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MRI findings and classification of brucella spondylitis: a China multicenter study

Abstract

Objectives

To propose a magnetic resonance imaging (MRI) classification of brucellosis spondylitis (BS) to determine a standard treatment method and a standard of post-treatment MRI follow-up.

Methods

This is a multicenter retrospective cohort study. All patients diagnosed with BS at six hospitals for 12 years, were included in the study. Data were collected retrospectively from the medical records of the patients. The classification of the cases was based on MRI. We analyzed MRI features of BS was categorized them into three types.

Results

Six hundred fifteen patients were included in the study, 78.9% of whom were males. The mean age was 53.05 ± 11.06 years. Involvement of single vertebrae occurred in 6.2% of patients, while 72.7% involved two vertebrae and 21.1% involvement of more than two vertebrae. The most common of the lumbar spine was 64.6%. The main findings of MRI were affected vertebral endplate 2/3 above (60.7%), intervertebral space narrow (77.9%), intervertebral disc involvement (83.6%), paravertebral abscess (50.9%), disc abscess (49.6%), epidural abscess (43.3%), vertebra height change (22.1%), psoas abscess (22.0%), and abnormal vertebral accessory (10.2%). MR imaging of BS was categorized into three types. Type I: 57 (9.3%) patients; Type II: 526 (85.5%) patients, including IIa (26.5%), IIb (36.9%), and IIc (22.1%); Type IV: vertebral appendage type, 63 (10.2%) cases; Type III: 32 (5.2%) patients.

Conclusions

MRI features of multicenter data can provide theoretical support for diagnosing BS. MRI classification of BS can afford better help for clinical treatment and follow-up after clinical treatment.

Key Points

  • This is a China multicenter study on MRI features and classification in brucella spondylitis.

  • Multicenter MRI feature data can provide a reliable theoretical support for the classification of brucella spondylitis. MRI classification of brucella spondylitis can afford better help for clinical treatment and follow-up after clinical treatment.

Introduction

Brucellosis is a global zoonotic disease caused by intracellular Brucella species. It is a growing public health concern in high-risk countries and a neglected illness worldwide [1]. Brucellosis can occur in any organ, and the most common site is the skeletal system, with 10% to 85% of patients affected. Spinal involvement is the most common, with an infection rate of 54% [2]. Because brucella spondylitis (BS) is clinically nonspecific, it may be misdiagnosed and mistreated. Although low mortality rate, BS can be severely debilitating and disabling [3, 4]. It is critical to diagnose accurately and treat timely BS. There is no widely accepted radiological classification system based on objective results to guide in selecting a treatment method for BS. Therefore, it is urgent to improve clinicians' understanding of the imaging features of BS, and it is essential to screen firstly, relying on the imaging characteristics to determine whether it is BS. Between 2000 and 2019, research into the imaging characteristics of BS was done in Iran, Greece, Turkey, and Saudi Arabia [1]. However, these findings are different, due to the small sample size or other classification methods. There was a multicenter study to provide reliable imaging features and classification of BS, and its sample size was more extensive than previous studies [5,6,7]. Moreover, the extensive data on human BS should improve the identification of relevant prognostic factors and promote this debilitating condition’s clinical management. At present, there is no standardized magnetic resonance imaging (MRI) classification for BS. This paper proposes an MRI classification method for standardized treatment of the disease. This study aims to describe the MRI findings of 615 hospitalized patients with confirmed BS, and explore MRI features and classification in BS.

Materials and methods

This is a retrospective multicenter observational study from six medicine centers or departments that perform spinal MR examinations in China. BS patients from six hospitals were recruited as study cases with ethical approval for retrospective review of MR images by the local ethics committees, without the need for specific patient consent.

The radiologic database of each institution was searched for consecutive MRI studies performed during the ten years between January 1, 2010 and December 31, 2021 by looking for cases that fulfilled the following criteria [8, 9]: Diagnosis of BS was based on the Brucella agglutination titer test (≥ 1:160) and isolation of Brucella species from blood, bone marrow, or tissues and infection in the vertebra or intervertebral disc on MRI. The inclusion criteria include the following aspects. (I) Diagnosis confirmed by biopsy or culture from sample taken during surgery. (II) The patients who had undergone an MRI. III. All patients were supposed to be adults (Age > 18 year). The exclusion criteria were as follows: (I) The patients who had congenital spinal dysplasia. (II) Patients with spinal dysplasia or suspected cancer. (III) The patients received any surgery or medication before the study.

