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Association of chronic degenerative arthritis related chronic low back pain with altered lumbar facet joint orientation
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ScienceDirect Radiology of Infectious Diseases 6 (2019) 15e20 www.elsevier.com/locate/jrid
Research Article
Association of chronic degenerative arthritis related chronic low back pain with altered lumbar facet joint orientation Gary X. Gong a,*, Dennis H. Gong b, Haiyan Wang c, Martin Auster d Neuroradiology Quantitative Imaging Lab, The Russel H. Morgan Department of Radiology & Radiological Sciences, The Johns Hopkins University School of Medicine, 600 N. Wolfe St./Phipps B-100, Baltimore, MD 21287, USA b Johns Hopkins University Whiting School of Engineering Department of Biomedical Engineering, 3400 N. Charles Street, Clark Hall Suit 208, Baltimore, MD 21218, USA c Shandong Medical Imaging Research Institute Affiliated to Shandong University, Jingwu Road No. 324, Jinan, Shandong 250021, China d Department of Diagnostic Imaging, Johns Hopkins Bayview Medical Center, The Johns Hopkins University School of Medicine, 4940 Eastern Ave., Baltimore, MD 21224, USA a
Received 1 November 2018; revised 12 December 2018; accepted 13 February 2019 Available online 19 February 2019
Abstract Objective: To examine the relationship between changes in lumbar spine facet joint (FJ) orientation and chronic low back pain (CLBP). Methods: We retrospectively analyzed lumbar spine CT and MRI images of 98 patients referred for localized paraspinal CLBP and 98 age-and sex-matched asymptomatic individuals as controls. They were divided into four age groups (A, <40; B, 41e50; C, 51e60; D, 61e70; and E, 71e80 years old, respectively). FJ orientations were evaluated at the L3-4, L4-5, and L5-S1 lumbar levels. Results: FJ angle showed a statistically significant more sagittal orientation in CLBP patients than in control groups in lower lumbar spine segments. The overall mean FJ angles in CLBP groups including all age groups combined at L3-4, L4-5, and L5-S1 levels were 32.33 ± 4.5, 36.11 ± 2.9, and 37.4 ± 6.1, degrees, respectively. The FJ angles in control group for all ages were 32.21 ± 3.7, 38.01 ± 4.6, and 40.18 ± 6.8 , respectively. The differences in FJ angle were statistically significant at both L4-5 and L5-S1 levels between the control and the CLBP groups (p < 0.01). The FJ orientation from upper lumbar spine to lumbar sacral junction demonstrated a gradual more coronal orientation transition in all subjects but this trend was significantly less in CLBP patients. The mean FJ angles for the control group at age groups A, B, C, D, and E were 33.52 ± 3.8, 35.7 ± 4.5, 38.25 ± 2.4, 35.49 ± 4.1, and 38.13 ± 5.8, respectively, while those in the CLBP groups were 35.63 ± 2.4, 35.26 ± 3.6, 35.99 ± 5.1, 35.3 ± 4.3, and 35.17 ± 6.7, respectively. Conclusion: There is a significant association between a more sagittal FJ orientation and facetogenic CLBP in lower lumbar vertebral levels. There is also age-dependent decrease in FJ orientation in sagittal plane at lower lumbar spinal levels in control as well as CLBP groups, however, this decrease in the CLBP groups was significantly more pronounced. Whether this change was an adaptive remodeling or alterations associated with chronic FJ osteoarthropathy should warrant further longitudinal studies. © 2019 Beijing You’an Hospital affiliated to Capital Medical University. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
* Corresponding author. Division of Neuroradiology/Phipps B-100, Johns Hopkins University Hospital, 600 North Wolfe Street, Baltimore, MD 21287, USA. E-mail address: [email protected] (G.X. Gong). Peer review under responsibility of Beijing You'an Hospital affiliated to Capital Medical University.
