Type II Modic Changes May Not Always Represent Fat Degeneration a Study Using MR Fat Suppression Sequence

DIAGNOSTICS

Type II Modic Changes May not Always Represent Fat Degeneration A Study Using MR Fat Suppression Sequence

Zhiyun Feng, MD, Yuanhao Liu, MD, Wei Wei,y Shengping Hu, MD,y and Yue Wang, PhD

(24.7%) type II MCs was suppressed on FS images, that of 113 Study Design. A radiological study of type II Modic changes (75.3%) was not suppressed. The discs adjacent to type II MCs (MCs). had lower signal intensity (0.13 0.003 vs.0.14 0.004, Objectives. The aim of this study was to determine the P < 0.001), lesser disc height (9.73 1.97 vs.11.07 1.99, characteristics of type II MCs on fat suppression (FS) magnetic P < 0.001) and greater bulging area (80.0 31.4 vs. 61.3 27.5 resonance (MR) images and its association with radiological disc for anterior bulging, 33.72 21.24 vs. 27.93 12.79 for degeneration. Summary of Background Data. Type II MCs are common posterior bulging, and 113.7 39.9 vs. 89.2 35.2 for total < endplate signal changes on MR images. On the basis of limited bulging, P 0.05) than normal controls. Type II MCs that were histological samples, type II MCs are thought to be stable fat not suppressed on FS image were associated with greater age < degeneration. FS technique on MR, which can quantify fat [odds ratio (OR) ¼ 1.11, P 0.001], lower height (OR ¼ 0.94, < < content, may be an alternative to explore the pathology of MCs. P 0.05), and greater posterior bulging (OR ¼ 1.05, P 0.001) at To date, however, the characteristics of type II MCs on FS the adjacent disc. Conclusion. Signal of most type II MCs was not suppressed on sequence have not been studied. Methods. Lumbar MR images conducted in a single hospital FS MR images, suggesting that there are ongoing complicated during a defined period were reviewed to include those with pathologies. Type II MCs may not merely represent fat replace- type II MCs and FS images. On FS images, signal status of type ment. Key words: disc degeneration, fat suppression, lumbar spine, II MCs was visually classified as suppressed or not-suppressed. magnetic resonance imaging, Modic changes, quantitative image Signal intensity of vertebral regions with and without MCs was analysis. measured quantitatively on T2-weighted (T2W) and FS images to Level of Evidence: 3 calculate fat content index and validate the visual classification. Spine 2016;41:E987–E994 Using image analysis program Osirix, MCs size and adjacent disc degeneration were measured quantitatively. Paired t-tests and logistic regressions were used to determine the associations studied. odic changes (MCs), or endplate signal changes, Results. Sixty-four lumbar MRIs were included and 150 end- are common findings on lumbar spine magnetic plates with type II MCs were studied. Although signal of 37 M resonance (MR) images. The prevalence rates of MCs reportedly vary from 19% to 59%, depending on study samples.1 Traditionally, MCs are classified into three types. From the Spine Lab, Department of Orthopedic Surgery, The First Affiliated Type I MCs present decreased signal intensity on T1- Hospital, College of Medicine, Zhejiang University, Hangzhou, China; and yDepartment of Orthopedic Surgery, Integrated Chinese and Western Medi- weighted (T1W) images and increased signal intensity on cine Hospital of Zhejiang Province, Hangzhou, China. T2-weighted (T2W) images. Type II MCs reflect increased Acknowledgment date: September 14, 2015. First revision date: December signal intensity on both T1W and T2W images and type III 12, 2015. Acceptance date: January 22, 2016. MCs display decreased signal intensity on both T1W and The manuscript submitted does not contain information about medical T2W images.2 While type II MCs are the most common device(s)/drug(s). endplate signal changes, type III MCs are rare. National Natural Science Foundation of China (NSFC, No. 81371995) and AO Spine 2015 China Research Grant [AOSCN (R) 2015-03] funds were Although MCs were intensively studied for decades, received in support of this work. much remained unclear. The association between MCs No relevant financial activities outside the submitted work. and back pain, for example, remains controversial. Address correspondence and reprint requests to Dr. Yue Wang, PhD, Although many researchers reported that both type I and Building 3-2, 79#, Qingchun