Analysis of imaging

The following was recorded on BS patients: patients’ age, sex, nationality, and MRI findings. MRI findings including the location of involvement in the spine (cervical, cervicothoracic, thoracic, thoracolumbar, lumbar, lumbosacral, or sacral), multiple noncontiguous levels, vertebral height (normal or compression), vertebral number (one, two, or > 2), location of vertebral destruction (posterior 1/3 of vertebral endplate, middle 1/3 of vertebral endplate, anterior 1/3 of vertebral endplate, more than 2/3 of vertebral endplate), the height of intervertebral space (normal, narrow ≤ 1/2, or narrow > 1/2), intervertebral disc destruction (normal, destruction grading ≤ 1/2, or destruction grading > 1/2), abnormal vertebral accessory structure (pedicle, spinous process, or transverse process), abscess (intervertebral disc abscess, epidural abscess, psoas abscess) [10].

BS was matched according to MRI finding classification [11]: Type I (Early stage): vertebral inflammatory edema type, BS showed only vertebral marrow edema without/with paravertebral edema, a hypointense signal on T1WI, and hyperintense signal on T2WI (Fig. 1a). Type II (Progressive stage): vertebral bone destruction and bone repair coexist, and the degree of bone destruction is greater than that of bone repair. This type has three sub-types: IIa, IIb, and IIc. Type IIa: MRI revealed 1/3 of the vertebra endplate destruction, vertebral height normal, without abscess (Fig. 1b); Type IIb: MRI showed more than 2/3 of the vertebral endplate destruction, vertebral height normal (Fig. 1c); Type IIc: MRI presented destruction of vertebral endplate 2/3 above, vertebral compression (Fig. 1d). Type III (Repair stage): bone destruction and bone repair coexist, and the degree of bone repair is greater than that of bone destruction (Fig. 1e). The vertebral lesion showed a homogeneous/heterogeneous hypointense signal on T1WI and homogeneous/heterogeneous hypointense signal on T2WI. The edge of the lesion is sclerosed.

Fig. 1
figure 1

This is the schematic diagram of BS imaging classification. The area marked red represents bone marrow edema and abscess formation. The blue area is bone destruction, and the black area is bone hyperplasia and sclerosis

MRI data were collected by six radiologists (from 6 hospitals) who each had more than eight years of experience. Before these data were collected, six doctors were trained online. Training results were tested using 10 patients, and the Kappa consistency was 8.991.

Statistical analysis

Statistical analysis was performed with SPSS17.00 statistical software. Continuous variables were shown as mean ± standard deviation, and categorical variables were presented as percentages.

Results

Demographic characteristics

Demographic characteristics of patients with BS are shown in Table 1. This study evaluated 615 patients with BS. The study population consisted of 485 men and 130 women, and the ratio was 3.7 to 1. The mean age was 53.05 ± 11.06 (range 19–82) years. The incidence of ethnic groups is 44.9% Han, 34% Uygur, 10.2% Kazak, 8.3% Hui, 1.6% Mongol, and 0.1% other nationalities.

Table 1 Demographic characteristics of brucella spondylitis patients

MRI findings

MRI characteristics of BS patients are shown in Table 2. Of the 615 patients with BS, thirty-eight patients had a single vertebrae, 447 (72.7%) had involvement of two vertebrae whereas 130 (21.1%) had more than two regions. The lumbar spine is the commonest affected region (397 patients, 64.4%), while the lumbosacral spine was affected in 118 (18.5%) patients, thoracic spine affected in 35 (5.7%) patients, cervical spine in 16 (2.6%) patients, while thoracolumbar spine was affected in 8 (1.3%) patients, sacral spine was affected in 3 (0.5%) patients and cervicothoracic spine was affected in 2 (0.3%) patients.

Table 2 MRI characteristics of brucella spondylitis patients

Of the 615 patients with BS, vertebra height was collapsed in 136 (22.1%) patients, while the remaining vertebra height was normal. The most common was involvement of more than 2/3 of the endplate, accounting for 373 (60.7%) patients, followed by 118 (19.2%) posterior of endplate 1/3, 98 (15.9%) anterior of endplate 1/3, 26 (4.2%) middle of endplate 1/3. The vertebral appendices of 63(10.2%) patients were infected by Brucella.