CLBP is a major health problem affecting close to 85% population during their lifetime with over $600 billion in annual costs associated with medical care and disabilityrelated loss of productivity [1,2]. Roughly 45% of CLBP was caused by FJ pain in patients over age 55 years old [3e5]. FJs also bear about 12%e25% of the vertical spinal
https://doi.org/10.1016/j.jrid.2019.02.001 2352-6211/© 2019 Beijing You’an Hospital affiliated to Capital Medical University. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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G.X. Gong et al. / Radiology of Infectious Diseases 6 (2019) 15e20
burden, depending on the posture and the individuals' morphology [6,7]. To certain degree, FJs are freely moveable diarthrodial joints with synovial lining at their joint surface arranged in different angles at different vertebral levels. A more sagittal FJ orientation can reduce the resistance to anterior shearing force which could lead to increased tendency of anterior gliding with a greater degree of movement [8]. Subsequent such repetitive increased movement could cause FJ arthropathy and FJ pain. Within individuals, the upper segments has a more sagittal and curved orientation resulting in less axial rotation. In the lower segments, the FJs are in more coronal and flat orientation which permits less flexion. It is unclear (1) if this change in FJ orientation in the same patient could explain that CLBP is more frequently caused by pathologies in the lower lumbar segment; and (2) if different FJ angles in certain individuals could impose them to more easily develop CLBP [8,9]. FJ orientation has previously been studied mostly in degenerative spondylolisthesis and tropism. Almost all of those studies were based on radiographs or CT, while CT has been shown as unreliable for characterizing FJ pain [15], since the causes of FJ pain could be compounded by other underlying pathologies which are only detectable by MRI exams, such as, facet synovial cyst or early infection as the cause of symptoms. CLBP caused by altered facet orientations has not been comparatively studied using MRI and other imaging modalities [7]. Furthermore, the variability of FJ orientation differences among individuals has not been studied in age and sex matched asymptomatic control and CLBP patient groups using MRI and CT techniques. Therefore, our goal was to examine the association between FJ orientation and CLBP at different age groups using both MRI and CT in order to define whether changes in FJ orientation can be used as an imaging marker for facetogenic CLBP. 2. Method 2.1. Patient selection After institutional review board approval, retrospective analysis of all the patients' medical records, lumbar spine CT and MRI scans were performed between January 2014 and February 2015 at our institution and affiliated imaging centers. Initially, 325 patients who had lumbar spine MRI scans were identified based on clinical diagnosis of axial CLBP over duration of more than 3 years without radiculopathy. Electronic medical record and pertinent patient questionnaires data at the time of MRI scanning in a standardized manner blinded to MRI images and reports were reviewed. Of those, 232 patients also had lumbar spine CT exams within 6 months period of MRI scan. The CT and MRI scans of these 232 patients were further reviewed with 134 patients excluded due to pathologies which could be responsible for patient's symptoms, including infection, fracture, neoplasm, and facet synovial cyst (>3 mm). Patients with prior spine surgery before undergoing MRI or spinal injections within 6 months before MRI were excluded. Other exclusion criteria also included advanced age
Fig. 1. Patient selection flowchart.
of over 80 years, significant disc space reductions, significant spinal stenosis, congenital spine defect, and previous spinal trauma. The remaining 98 patients were enrolled as the CLBP symptomatic study group. The demographics of patients are shown in Table 1. During the same period of time, 285 CT scans of abdomen and lumbar spine were examined with clinical indications not related to back pain (renal stone, appendicitis, and diverticulitis). From those, 98 individuals were randomly selected with sex and age matched to the symptomatic group to serve as the asymptomatic control group (see Fig. 1). 2.2. Measurement methods The CT scans were performed on multi-slice scanners using continuous 3D volumetric data acquisitions with images reconstructed in bone algorithm and displayed in axial, sagittal and coronal planes in 3 mm reformatted thickness. All the lumbar spine MRI scans include T1- and T2-weighted sagittal and axial views, as well as sagittal STIR and/or T2 fatsaturation sequences on 1.5T and 3T clinical scanners, Table 1 Characteristics of participants (n ¼ 196). Age (range in years) Gender (M/F in %) Back Pain Duration (in month) Body Mass Index (kg/m2, Mean ± SE) Presence of FJ osteoarthropathy (%)
Control
CLBP
P Values
40e72 55/45
45e75 59/41 7e24 31.2 ± 4.7 88.56
>0.05 >0.05
29.5 ± 6.1 31.54
>0.05 <0.0001
G.X. Gong et al. / Radiology of Infectious Diseases 6 (2019) 15e20
displayed in 4 mm thickness. Those CT and MRI images were transmitted in DICOM format and analyzed on clinical work stations. Each MRI or CT scan was systematically assessed for FJ features of interest specifically for the purpose of this study. The same FJ angles were measured on CT axial images and MRI images. Repeated measurements on both CT and MRI confirmed the validity of the method. However, the primary purpose of MRI images was to exclude other compounding underlying pathologies. When there is measurement discrepancy between CT and MRI, CT measurements were taken as the reading since CT had better delineation of the FJ bony contour. The radiologists were blinded to pain and other clinical data when measuring the FJ angles. The FJs angles were measured on axial images at the level of the superior endplate of caudal vertebrae. The angle was measured as described previously [10,11] with MRI and CT modifications (Fig. 2). The angle was calculated by the viewing software automatically. It is defined that the smaller this angle, the FJ is in more sagittal orientation. The angles from both left and right sides were averaged and taken as the orientation data of the facet joints for regression analysis. 2.3. Data analysis Descriptive statistics were calculated separately for males and females with respective t and c2 tests depending upon the variables. Association between age and FJ orientation was evaluated by the Pearson correlation. The criterion for statistical significance was P < 0.05. Statistical analysis was performed with SAS software package, (SAS Institute Inc., Cary, NC).