Road, Hangzhou 310003, China. II MCs were associated with back pain,3,4 some specified E-mail: [email protected] that it was type I MCs, but not type II MCs, that was 5 DOI: 10.1097/BRS.0000000000001526 associated with back pain. The association between MCs Spine www.spinejournal.com E987 Copyright © 2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. DIAGNOSTICS Type II Modic Changes Feng et al and back pain, however, was not observed in some clinical MATERIALS AND METHODS studies.6–8 On the contrary, although it is generally accepted that MCs are associated with disc degeneration, quantitative Samples data supporting this relationship are insufficient. Image samples of this study were collected at the Integrated A limited understanding of clinical relevance of MCs is Chinese and Western Medicine Hospital of Zhejiang Prov- due, at least in part, to the poor knowledge of MCs path- ince, China. Lumbar spine imaging conducted here routinely ology. According to an early report, type I MCs were includes T1W, T2W, and FS sequence. All lumbar spine MR characterized by inflammatory reactions and vascular gran- imaging performed from April 1 to September 31 of 2014 ulation formation, and fatty degeneration was a prominent were reviewed by an orthopedic surgeon (ZYF) for the pathological finding for type II MCs.9 Surprisingly, how- presence of any type of MCs. MRIs were excluded if there ever, this widely spread concept was based on merely six were suspected metastatic lesions, ankylosing spondylitis, histological samples.9 The pathological entities of MCs, lumbar spine infections, scoliosis, fresh vertebral fractures, therefore, deserve further investigation. or lumbar instrumentations. If MCs are present, MRIs were Given the scarcity of histological samples nowadays, a downloaded in DICOM format for further evaluation. Two radiological study may be a reasonable alternative to authors (SPH and YHL) further reviewed all selected lumbar further understand the pathology for MCs. Fat suppression spine MRIs together to evaluate specific type of MCs. MCs (FS) techniques are commonly used in the differential were classified as type I (hypo-intensity on T1W images and diagnosis for spine disorders. On FS sequence, signal hyper-intensity on T2W images), type II (hyper-intensity on contribution from fat or fat-related components is sup- both T1W and T2W images), type III (hypo-intensity on pressed and thus displays decreased signal on MR images. both T1W and T2W images), and mixed type of MCs Recently, FS techniques were used to quantify fat content (mixed I/II and mixed II/III).2,13 in liver,10 subcutaneous tissue,11 and bones.12 Although fat As the focus of the current study was type II MCs, only may be an important component of type II MCs, the lumbar MRIs with type II MCs were included for further characteristics of type II MCs on FS sequence have not assessment and type I, type III, and mixed MCs were all been studied yet. excluded. In MCs evaluation, we excluded small signal In clinical practice, we have noticed an interesting changes on vertebral body corners and those endplate signal phenomenon that type II MCs had different presentations changes that presented on less than three sagittal slices to on FS images. Although signal of some type II MCs was minimize measurement errors.14 As only patients’ images suppressed on FS images, as compared with that of adjacent were reviewed in the present study, ethic permission was vertebral marrow without MCs (Figure 1 A-C), in many waived by the authors’ institutional review boards. cases, signal on FS images was not suppressed (Figure 1 D-F). We postulated that the divergent presentations of type II MR Imaging Technique MCs on FS images may be due to varied pathologies under- MR imaging was performed using a 3.0 Tesla scanner lying, which may have different pathological effects on the (Philips Medical Systems; Best, The Netherlands). Sagittal adjacent intervertebral disc. The purposes of the current T2W images were acquired using a fast spin-echo sequence study, therefore, are to characterize type II MCs on FS with a repetition time (TR) of 4000 ms, echo time (TE) of sequence and further to determine the association between 118 ms, echo train length of 27, and the number of acqui- FS status of type II MCs and adjacent disc degeneration. sitions of 4. The matrix size was 448 224, field of view