Of the 615 patients with BS, no more than 1/2 of the intervertebral space height was altered in 323 (52.5%) patients, and 156 (25.4%) patients with intervertebral space were changed more than 1/2, while 136 (22.1%) patients with intervertebral space were normal.

Of the 615 patients with BS, intervertebral disc involvement was observed in 453 patients. Of the patients with intervertebral disc involvement, 297 (48.3%) cases had the destruction grading (≤ 1/2) of the intervertebral disc, and 156 (25.4%) patients with the destruction grading (> 1/2) of the intervertebral disc.

Of the 615 patients with BS, the most common abscess formation was the paravertebral abscess (313, 50.9%) patients, followed by 305 (49.6%) disc abscess, 266 (43.3%) epidural abscess, 135 (22.0%) psoas abscess. In paravertebral abscess, epidural abscess, and psoas abscess, the abscess beyond the adjacent vertebral bodies had 77 (12.5%) patients, while the abscess in the adjacent vertebral bodies had 88.5% of patients.

MRI classification

Type I. It has 57 (9.3%) patients. 38 (6.2%) involved a single vertebrae, and 19 (3.1%) involved two vertebrae (Fig. 1a, Fig. 2a). A total of 76 vertebrae presented marrow edema. There were 33 (5.4%) patients for anterior 1/3 of the vertebral endplate destruction and 24 (3.9%) for posterior 1/3 of the vertebral endplate destruction. Type II. It has 526 (85.5%) patients, including IIa (163), IIb (237), and IIc (136). Type IIa has 163 (26.5%) patients with vertebral height normal and without abscess (Fig. 1b, Fig. 2b), including 84 (13.7%) the posterior vertebral endplate destruction, 55 (8.9%) the anterior vertebral endplate destruction, 24 (3.9%) the middle vertebral endplate destruction, 57 (9.3%) intervertebral space normal, 84 (13.7%) intervertebral space narrow, 22 (3.6%) without intervertebral disc destruction, 141 (22.9%) with intervertebral disc destruction, a hypointense signal on T1WI and hyperintense signal on T2WI. Type IIb has 227 (36.9%) patients with vertebral height normal, more than 2/3 of the vertebral endplate destruction, abscess, intervertebral space narrow, intervertebral disc destruction (Fig. 1c, Fig. 2c), homogeneous/heterogeneous hypointense signal on T1WI, and homogeneous/heterogeneous hyperintense signal on T2WI. The abscess occurred in 180 (29.3%) intervertebral disc abscesses, 147 (23.9%) epidural abscesses, 59 (9.6%) psoas muscle abscesses, 27 (4.48%) paravertebral abscesses. Type IIc has 136 (22.1%) patients with vertebral wedge-shaped, more than 2/3 of the vertebral endplate destruction, intervertebral space narrow, intervertebral disc destruction (Figs. 1d, 2d), homogeneous/heterogeneous hypointense signals on T1WI, and heterogeneous signals on T2WI. Among them, there were 125 intervertebral disc abscesses (20.38%), 119 epidural abscesses (19.3%), 109 paravertebral abscesses (17.7%), and 76 psoas muscle abscesses (12.4%). Type III. There were 32 patients (5.2%). Seventeen (2.8%) patients with BS showed a hypointense signal on T1WI and T2WI. 15 (2.4%) patients with BS showed a hypointense signal on T1WI and a heterogeneous hypointense signal on T2WI (Figs. 1e, 2e).

Fig. 2
figure 2

This is MRI of BS image classification

Discussion

This study retrospectively collected multicenter data from MRI features of 615 patients with BS in China. The results provided a theoretical basis for diagnosis in MRI and classification of BS. To our knowledge, this study had the most data on MRI features compared with previous studies, and the MRI classification of BS was few reported.

The patients’ mean age was 53 years (range 19–82 years), consistent with previous studies [8, 12,13,14,15,16,17]. Male patients predominated (64–74%) [14, 15]. In our study, the male patients’ ratio was higher (78.9%), similar to studies by Çıraklı et al. [18]. This may be the nature of the male job in such regions, facilitating increased exposure to animals and their products, as observed in herders, ranchers, pastoralists, and abattoir workers [17]. In the current study, the most common nationality is Han (44.9%), followed by Uygur (34.0%), Kazak (10.2%), Hui (8.3%), Mongol (1.6%), and Other (0.1%).