17
3. Results There were total of 196 subjects evaluated, 81 were females (mean age 62.7 ± 12.61, range 40e75) and 115 were males (mean age 59.81 ± 11.72, range 40e74) (Table 1). The duration of CLBP ranges from 7 to 24 months. The majority (88.56%) of the symptomatic group patients demonstrated varying degree of CT and MRI evidence of FJ osteoarthropathy (hypertrophic articular process and osteophyte, cystic lesions around the FJs, joint effusion on MRI), which has a strong correlation with facetogenic CLBP as demonstrated previously [1e3]. The prevalence of FJ osteoarthropathy (either left or right side) in the CLBP group was 78.56% in females and 92.23% in males, mean 88.56% combined, higher than in the control group (combined at 35.54%). The difference between sexes for the presence of FJ osteoarthropathy was not significant between sexes. For most of the cases, the FJ arthropathy were bilateral (r ¼ 0.91). The FJ orientation was slightly more sagittal in females than in males at L3-4 and L4-5 levels, although the differences were not statistically significant. The correlation between age and facet orientation on both the left (p ¼ 0.031) and right (p ¼ 0.005) sides was significant. There was a more sagittal oriented FJ angle in older age groups at L4-5 and L5-S1 levels (Table 2). This was observed in both control and CLBP groups. However, the FJ angles were significantly more sagittal in orientation in CLBP groups at L4-5 and L5-S1 levels than in control groups (p < 0.01).The overall mean FJ angles in CLBP groups including all ages combined at L3-4, L4-5, and L5-S1 levels were 32.33 ± 4.5, 36.11 ± 2.9, and 37.4 ± 6.1, degrees, respectively. This combined mean FJ
Fig. 2. Method of measuring facet joints angles from the CT (right) and MRI (left) images showing the FJ angle (in red) of the midsagittal line to the facet line, at 2 different lumbar levels. a ¼ FJ angle.
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G.X. Gong et al. / Radiology of Infectious Diseases 6 (2019) 15e20
Table 2 Summary of FJ angles in the Control and CLBP groups. Control
CLBP
L3-4 Age groups (years)
<40, n ¼ 15 41e50, n ¼ 20 51e60, n ¼ 20 61e70, n ¼ 20 71e80, n ¼ 23
30.38 29.11 33.74 33.62 34.21
L4-5 ± ± ± ± ±
1.7 8.3 3.8 3.7 3.2
35.58 36.56 38.63 40.21 39.28
L5-S1 ± ± ± ± ±
6.4 3.7 8.4 1.8 3.4
40.61 41.43 42.39 32.65 40.91
L3-4 ± ± ± ± ±
8.7 5.6 6.4 7.3 1.2
29.67 31.65 32.91 34.01 33.42
L4-5 ± ± ± ± ±
3.8 8.2 1.2 7.3 6.9
34.85 36.21 37.54 35.65 36.23
L5-S1 ± ± ± ± ±
2.3 7.4 6.3 5.7 4.9
39.37 37.92 37.62 36.26 35.85
± ± ± ± ±
7.2 3.6 6.2 3.8 4.3
Data are measured FJ angles in degrees expressed as mean ± standard deviation. L3-4, L4-5, and L5-S1 refer to lumbar spine levels where FJ levels were measured. CLBP: chronic lower back pain. The "n" in each age groups represents the number of individuals in each Control and CLBP groups.