Figure 1. Different presentations of type II MCs on fat suppression (FS) sequence. Type II MCs in a 33-year-old woman (A,B). Signal of the type II MCs region was suppressed on FS image, as compared with adjacent normal vertebral region without MCs (C). Type II MCs in a 54-year-old woman (D,E). On FS image, signal of region with type II MCs was not suppressed, as refer to the adjacent vertebral region without MCs (F). FS indicates fat suppression; T1W, T1-weighted; T2W, T2-weighted.

28 28 cm, slice thickness 4 mm, and intersection gap Due to the heterogeneity of signal on MR imaging, it may 1 mm. Sagittal T1W images were acquired using a fluid- not be suitable to directly compare signal intensity measure- attenuated inversion recovery sequence with a TR of ments of different regions or sequences. We used the mean 2060 ms, TE of 21 ms, inversion time (TI) of 860 ms, echo signal intensity of adjacent cerebrospinal fluid (CSF) as a train length of 6, and the number of acquisitions of 4. The reference to adjust all signal intensity measurements for the matrix size was 256 224, FOV 28 28 cm, slice thickness vertebral regions and intervertebral disc.15 A representative 4 mm, and intersection gap 1 mm. FS images were acquired area of CSF that was closely adjacent to the MCs regions, using spectral pre-saturation attenuated inversion recovery either on the same sagittal slice or the adjacent sagittal slice, (SPAIR) sequence with T2 suppression. This technique is was sampled to measure mean signal intensity for CSF. based on a frequency-selective inversion pre-pulse tuned to Signal intensity measurements, therefore, are the ratio of fat off-resonance and with an inversion time adjusted to mean signal intensity of targeted regions relative to the mean 100 ms for optimal fat nulling. signal intensity of the adjacent CSF. In addition, ROIs defined on T2W images were copied to Suppression Status of Type II MCs on FS Images the corresponding FS images to obtain another set of signal When the presence of type II MCs was confirmed, the intensity measurements (Figure 2). Fat content index (FCI), involved spinal level, location, and suppression status on which is the percentage signal intensity change between FS sequence were recorded. On T2W sagittal image, a T2W and FS images, was calculated to estimate fat content lumbar vertebral body with type II MCs was classified into for MCs region and non-MCs region.16 MCs region and adjacent non-MCs region for further assess- ðÞSIMCs=SICSF ðÞSIMCs=SICSF ment. The signal intensity of MCs regions on FS images was FCI ¼ T2 FS ðÞSI =SI first assessed visually, taking the adjacent non-MCs region MCs CSF T2 as a reference. On FS images, Type II MCs were defined as suppressed if the MCs regions present hypo-intensity as FCI, fat content index; SI, signal intensity; SIMCs, signal relative to the adjacent non-MCs region in the same vertebra intensity for MCs region; SICSF, signal intensity of adjacent (Figure 1A–C), and not-suppressed if present iso-intensity CSF; T2, T2-weighted image; FS, FS image. or hyper-intensity as compared with the adjacent non-MCs regions (Figure 1D–F). MCs Size Assessment Using a method we previously validated,14 the size of MCs, Quantitative Measures of Signal Intensity including area, anteroposterior (AP) diameter, transverse The T2W sagittal image with the largest MCs region was diameter, and height were measured on T2W image. Area used to measure signal intensity. Using an image analysis was obtained by defining an ROI for MCs. The AP diameter program Osirix (version 3.1; Geneva, Switzerland), the MCs was measured as the ratio of AP MCs diameter to AP region was defined as a region of interest (ROI) using a vertebral body diameter on middle sagittal image, as shown closed polygon. As shown in Figure 2, area and signal in Figure 2. Transverse diameter of MCs was defined as the intensity measurements of ROI were acquired. percentage of slices with the presence of MCs (11 slices for