MRI has a high diagnostic sensitivity, specificity, and accuracy of > 90% in spinal infection [19,20,21,22,23]. MRI is the diagnostic imaging modality of BS [12, 24], the most valuable method to diagnose BS [25, 26]. It is stated that most sites involved in the lumbar, followed by the thoracic, and cervical segments, are reported to be more involved in BS [18, 27,28,29,30,31,32,33,34,35,36,37,38,39,40,41]. In the current study, the sites of involvement were lumbar (64.6%), lumbosacral (18.5%), thoracic (5.7%), cervical (2.6%), thoracolumbar (1.3%), sacral (0.5%) and cervicothoracic (0.3%). Compared with previous studies, the incidence of involvement in the lumbar is similar to previous studies [14, 18, 27,28,29,30,31,32,33,34,35,36,37,38,39,40,41], and the rate of the lumbosacral region is higher than that of previous studies [14, 38, 41], whereas the rate of the thoracic [14, 18, 27,28,29,30,31,32,33,34,35,36,37,38, 40], cervical [14, 28,29,30,31,32,33,34,35,36,37,38,39,40,41], thoracolumbar [14, 38, 39, 41] and cervicothoracic [39] region is lower than that of previous studies. This difference may be related to multicenter, extensive data studies.

BS can be seen as single-focal and contiguous or non-contiguous multi-focal involvements. It was reported that involvement of a single spinal region has predominated (91–95.5%) [24, 39], and multiple regions have different results in different literatures (3–36%) [24, 30, 31, 35, 38, 39, 41,42,43,44,45,46,47,48,49,50]. In this study, the most common were lesions involving two vertebral bodies (72.7%), followed by lesions involving more than two vertebral bodies (21.1%), and lesions involving one vertebral body (6.2%). 40 (6.5%) had noncontiguous multifocal spinal involvement in our study, a figure lower than those reported in the literature [39, 46, 51].

Due to the rich blood supply of the superior endplate, the superior endplate is the usual starting point in most spinal brucellosis, although the inferior endplate may also be involved [41]. In MRI, the lesion is destructive in an anterosuperior corner of the vertebrae, accompanied by prominent osteosclerosis [52, 53]. When the balance between the organism’s virulence and host defense mechanism is destroyed, disease progression can involve the entire vertebral body [41]. Therefore, the vertebrae of BS is abnormally altered with focal or diffuse bone destruction. In focal involvement, the lesion is localized in the anterior endplate 1/3, middle of endplate 1/3, and posterior endplate 1/3 at the vertebral junction. Still, in the diffuse type, the lesion affects the vertebral endplate 2/3 above or the whole vertebral body [31, 54]. In this study, the location of vertebral destruction was vertebral endplate 2/3 above (60.7%), posterior of endplate 1/3 (19.2%), anterior of endplate 1/3 (15.9%), middle of endplate (4.2%). 10.9 percent of patients with vertebral appendages were abnormal.

The superior endplate is the first part of the vertebrae involved because of its rich blood supply wich causes bone destruction in the early stages. The inflammation can spread to the entire vertebrae and may involve the adjacent disc space [41]. Vertebral collapse may lead to vertebral compression fracture resulting in vertebral flattening. In the current study, vertebra height was altered in 22.1% of patients, while the remaining patients’ vertebra height was normal.

Of the 615 patients with BS, intervertebral disc involvement was observed in 73.7% patients. Of the patients with intervertebral disc involvement, 48.3% had the destruction grading (≤ 1/2) of the intervertebral disc, and 25.4% of patients with the destruction grading (> 1/2) of the intervertebral disc. Intervertebral disc damage may cause the intervertebral space narrow. In our study, no more than 1/2 of the intervertebral space height was altered in 52.5% of patients, and 25.4 percent of patients with intervertebral space was changed more than 1/2, while 22.1% of patients with intervertebral space was normal. Disease progression is inevitable when the balance between the organism’s virulence and host defense mechanism is destroyed. Finally, the process can involve the entire vertebral body, invade the neighboring intervertebral disc space, and invade adjacent vertebrae [41].