angles in control groups were 32.21 ± 3.7, 38.01 ± 4.6, and 40.18 ± 6.8 , respectively. There was no significant tropism found in either control or CLBP groups. The FJ angles from upper lumbar spine to lumbar sacral junction demonstrated a gradual more coronal orientation transition in all subjects but this trend was significantly less in CLBP patients (Figs. 3 and 4). The mean FJ angles in the control at age groups A, B, C, D, and E were 33.52 ± 3.8, 35.7 ± 4.5, 38.25 ± 2.4, 35.49 ± 4.1, and 38.13 ± 5.8, respectively, while those in the CLBP groups were 35.63 ± 2.4, 35.26 ± 3.6, 35.99 ± 5.1, 35.3 ± 4.3, and 35.17 ± 6.7, respectively. The sagittal orientation of FJ was more significant (p < 0.05) in CLBP groups for patient at 51e60 year old and >71 year old, when compared to control. The body mass index between control and CLBP at all age groups were not significantly different.
In this study, we investigated the association between FJ orientation and CLBP using both MRI and CT images. The results revealed that changes in FJ orientation had a statistically significant association with CLBP. This study is also the first to demonstrate age-related changes of the FJ orientations
at multiple lumbar vertebral levels by CT and MRI in age matched control and CLBP individuals. Our data demonstrated that with aging, the tendency of more coronal orientation of the lumbar FJs gradually decreased, most noticeably in the lower vertebral segments. And more sagittal FJ orientation in the lower lumbar spine levels was significantly correlated with the incidence of CLBP as illustrated in Fig. 5. There were several possible explanations for this observation. The more sagittally aligned lower lumbar spine FJ permitted a greater degree of FJ movement and, in addition, patient body weight induced shearing stresses could cause injuries to the FJ [1214]. Repetitive injuries to the FJ could destroy the FJ joint hyaline cartilaginous surface leading to direct bony contact of the FJ articulation [17]. Some researchers [18,19] have shown that the repetitive direct bony impactions on the FJ could cause stress related micro-fractures of the facets resulting in pain. Others [19,20] believed that degenerative disc volume loss could induce alteration of FJ orientation as a result of adaptive changes of the facet joints due to chronic weight shifting of axial load onto the FJs [21]. This shift could lead to FJ orientation changes producing CLBP over long duration as described above. This theory is partially supported by previous
Fig. 3. Age related changes of FJ angle at different vertebral levels in the control group. Data are expressed as mean.
Fig. 4. Age related changes of FJ angle at different vertebral levels in the CLBP group. Data are expressed as mean.
4. Discussion
G.X. Gong et al. / Radiology of Infectious Diseases 6 (2019) 15e20
19
Fig. 5. Representative FJ angles images in control (upper row) and CLBP (lower row) individuals.
report that there is indeed higher stress in the anteromedial facet joint and a higher degree of abrasion during flexion and rotation [22] by biomechanical modulations. This study also demonstrated age-related changes of FJ orientations at multiple lumbar vertebral levels in age matched control and CLBP individuals (Fig. 6). Our data showed that with aging, the coronal orientation of the lumbar FJs gradually decreased, most dramatically in the lower vertebral segments. With aging there is gradual decrease in intervertebral disc volume causing reduced disc height. As a result, there was an
Fig. 6. Age related changes of FJ angle at the same L5-S1 level in the CLBP group. Data are expressed as mean.