Figure 2. Quantitative measurements for MCs and cerebrospinal fluid (CSF). Using Osirix program, regions of interests (ROIs) were defined to acquire quantitative signal intensity measurements for MCs region and adjacent CSF (A). Fur- ther, the ROIs were copied to corresponding fat suppression images to acquire similar quantitative measurements (B). MCs size, including area, anteroposterior (AP) diameter, and height, was measured on T2W images. The AP diameter was measured as the ratio of AP MC diameter (the distance from point ‘‘a’’ to point ‘‘c’’ of the involved endplate) to the AP vertebral endplate diameter on the middle sagittal image (the distance from the anterior most point ‘‘a’’ to posterior most point ‘‘d’’ of the vertebral endplate). Point ‘‘b’’ and ‘‘f’’ divided the lower and upper endplate of vertebrae into two portions, respectively. The height of MCs region was measured as the ratio of MCs height [the vertical distance from the highest point (e) of MCs region to the involved vertebral endplate] to the vertebral height measured in the middle of the vertebral body (line bf). Spine www.spinejournal.com E989 Copyright © 2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. DIAGNOSTICS Type II Modic Changes Feng et al

MCs present at the endplates adjacent to L4/5 disc, then the L5/S1 disc without adjacent MCs was measured for control (Figure 3). As MCs classification was generally reliable,13,17 we did not evaluate reliability of MCs evaluation but had two authors evaluate specific MCs types together. Twenty lumbar MRIs randomly selected from the database were repeat- edly measured by two authors to estimate inter- and intrareliabilities of specific measurements of MCs and disc degeneration.

Statistical Analysis Statistical analyses were performed using STATA (version 12.0; Stata Corp LP, TX). Kappa statistics and intraclass correlation coefficient (ICC) were used to evaluate the reliability of MR measurements. Descriptive statistics were used to depict the characteristics of subjects, the number and location of MCs, disc degeneration, and percentage of fat- suppressed type II MCs. Continuous variables were presented as mean standard deviation (SD). Paired t-tests Figure 3. Quantitative measurements of disc degeneration. The were used to study the relationship between type II MCs anterior most point ‘‘a,’’ posterior most point ‘‘p,’’ and middle point and disc degeneration. Logistic regression was used to ‘‘m’’ were defined for each vertebral endplate. Disc height was cal- determine the associations between FS status and disc culated as the average of aa/,mm/, and pp/. Closed polygon tool in degeneration, adjusting for age. Osirix program was used to define regions of interests for the disc to obtain area and signal intensity measurements. Disc bulging was the RESULTS area exceeding anteriorly and posteriorly to the vertebral edge, and There were 576 lumbar spine MRIs conducted at the hos- total disc bulging was also calculated as anterior bulging plus posterior bulging. As defined previously, endplates showing hyper- pital during the defined period. Among them, 64 lumbar intensity on both T1W and T2W images was classified as type II spine MRIs that meet the inclusion criteria were included in MCs. In this case, type II MCs are present at both endplates adjacent the current study. There were 17 men and 47 women (mean to L4/5 disc, and the endplates adjacent to L5/S1 disc are without age 58.5 yrs, range 32–82 yrs). Type II MCs were presented MCs. Therefore, both L4/5 and L5/S1 discs were measured and at 150 lumbar vertebral endplates. L5/S1 disc serves as a control in statistical comparison. Reliability of Measurements Kappa statistics revealed good to excellent intrarater and each lumbar spine MR imaging). The height of MCs region inter-rater reliabilities for MCs and disc degeneration was measured as the ratio of MCs height to the vertebral measurements (Table 1). body height (Figure 2). Suppression Status of Type II MCs on FS Images Evaluation of Disc Degeneration Type II MCs were more common in the lower lumbar region The degree of disc degeneration was assessed using disc than in the upper lumbar region. According to our visual signal intensity, disc height, and disc bulging, which were classification, only 37 (24.7%) endplates with type II MCs acquired on mid-sagittal T2W image. The mean disc signal were rated as suppressed, and the other 113 (75.3%) were intensity was acquired by defining a ROI for the interverte- rated as not-suppressed on FS images. The distribution of bral disc, which was further adjusted for adjacent CSF signal type II MCs was presented in Figure 4. intensity (Figure 3). Disc height was defined as the mean of anterior, middle, and posterior height of the intervertebral Fat Suppression Status in Relation to FCI and MCs disc. Disc bulging, which includes anterior and posterior Size disc bulging, was measured as the area of the portion of the Regardless of FS status on FS images, FCIs were statisti- disc that exceeds the anterior and posterior edges of cally significantly different at MCs region and adjacent vertebral bodies (Figure 3). non-MCs region (Table 2). When the difference of FCIs As the lumbar spine was typically divided into upper (L1- between MCs region and adjacent non-MCs region was L3) and lower regions (L4-S1), a neighboring disc from the calculated, the difference of FCI in not-suppressed group same region was selectively measured as a control. If MCs (9.6 10.8%) was significantly lower than that in sup- present at the endplates adjacent to L1/2 disc, for example, pressed group (28.9 15.2%) (P < 0.001, Table 2), L2/3 or L3/4 disc that is without MCs at the adjacent suggesting that the visual classification for FS status endplates was measured as a control, or vice versa.If was reasonable.

