogenic and 14%
ligamentous spread of inflammation was defined as Candida spondylitis or tuberculous spondyli- of tuberculous spondylitis cases. Candida
an inflammatory mass or abscess under the anteri- tis but was involved in two patients with bac- spondylitis involved 2.3 ± 0.4 vertebrae com-
or longitudinal ligament. Skip lesion was defined terial spondylitis. The thoracic spine was in- pared with 2.3 ± 0.9 in bacterial spondylitis and
as spondylitis at different vertebral levels without volved in one Candida, three bacterial, and 3.0 ± 1.7 in tuberculosis. Diffusely enhancing
intervening level involvement. The numbers of in- five tuberculous spondylitis patients. The paraspinal inflammatory masses were seen in
volved vertebrae were determined by counting in- thoracolumbar junction was involved in one 100%, 100%, and 76%, and rim-enhancing ab-
volved vertebral bodies. Contrast enhancement bacterial and one tuberculous spondylitis pa- scesses in 100%, 66%, and 90%, of Candida,
patterns of the paraspinal soft-tissue lesions were tient, and the lumbar spine was involved in bacterial, and tuberculous cases, respectively.
assessed by reviewing the axial set of T1-weight- 10 Candida, 21 bacterial, and 16 tuberculous Low-signal-intensity paraspinal mass on T2-
ed, T2-weighted, and contrast-enhanced images. spondylitis patients. weighted imaging was noted in 80%, 21%,
The soft-tissue lesions outside the vertebral body A review of clinical data showed that 90% and 67% of Candida, bacterial, and tubercu-
showing low signal intensity on T1-weighted im- of the Candida spondylitis patients were im- lous cases, respectively (Fig. 2), whereas T2-
aging and diffuse enhancement were categorized as munocompromised or had other long-stand- high-signal-intensity paraspinal lesions were
paraspinal inflammatory masses, and those with a ing debilitating disease due to cancer treat- seen in 20%, 79%, and 24%, respectively (Fig.
2). Large confluent paraspinal abscesses were
TABLE 1: Underlying Diseases of Patients With Candida Spondylitis seen in 24% and 65% of bacterial and tuber-
Patient No. Underlying Disease culous cases, but none in Candida spondyli-
1 Paraplegia due to bursting fracture of thoracic spine tis (Figs. 2 and 3). Small abscesses were noted
in 100%, 76%, and 35% of Candida, bacteria,
2 Bedridden due to intestinal adhesion and fracture after motor vehicle accident
and tuberculosis infections, respectively.
3 Chemotherapy due to lung cancer The correlation coefficient (R2) values be-
4 After colon cancer operation tween the T2 signal intensity and the symptom
5 After colon cancer operation duration or the patient’s age, calculated based
on the hypothesis that the longer the symptom
6 After fusion and revision for spinal stenosis
duration or the older the patient, the lower the
7 Hepatocellular carcinoma, alcoholic liver cirrhosis T2 signal intensity, were 0.215 and 0.001, re-
8 After diskectomy spectively. The low R2 values suggest that the
9 Esophagus and lung cancer symptom duration or age does not cause sig-
nificant effect on the T2 signal intensity. A
10 Spine anesthesia for bladder tumor removal, 20-year history of diabetes mellitus
summary of results is provided in Table 2.

AJR:201, October 2013 873


Lee et al.

Differences between the imaging findings TABLE 2: Spectrum of Imaging Findings of Candida Spondylitis, Bacterial
in the three groups were statistically signifi- Spondylitis, and Tuberculous Spondylitis
cant (p < 0.05) except for the number of in- Spondylitis
volved vertebrae (p = 0.09) and presence of MRI Findings Candida Bacterial Tuberculous
skip lesions (p = 0.54).
Intervertebral disk destruction 50 93 30
Discussion Subligamentous spread 22 10 85
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The incidences of fungal infections have Skip lesion 0 10 14