increased FJ weight burden [22] as the vertical load upon the disc was being shifted to the posterior elements mainly the FJs. For this reason, it is tempting to explain this finding by FJ articular process remodeling from biomechanical point of view. Over time, the FJ alignment would change adaptively from more coronal to more sagittal orientations. Interestingly, this age related change in FJ orientation in the control group was relatively milder as compared to CLBP group. One possible explanation was that the individuals in control group were more resistant to the possible adaptive remodeling. This was likely not related to individual body weight as the body mass index, which was positively correlated to axial weight load on the intervertebral discs and FJs, in our CLBP group was not significantly higher than that in the control group. Another hypothetical explanation is that those who would later develop CLBP have a congenital or developmental variant of reduced lumbar spine sagittal FJ angles. If the latter is true, this radiographic evidence of more sagittal FJ orientation could be used as an imaging marker to predict possible eventual development of CLBP. This hypothesis will need further investigation in a larger sample longitudinal study. Using axial CT scans for measurement of the FJ angle was previously demonstrated to be effective and precise [23]. The measurements were straight forward using a well-established technique, and the measurements were performed by experienced radiologists, therefore, we did not test the intra- or interobserver variability. One of the strength of this study was the combined evaluation of MRI images on the same patient. This excluded other causes of facetogenic CLBP. By adding MRI analysis to exclude any underlying compounding factors, our data extended and confirmed previous reports that in the
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thoracolumbar junction (T12eL2), there was a more sagittal orientation of the FJs than in the lower lumbar spine [16]. More recent study also demonstrated this association with severity of FJ arthritis using CT [https://doi.org/10.1155/2013/ 693971]. We did not examine the correlation of the degree of FJ arthropathy in relation to changes in FJ orientation using MRI as MRI was less accurate in grading the severity of hypertrophic bony arthritic changes associated with CLBP. This study could not determine whether the change in FJ orientation represented a pre-existing phenotypic morphology or whether it actually should be considered a result of secondary remodeling. 5. Conclusion The current combined CT and MRI study measured the FJ angles on axial images using large samples of CLBP patients compared with age and sex matched asymptomatic controls. The data demonstrated a significant association between a more sagittal FJ orientation of the lower lumbar spine and facetogenic CLBP. In addition, there was also a gradual decrease of the FJ angles in sagittal orientation with age in both control and CLBP individuals. In CLBP patients this negative correlation of sagittal FJ angle with age was significantly more pronounced at lower lumbar vertebral segments. This study, however, could not determine whether the change in FJ orientation represented a pre-existing phenotypic morphology of certain individuals, or whether the change was due to adaptive remodeling of the FJ from chronically increased axial loading induced by disc volume loss. Further large sample longitudinal studies for better understanding of the age related changes in FJ orientation are needed. References [1] Hoy D, Bain C, Williams G, March L, Brooks P, Blyth F, et al. A systematic review of the global prevalence of low back pain. Arthritis Rheum 2012;64(6):2028e37. [2] Dahlhamer J, Lucas J, Zelaya C, Nahin R, Mackey S, DeBar L, et al. Prevalence of chronic pain and high-impact chronic pain among adults d United States, 2016. MMWR Morb Mortal Wkly Rep 2018;67: 1001e6. [3] DePalma MJ, Ketchum JM, Saullo T. What is the source of chronic low back pain and does age play a role? Pain Med 2011;12:224e33. [4] Manchikanti L, Manchikanti KN, Cash KA, Singh V, Giordano J. Agerelated prevalence of facet-joint involvement in chronic neck and low back pain. Pain Physician 2008;11:67e75.
[5] Manchikanti L, Singh V, Pampati V, Damron KS, Barnhill RC, Beyer C, et al. Evaluation of the relative contributions of various structures in chronic low back pain. Pain Physician 2001;4(4):308e16. [6] Adams MA, Hutton WC. The effect of posture on the role of the apophysial joints in resisting intervertebral compressive forces. J Bone Joint Surg 1980;62(3):358e62. British. [7] Kalichman L, Hunter DJ. Lumbar facet joint osteoarthritis: a review. Semin Arthritis Rheum 2007;37(2):69e80. [8] Cohen SP, Raja SN. Pathogenesis, diagnosis, and treatment of lumbar zygapophysial (facet) joint pain. Anesthesiology 2007;106(3):591e614. [9] Kalichman L, Suri P, Guermazi A, Li L, Hunter DJ. Facet orientation and tropism: associations with facet joint osteoarthritis and degeneratives. Spine 2009;34(16):E579e85. [10] Noren R, Trafimow J, Andersson GB, Huckman MS. The role of facet joint tropism and facet angle in disc degeneration. Spine 1991;16:530e2. [11] Kalichman L, Suri P, Guermazi A, Li L, Hunter DJ. Facet orientation and tropism: associations with facet joint osteoarthritis and degenerative spondylolisthesis. Spine (Phila Pa 1976) 2009;34:E579e85. [12] Hanney WJ, Kolber MJ, Beekhuizen KS. Implications for physical activity in the population with low back pain. Am J Lifestyle Med 2009;3: 63e70. [13] Katz JN. Lumbar disc disorders and low-back pain: socioeconomic factors and consequences. J Bone Joint Surg Am 2006;88(Suppl. 