TABLE 1. Reliability of MCs and Disc Degeneration Measurements (ICC and 95% Confidence Interval, N ¼ 20) Variable Intra-rater ICC Inter-rater ICC MCs signal intensity 0.95 (0.91–0.99) 0.96 (0.91–1.00) Non-MCs vertebral signal intensity 0.95 (0.90–0.99) 0.97 (0.93–1.00) MCs area 0.92 (0.86–0.99) 0.89 (0.79–1.00) MCs height 0.90 (0.81–0.98) 0.80 (0.61–0.99) Transverse diameter of MCs 0.83 (0.69–0.97) 0.70 (0.55–0.85) Anteroposterior diameter of MCs 0.77 (0.63–0.86) 0.74 (0.60–0.83) Disc signal intensity 0.95 (0.91–0.99) 0.94 (0.87–1.00) Disc height 0.92 (0.85–0.99) 0.79 (0.59–0.99) Disc bulging 0.95 (0.90–0.99) 0.96 (0.92–1.00) Weighted kappa for this ordinal variable.

from the same lumbar region as a control. The disc adjacent to type II MCs had lower signal intensity (P < 0.001), lesser disc height (P < 0.001), and greater bulging area (P < 0.05), than the matched control disc (Table 4).

Association Between Fat Suppression Status and Disc Degeneration Using multiple variable logistic regression, the associations between FS status and disc bulging, disc height, and disc signal intensity were analyzed, taking ‘‘suppressed’’ as the reference. Older patients tended to have type II MCs that were not suppressed on FS images (OR ¼ 1.11 for 1 year, P < 0.001, Table 5). Moreover, type II MCs that were not suppressed on FS images statistically had greater adjacent posterior disc bulging (OR ¼ 1.05, P < 0.001) and lower disc height (OR ¼ 0.94, P ¼ 0.038). Disc signal intensity Figure 4. Suppression status of type II Modic changes (MCs) on fat was not statistically significantly associated with FS status suppression images in each lumbar disc level. The percentages are of type II MCs (Table 5). relative to the total number of endplates with type II MCs investi- gated (N ¼ 150). Data from cranial and caudal endplates of a disc were presented together. DISCUSSION Type II MCs have long been thought to be fat degeneration Type II MCs that were suppressed on FS images tended to and thus were regarded as relatively ‘‘quiescent’’ or have greater AP diameter (P < 0.05) and height (P < 0.05), ‘‘stable.’’ Using visual and quantitative measures, this radio- than those of not-suppressed (Table 3). logical study revealed that signal of most type II MCs was not suppressed on FS sequence and older adults were more Association Between Type II MCs and Adjacent likely to have type II MCs that are not suppressed on FS Disc Degeneration sequence. Findings suggested that there may be ongoing Paired t-test was used to examine the effects of type II MCs inflammatory reactions and edema and type II MCs may not on adjacent disc degeneration, taking a neighboring disc always represent fat replacement, questioning the current