increased because of the greater use of im- Contrast enhancement pattern of paraspinal lesion
munosuppressants, prolonged use of broad-
spectrum antibiotics and indwelling cathe- Diffuse enhancing inflammatory mass 100 100 76
ters, and the higher prevalence of AIDS [1, Rim-enhancing abscess 100 66 90
3]. Nevertheless, fungal spine infections still Low T2 signal intensity of inflammatory mass 80 21 67
have much lower incidences than bacterial
No. of involving vertebrae (p = 0.09) 2.3 2.3 3.0
and tuberculous infections [4]. Knowledge of
the disease itself is limited, and the diagnosis Large paraspinal abscess 0 24 65
is based on exclusion rather than definite di- Small paraspinal abscess 100 76 35
agnostic criteria. In a clinical study, Frazier et Note—Findings with statistical significance (p < 0.05) are in bold. All data are presented as percentages
al. [1] analyzed 11 cases in three tertiary cen- except for number of involving vertebrae.
ters over the course of 16 years, causative or-
ganisms included Candida, Aspergillus, and
Coccidioides species. According to another or weaker proteolysis will result in atypical as significant as the hypothesis. Further study
researcher, the initial clinical manifestations forms of spondylitis that can mimic tubercu- may be necessary in larger number of groups
of Candida infections are usually mild and losis or even a metastatic mass. For example, comparing CT and MRI side by side.
nonspecific. This report concluded that ear- if the pathogen is low in virulence or the host- The limitations of our study are as follows:
ly diagnosis of fungal spondylitis depends on immune reaction is low, the inflammatory tis- Only patients with a biopsy-proven pathogen
a high index of suspicion and clinical judg- sue reaction will be low grade and long-stand- were included in this study. According to oth-
ment, especially in patients with a history of ing, resulting in fibrosis in the inflammatory er researchers, infectious agents are found by
immunosuppression or of travel to endemic mass and a low tissue-water component, and biopsy in fewer than 70% of infectious spon-
areas [5]. MRI can aid the diagnosis, but ra- the resulting signal intensity will be low on T2- dylitis cases [11, 12]. In the current study, pa-
diologic findings have not been evaluated in weighted imaging [7–9]. The pathologic diag- tients diagnosed with infectious spondylitis
previous studies. Published imaging studies noses of the cases in our study described chron- by imaging without a definite pathogen yield
of fungal spondylitis involve anecdotal re- ic inflammation and fibrosis and support our were treated with empirical antimicrobials,
ports in the form of case studies, and the larg- hypothesis. Hence, chronic inflammation and and exclusion of these patients might have
est report issued on the subject involved three fibrosis in Candida spondylitis and formation led to selection bias and a higher proportion
cases and no comparison with other causes of of paraspinal abscess cavities can resemble tu- of atypical and severe cases. The cases in our
infectious spondylitis [6]. berculous spondylitis in some cases (Fig. 3). In study did not involve the cervical spine, but
In this study, we analyzed the MRI find- addition, some species of fungus have been re- our literature search shows that cervical spine
ings of Candida spondylitis, the most com- ported to synthesize paramagnetic substances, is not immune to Candida infection albeit un-
mon fungal spondylitis in the immunocom- such as, melanin (a T2-shortening substance), usual [1, 13–15]. The study was retrospective
promised population, and we compared these which contributes to low signal intensity [10]. in nature, and some of the clinical informa-
with the findings of pyogenic and tubercu- The list of pathologic reports of our Candida tion on the medical record, such as the histo-
lous spondylitis. Our results indicate that spondylitis patients included chronic osteomy- ry of antibiotic therapy before the visit to our
Candida spondylitis should be suspected if elitis, dense fibrous tissue with calcifications, tertiary medical center, was incomplete. Fur-
MRI shows spondylitis in two adjacent ver- chronic granulomatous inflammation with ne- thermore, although our cases were collected
tebral bodies, with small paraspinal abscess, crosis, fibrinous exudate, marrow fibrosis with over 10 years, the sample size was small.
or with phlegmon, which on T2-weighted mild chronic inflammation, degenerated and In conclusion, Candida spondylitis should
imaging is of lower signal intensity in con- necrotic synovial tissue, extensive degeneration be considered when the infectious lesions in-
trast to the high signal intensity expected of of cartilage with granulation tissue, and chron- volve contiguous vertebrae without interver-
inflammatory lesions in cases with a pyogen- ic granulomatous inflammation with necrosis. tebral disk destruction with paraspinal in-
ic or tuberculosis infection. Less interverte- In addition, underlying degenerative osteo- flammatory mass of unusually low signal
bral disk involvement may also suggest Can- phytosis may contribute to the T2 low signal intensity, and paraspinal abscess, when pres-
dida rather than pyogenic spondylitis. intensities of lesions in elderly patients. But ent, is small. A clinical history of chronic ill-
The well-known differences between pyo- the R2 value in our study between the patients’ ness would be helpful during the differential
genic and tuberculous spondylitis depend on age and the T2 hypointensity, which can be diagnosis. These MRI findings may alert clini-
the virulence of the pathogen, aggressive prote- seen in degenerative spur formation, did not cians to the possibility of a rare cause of spon-
olysis, and host-immune reactions. Variable indicate any relevance, suggesting that the ef- dylitis and thus aid antimicrobial selection and
host interactions with bacteria of low virulence fect of degenerative spine lesions may not be patient management.