2): 21e4. [14] Heneweer H, Staes F, Aufdemkampe G, van Rijn M, Vanhees L. Physical activity and low back pain: a systematic review of recent literature. Eur Spine J 2011;20:826e45. [15] Jaumard NV, Welch WC, Winkelstein BA. Spinal facet joint biomechanics and mechanotransduction in normal, injury and degenerative conditions. J Biomech Eng 2011 Jul;133(7):071010e31. [16] Steven P, Cohen A, Raja S. Pathogenesis, diagnosis, and treatment of lumbar zygapophysial (facet) joint pain. Anesthesiology 2007;106: 591e614. [17] Benoist M. Natural history of the aging spine. Eur Spine J 2003;12(suppl 2):S86e9. [18] Sengupta DK, Herkowitz HN. Degenerative spondylolisthesis: review of current trends and controversies. Spine 2005;30:S71e81. [19] Fujiwara A, Tamai K, An HS, Lim TH, Yoshida H, Kurihashi A, et al. Orientation and osteoarthritis of the lumbar facet joint. Clin Orthop Relat Res 2001:88e94. [20] Boden SD, Riew KD, Yamaguchi K, Branch TP, Schellinger D, Wiesel SW. Orientation of the lumbar facet joints: association with degenerative disc disease. J Bone Joint Surg Am 1996;78:403e11. [21] Garfin SR, Herkowitz HN. Lumbar disc degeneration: normal aging or a disease process? In: Wiesel SW, Weinstein JN, Herkowitz HN, et al., editors. The lumbar spine. Philadelphia, PA: WB Saunders; 1996. p. 458e73. [22] Dunlop RB, Adams MA, Hutton WC. Disc space narrowing and the lumbar facet joints. J Bone Joint Surg Br 1984;66:706e10. [23] Gunzburg R1, Sandhu A, Fraser RD. The value of computerized tomography in determining lumbar facet joint orientation. J Spinal Disord 1989 Sep;2(3):170e5.
Available online at www.sciencedirect.com
ScienceDirect Radiology of Infectious Diseases 6 (2019) 15e20 www.elsevier.com/locate/jrid
Research Article
Association of chronic degenerative arthritis related chronic low back pain with altered lumbar facet joint orientation Gary X. Gong a,*, Dennis H. Gong b, Haiyan Wang c, Martin Auster d Neuroradiology Quantitative Imaging Lab, The Russel H. Morgan Department of Radiology & Radiological Sciences, The Johns Hopkins University School of Medicine, 600 N. Wolfe St./Phipps B-100, Baltimore, MD 21287, USA b Johns Hopkins University Whiting School of Engineering Department of Biomedical Engineering, 3400 N. Charles Street, Clark Hall Suit 208, Baltimore, MD 21218, USA c Shandong Medical Imaging Research Institute Affiliated to Shandong University, Jingwu Road No. 324, Jinan, Shandong 250021, China d Department of Diagnostic Imaging, Johns Hopkins Bayview Medical Center, The Johns Hopkins University School of Medicine, 4940 Eastern Ave., Baltimore, MD 21224, USA a
Received 1 November 2018; revised 12 December 2018; accepted 13 February 2019 Available online 19 February 2019
Abstract Objective: To examine the relationship between changes in lumbar spine facet joint (FJ) orientation and chronic low back pain (CLBP). Methods: We retrospectively analyzed lumbar spine CT and MRI images of 98 patients referred for localized paraspinal CLBP and 98 age-and sex-matched asymptomatic individuals as controls. They were divided into four age groups (A, <40; B, 41e50; C, 51e60; D, 61e70; and E, 71e80 years old, respectively). FJ orientations were evaluated at the L3-4, L4-5, and L5-S1 lumbar levels. Results: FJ angle showed a statistically significant more sagittal orientation in CLBP patients than in control groups in lower lumbar spine segments. The overall mean FJ angles in CLBP groups including all age groups combined at L3-4, L4-5, and L5-S1 levels were 32.33 ± 4.5, 36.11 ± 2.9, and 37.4 ± 6.1, degrees, respectively. The FJ angles in control group for all ages were 32.21 ± 3.7, 38.01 ± 4.6, and 40.18 ± 6.8 , respectively. The differences in FJ angle were statistically significant at both L4-5 and L5-S1 levels between the control and the CLBP groups (p < 0.01). The FJ orientation from upper lumbar spine to lumbar sacral junction demonstrated a gradual more coronal orientation transition in all subjects but this trend was significantly less in CLBP patients. The mean FJ angles for the control group at age groups A, B, C, D, and E were 33.52 ± 3.8, 35.7 ± 4.5, 38.25 ± 2.4, 35.49 ± 4.1, and 38.13 ± 5.8, respectively, while those in the CLBP groups were 35.63 ± 2.4, 35.26 ± 3.6, 35.99 ± 5.1, 35.3 ± 4.3, and 35.17 ± 6.7, respectively. Conclusion: There is a significant association between a more sagittal FJ orientation and facetogenic CLBP in lower lumbar vertebral levels. There is also age-dependent decrease in FJ orientation in sagittal plane at lower lumbar spinal levels in control as well as CLBP groups, however, this decrease in the CLBP groups was significantly more pronounced. Whether this change was an adaptive remodeling or alterations associated with chronic FJ osteoarthropathy should warrant further longitudinal studies. © 2019 Beijing You’an Hospital affiliated to Capital Medical University. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
* Corresponding author. Division of Neuroradiology/Phipps B-100, Johns Hopkins University Hospital, 600 North Wolfe Street, Baltimore, MD 21287, USA. E-mail address: [email protected] (G.X. Gong). Peer review under responsibility of Beijing You'an Hospital affiliated to Capital Medical University.