TABLE 2. Fat Content Index (FCI) for the Vertebral Regions With or Without MCs Suppressed (N ¼ 37) Not-suppressed (N ¼ 113) MCs region 63.1 12.1% 68.4 9.9% Non-MCs region 34.3 22.5% 58.8 13.1% FCI difference 28.9 15.2% 9.6 10.8% A vertebra was divided into MCs region and non-MCs region. FCI difference was calculated as FCI of MCs region minus FCI of non-MCs region. P < 0.05. P < 0.001.

TABLE 3. MCs Size in Relation to Suppression Status on Fat Suppression Images Size of MCs Suppressed (N ¼ 37) Not-suppressed (N ¼ 113) Area 111.8 55.3 92.2 55.8 Transverse diameter 55.5 24.5% 50.6 23.6% Anteroposterior diameter 72.4 19.7% 60.0 21.8% Height 41.0 11.5% 35.6 10.7% Area: the largest MCs region on T2W sagittal image was measured. Transverse diameter was defined as the percentage of slices with the presence of MCs (11 slices for each lumbar spine MR imaging). Anteroposterior diameter was calculated as the ratio of the largest anteroposterior diameter of MCs to the anteroposterior diameter of the vertebral body on the middle sagittal image. Squared millimeter (mm2) for area measurement, percentage rate for transverse, and anteroposterior diameter and height measurements. P < 0.05.

TABLE 4. The Association Between type II MCs and Adjacent Disc Degeneration: Results From Paired t-tests N ¼ 69 Control Disc Disc Adjacent to MCs Disc signal intensity 0.14 0.004 0.13 0.003 Disc height 11.07 1.99 9.73 1.97 Anterior bulging 61.3 27.5 80.0 31.4 Posterior bulging 27.9 12.8 33.7 21.2 Total bulging 89.2 35.2 113.7 39.9 The lumbar spine was divided into upper (L1-L3) and lower region (L4-S1). Paired t-tests were used and a neighbor disc from the same lumbar region was used as the control. Disc signal intensity was adjusted by that of adjacent cerebrospinal fluid. Millimeter (mm) for disc height measurement, Squared mm for bulging measurements. P < 0.05. P < 0.001.

understanding of pathology for type II MCs. Using quan- approaches to study the pathogenesis of MCs. By comparing titative measures and paired controls, the present study MR and CT images, for example, Kuisma et al.4 suggested confirmed that type II MCs were associated with adjacent that endplate sclerosis presents not only in type III MCs but disc degeneration. In addition, the adjacent disc tended to also in MCs of other types, challenging previous views of have greater degree of degeneration when signal of type II pathological components for MCs. Radiological study with MCs was not suppressed on FS images. quantitative measurements, therefore, may be used as pre- Although the association between MCs and back pain liminary exploration for the pathological entity of type remains controversial,3–8 less attention has been paid to the II MCs. pathological entity of MCs, though it is important to under- For type II MCs, early histological studies reported that stand the association studied. Given the scarcity of histo- the endplate was disrupted and bone marrow under the logical specimen, some researchers tried radiological endplate was full of no-nuclear fat cells.9,18 Thereafter, type