874 AJR:201, October 2013


MRI of Candida Spondylitis

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1. Frazier DD, Campbell DR, Garvey TA, Wiesel S, A, Johnson DW, Welch W. Fungal spinal osteo- eneck K. CT-guided spinal biopsy in spondylodisci-
Bohlman HH, Eismont FJ. Fungal infections of the myelitis in the immunocompromised patient: MR tis [in Danish]. Ugeskr Laeger 1998; 160:5931–5934
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low-up. J Bone Joint Surg Am 2001; 83-A:560–565 7. Hsu CY, Yu CW, Wu MZ, Chen BB, Huang KM, crobiologically verified diagnosis of infectious
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3:450–460 tastases. AJNR 2008; 29:1104–1110 13. Lee DG, Park KB, Kang DH, Hwang SH, Jung
3. Gamaletsou MN, Kontoyiannis DP, Sipsas NV, et 8. Tins BJ, Cassar-Pullicino VN, Lalam RK. Mag- JM, Han JW. A clinical analysis of surgical treat-
al. Candida osteomyelitis: analysis of 207 pediat- netic resonance imaging of spinal infection. Top ment for spontaneous spinal infection. J Korean
ric and adult cases (1970–2011). Clin Infect Dis Magn Reson Imaging 2007; 18:213–222 Neurosurg Soc 2007; 42:317–325
2012; 55:1338–1351 9. Ahmadi J, Bajaj A, Destian S, Segall HD, Zee CS. 14. Khazim RM, Debnath UK, Fares Y. Candida albi-
4. Gouliouris T, Aliyu SH, Brown NM. Spondylodis- Spinal tuberculosis: atypical observations at MR cans osteomyelitis of the spine: progressive clinical
citis: update on diagnosis and management. J Anti- imaging. Radiology 1993; 189:489–493 and radiological features and surgical management
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B
Fig. 1—Candida spondylitis.
A, MR images (T2-weighted, T1-weighted, and contrast-enhanced, respectively) show Candida spondylitis
infection in lumbar spine in 68-year-old man, with little intervertebral disk destruction (arrow).
B, MR images (T2-weighted, T1-weighted, and contrast-enhanced, respectively) show Candida spondylitis
infection in 59-year-old man with disk destruction (arrowhead). Intervertebral disk was destroyed in 50% of
Candida spondylitis patients compared with 93% of bacterial spondylitis patients and 28% of tuberculous
spondylitis patients.

AJR:201, October 2013 875


Lee et al.
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C
Fig. 2—Candida spondylitis.
A–C, MR images (T2-weighted, T1-weighted, and contrast-enhanced, respectively) of Candida spondylitis in 68-year-old man (A), bacterial spondylitis in 15-year-old boy (B),
and tuberculous spondylitis in 41-year-old man (C). Axial images of Candida spondylitis show inflammatory mass in paraspinal soft tissue of mixed low signal intensity (thick
white arrow, A) interspersed with punctate nonenhancing component (thin white arrow, A) compared with bacterial paraspinal inflammatory mass that is high signal intensity
on T2-weighted image and diffusely enhanced (arrowhead, B) or thin rim-enhancing soft tissue abscess cavity of tuberculous spondylitis (curved arrow, C).

876 AJR:201, October 2013


MRI of Candida Spondylitis
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D
Fig. 3—Paraspinal abscess and mass.
A, MR images (T2-weighted, T1-weighted, and contrast-enhanced, respectively) of 68-year-old man with Candida spondylitis show multiple small paraspinal abscesses
(thin arrow) and diffusely enhancing left paraspinal inflammatory mass that is low signal intensity on T2-weighted image (thick arrow).
B, MR images (T2-weighted, T1-weighted, and contrast-enhanced, respectively) of 15-year-old boy with bacterial spondylitis show paraspinal inflammatory mass that is
high signal intensity on T2-weighted image (double arrows).
C and D, MR images (T2-weighted, T1-weighted, and contrast-enhanced, respectively) of 68-year-old man (C) and 27-year-old man (D) with tuberculous spondylitis show
multiple small abscesses (black arrowhead) with T2-hypointense inflammatory mass (white arrowhead, C) and large confluent paraspinal abscess (curved arrow, D).

AJR:201, October 2013 877

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