CLBP is a major health problem affecting close to 85% population during their lifetime with over $600 billion in annual costs associated with medical care and disabilityrelated loss of productivity [1,2]. Roughly 45% of CLBP was caused by FJ pain in patients over age 55 years old [3e5]. FJs also bear about 12%e25% of the vertical spinal
https://doi.org/10.1016/j.jrid.2019.02.001 2352-6211/© 2019 Beijing You’an Hospital affiliated to Capital Medical University. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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G.X. Gong et al. / Radiology of Infectious Diseases 6 (2019) 15e20
burden, depending on the posture and the individuals' morphology [6,7]. To certain degree, FJs are freely moveable diarthrodial joints with synovial lining at their joint surface arranged in different angles at different vertebral levels. A more sagittal FJ orientation can reduce the resistance to anterior shearing force which could lead to increased tendency of anterior gliding with a greater degree of movement [8]. Subsequent such repetitive increased movement could cause FJ arthropathy and FJ pain. Within individuals, the upper segments has a more sagittal and curved orientation resulting in less axial rotation. In the lower segments, the FJs are in more coronal and flat orientation which permits less flexion. It is unclear (1) if this change in FJ orientation in the same patient could explain that CLBP is more frequently caused by pathologies in the lower lumbar segment; and (2) if different FJ angles in certain individuals could impose them to more easily develop CLBP [8,9]. FJ orientation has previously been studied mostly in degenerative spondylolisthesis and tropism. Almost all of those studies were based on radiographs or CT, while CT has been shown as unreliable for characterizing FJ pain [15], since the causes of FJ pain could be compounded by other underlying pathologies which are only detectable by MRI exams, such as, facet synovial cyst or early infection as the cause of symptoms. CLBP caused by altered facet orientations has not been comparatively studied using MRI and other imaging modalities [7]. Furthermore, the variability of FJ orientation differences among individuals has not been studied in age and sex matched asymptomatic control and CLBP patient groups using MRI and CT techniques. Therefore, our goal was to examine the association between FJ orientation and CLBP at different age groups using both MRI and CT in order to define whether changes in FJ orientation can be used as an imaging marker for facetogenic CLBP. 2. Method 2.1. Patient selection After institutional review board approval, retrospective analysis of all the patients' medical records, lumbar spine CT and MRI scans were performed between January 2014 and February 2015 at our institution and affiliated imaging centers. Initially, 325 patients who had lumbar spine MRI scans were identified based on clinical diagnosis of axial CLBP over duration of more than 3 years without radiculopathy. Electronic medical record and pertinent patient questionnaires data at the time of MRI scanning in a standardized manner blinded to MRI images and reports were reviewed. Of those, 232 patients also had lumbar spine CT exams within 6 months period of MRI scan. The CT and MRI scans of these 232 patients were further reviewed with 134 patients excluded due to pathologies which could be responsible for patient's symptoms, including infection, fracture, neoplasm, and facet synovial cyst (>3 mm). Patients with prior spine surgery before undergoing MRI or spinal injections within 6 months before MRI were excluded. Other exclusion criteria also included advanced age
Fig. 1. Patient selection flowchart.