TABLE 5. Association Between Fat Suppression Status of Type II MCs and Adjacent Disc Degeneration: Results From Multiple Variable Logistic Regression (N ¼ 150) Variable OR 95% CI P Age 1.11 1.05–1.17 0.001 Disc height 0.94 0.88–0.99 0.038 Posterior disc bulging 1.05 1.02–1.08 0.001 Disc signal intensity 1.05 0.81–1.14 0.651 Fat suppression status on FS image was the dependent variable and ‘‘suppressed’’ MCs was taken as the reference. 95% CI indicates 95% confidence interval; OR, odds ratio. In univariable regressions, posterior bulging was more strongly associated with fat suppression status of type II MCs, compared with anterior bulging and total bulging. Thus, posterior bulging was used in the final multiple logistic regression model. Disc signal intensity was adjusted by that of adjacent cerebrospinal fluid and further standardized in data analysis.

II MCs were typically regarded as fat degeneration in the MCs may also help to explain the inconsistent findings on vertebral marrow. We hypothesized that most type II MCs the association between type II MCs and back pain.18,32 will be suppressed on FS images, if the main pathological There are some limitations in this study. As a radiological component of type II MCs is fat. Contrary to our hypothesis, study, the current study is not able to fully elucidate the however, only a quarter of type II MCs presented suppressed pathology of type II MCs. A histological study is needed to signal on FS sequence. We thus postulated that other path- confirm our findings. Secondly, we used clinical patients as a ologies that can lead to relatively higher signal than fat on FS convenient sample. It is possible that more type II MCs will images, such as active inflammation and resultant edema, be suppressed on FS image, if asymptomatic young volun- may also contribute to the pathology of type II MCs. teers were studied. Also, we did not include clinical data and The present study used T2W and SPAIR sequences to the association between FS classification and back pain quantify fat component for type II MCs. SPAIR is a remains undetermined. In addition, signals on MR images powerful FS technique that excites only fat protons. In may be affected by various imaging conditions. Yet, the use quantification for fat, previous studies have proven that of adjacent CSF signal as a reference to adjust signal SPAIR is superior to conventional inversion-recovery FS measurements allows reasonable comparisons between technique such as STIR, as it has a high signal-noise ratio individual MRIs. and a low sensitivity to inhomogeneous radiofrequency In summary, the present study observed that signal of field.19–21 Such a reliable technique allows accurate only a quarter of type II MCs was suppressed on MR FS quantitative measurements. images, suggesting that type II MCs may not always Although MCs were deliberately classified as type I, type represent fat replacement. Histological studies are needed II, and type III, the borderlines between various types may to clarify the pathological entities of type II MCs and to not be clear. Mixed type of MCs, such as mixed type I/II, further understand the role of MCs in back pain. therefore, was further defined.13,22 Longitudinal studies observed that it is common for type I MCs transfer to type II MCs. On the contrary, type II MCs can also convert to Key Points type I MCs or type I/II MCs under certain circumstan- ces.13,23,24 It seems that MCs represent a consecutive proc- For most type II MCs, signal was not suppressed on fat suppression MR images. ess of endplate and bone marrow pathologies. With a specific focus on type II MCs, the current study excluded TypeIIMCsmaynotalwaysrepresentfat mixed-type MCs and other types of MCs. Yet, findings that replacement and there may be ongoing inflammation and edema. signal of most type II MCs was not suppressed on FS images suggested that there are simultaneous inflammatory reac- Older adults are more likely to have MCs that tions or bone edema. Moreover, typically vertebral fat were not suppressed on FS sequences. degeneration is more common in older adults.25–27 Finding Type II MCs was associated with a greater degree that the presence of type II MCs, which is not suppressed on of degeneration at the adjacent disc. FS images, was related to greater age further supports that Type II MCs that were not suppressed on FS there is a complicated pathological process ongoing there. images were associated with greater adjacent Type II MCs, therefore, may not as ‘‘quiescent’’ as pre- disc degeneration. viously thought. These findings may help to explain why type II MCs may transfer to type I or mixed MCs. The association between MCs and disc degeneration has 9,28 References been noticed when MCs were first reported. Measure- 1. Rahme R, Moussa R. 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