BS may also occur in psoas abscess, paraspinal abscess, and/or epidural abscess [2, 30, 55]. According to the report, the incidence of abscess formation findings was 29–65.6% [17, 34, 36]. Paravertebral abscesses have been reported to occur at a frequency of 13.6–30% in three studies [24, 32, 50]. Both paravertebral [14, 15, 17, 38, 39] and epidural [14, 38, 39] abscess formations were reported. In the current study, the incidence of findings of abscess formation was paravertebral abscesses (63.4%), disc abscesses (49.6%), epidural abscesses (43.3%), and psoas abscesses (22.0%). All abscesses may occur in a single form or multiple combinations. According to the imaging findings, paravertebral abscesses were divided beyond the adjacent vertebral bodies (12.5%) and the adjacent vertebral bodies (50.9%). If abscesses are found, a longer course of treatment and even surgical intervention may be needed.

MRI classification

In previous studies, BS was classified into the following five types according to imaging characteristics: vertebral osteomyelitis, discitis, paravertebral abscess or epidural abscess, and mixed type [5, 6]. Such a comprehensive imaging classification is not conducive to treating BS and post-treatment imaging follow-up. As MRI has a high diagnostic sensitivity, specificity, and accuracy in BS, the MRI classification of BS may be more conducive to the diagnosis, treatment, and prognosis follow-up of BS. In the current study, MRI findings were classified into the following three types according to the progression of spinal lesions. Type I (Early stage): vertebral inflammatory edema type, these patients can pass non-hand Surgical treatment and cure [7]. Type II (Progressive stage): vertebral bone destruction and bone repair coexist, and the degree of bone destruction is greater than that of bone repair. This type has three sub-types: IIa, IIb, and IIc. In Type IIa, the vast majority of patients can pass non-hand Surgical treatment and cure. When does not respond to medication, surgical treatment can be considered patients [6, 7]. In Type IIb and Type IIc, under the premise of effective drug treatment, minimally invasive or open surgical treatment can be selected according to different image credit types [7]. Type III (Repair stage): bone destruction and bone repair coexist, and the degree of bone repair is greater than that of bone destruction. The lesions of BS tend to heal, and the vast majority of patients do not need treatment. In the current study, the proportion of Type I and Type III was 9.3% and 5.2%, which were relatively small. The possible reason is that BS is a chronic disease with no early clinical symptoms or atypical clinical symptoms, which make it easy to delay diagnosis. Since there are few patients with type I BS when the patients with type I BS are treated with drugs, fewer patients with BS change to the repair stage (type III). We propose a classification system using the MRI information to help plan the appropriate and rational treatment for patients with BS.

This analysis has several limitations. Firstly, this was a retrospective study and therefore was susceptible to uncontrolled confounding. Secondly, the quality of images obtained by different parameters and MRI from other manufacturers in six hospitals was biased. Last but not least, all data was collected by the six investigators, thereby maximizing bias due to differences in data interpretation and admission coding.

In conclusion, we report the most extensive multicenter cohort study of MRI features and classification with BS. MRI features and classification of BS can provide better help for clinical diagnosis and treatment.

Availability of data and materials

Our data and images support the usability of our articles.

Abbreviations

BS:

Brucella spondylitis

MRI:

Magnetic resonance imaging

T1WI:

T1 weighted image

T2WI:

T2 weighted image

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Acknowledgements

The authors gratefully acknowledge the financial support provided by State Key Laboratory of Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asia Fund (Grant No. SKL-HIDCA-2021-22).

Funding

The authors gratefully acknowledge the financial support provided by State Key Laboratory of Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asia Fund (Grant No. SKL-HIDCA-2021-22).

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Study concept and design: Hui Guo, Wenya Liu, and Hongjun Li. Performed research: Li Gou, Hui Guo, and Wenya Liu. Analyzed data: Li Gou, Yuxin Yang, Junlin Li, Lei Cai, and Weihong Xing. Wrote the paper: Li Gou and Hui Guo. Revised the paper: Lingling Zhao and Yibo Lu. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Hui Guo or Hongjun Li.

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Ethical approval for the study was obtained from the ethical review committee for the first affiliated hospital of Xinjiang Medical University.

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Gou, L., Yang, Y., Li, J. et al. MRI findings and classification of brucella spondylitis: a China multicenter study. Eur J Med Res 29, 469 (2024). https://doi.org/10.1186/s40001-024-02011-2

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