of over 80 years, significant disc space reductions, significant spinal stenosis, congenital spine defect, and previous spinal trauma. The remaining 98 patients were enrolled as the CLBP symptomatic study group. The demographics of patients are shown in Table 1. During the same period of time, 285 CT scans of abdomen and lumbar spine were examined with clinical indications not related to back pain (renal stone, appendicitis, and diverticulitis). From those, 98 individuals were randomly selected with sex and age matched to the symptomatic group to serve as the asymptomatic control group (see Fig. 1). 2.2. Measurement methods The CT scans were performed on multi-slice scanners using continuous 3D volumetric data acquisitions with images reconstructed in bone algorithm and displayed in axial, sagittal and coronal planes in 3 mm reformatted thickness. All the lumbar spine MRI scans include T1- and T2-weighted sagittal and axial views, as well as sagittal STIR and/or T2 fatsaturation sequences on 1.5T and 3T clinical scanners, Table 1 Characteristics of participants (n ¼ 196). Age (range in years) Gender (M/F in %) Back Pain Duration (in month) Body Mass Index (kg/m2, Mean ± SE) Presence of FJ osteoarthropathy (%)
Control
CLBP
P Values
40e72 55/45
45e75 59/41 7e24 31.2 ± 4.7 88.56
>0.05 >0.05
29.5 ± 6.1 31.54
>0.05 <0.0001
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displayed in 4 mm thickness. Those CT and MRI images were transmitted in DICOM format and analyzed on clinical work stations. Each MRI or CT scan was systematically assessed for FJ features of interest specifically for the purpose of this study. The same FJ angles were measured on CT axial images and MRI images. Repeated measurements on both CT and MRI confirmed the validity of the method. However, the primary purpose of MRI images was to exclude other compounding underlying pathologies. When there is measurement discrepancy between CT and MRI, CT measurements were taken as the reading since CT had better delineation of the FJ bony contour. The radiologists were blinded to pain and other clinical data when measuring the FJ angles. The FJs angles were measured on axial images at the level of the superior endplate of caudal vertebrae. The angle was measured as described previously [10,11] with MRI and CT modifications (Fig. 2). The angle was calculated by the viewing software automatically. It is defined that the smaller this angle, the FJ is in more sagittal orientation. The angles from both left and right sides were averaged and taken as the orientation data of the facet joints for regression analysis. 2.3. Data analysis Descriptive statistics were calculated separately for males and females with respective t and c2 tests depending upon the variables. Association between age and FJ orientation was evaluated by the Pearson correlation. The criterion for statistical significance was P < 0.05. Statistical analysis was performed with SAS software package, (SAS Institute Inc., Cary, NC).
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3. Results There were total of 196 subjects evaluated, 81 were females (mean age 62.7 ± 12.61, range 40e75) and 115 were males (mean age 59.81 ± 11.72, range 40e74) (Table 1). The duration of CLBP ranges from 7 to 24 months. The majority (88.56%) of the symptomatic group patients demonstrated varying degree of CT and MRI evidence of FJ osteoarthropathy (hypertrophic articular process and osteophyte, cystic lesions around the FJs, joint effusion on MRI), which has a strong correlation with facetogenic CLBP as demonstrated previously [1e3]. The prevalence of FJ osteoarthropathy (either left or right side) in the CLBP group was 78.56% in females and 92.23% in males, mean 88.56% combined, higher than in the control group (combined at 35.54%). The difference between sexes for the presence of FJ osteoarthropathy was not significant between sexes. For most of the cases, the FJ arthropathy were bilateral (r ¼ 0.91). The FJ orientation was slightly more sagittal in females than in males at L3-4 and L4-5 levels, although the differences were not statistically significant. The correlation between age and facet orientation on both the left (p ¼ 0.031) and right (p ¼ 0.005) sides was significant. There was a more sagittal oriented FJ angle in older age groups at L4-5 and L5-S1 levels (Table 2). This was observed in both control and CLBP groups. However, the FJ angles were significantly more sagittal in orientation in CLBP groups at L4-5 and L5-S1 levels than in control groups (p < 0.01).The overall mean FJ angles in CLBP groups including all ages combined at L3-4, L4-5, and L5-S1 levels were 32.33 ± 4.5, 36.11 ± 2.9, and 37.4 ± 6.1, degrees, respectively. This combined mean FJ
Fig. 2. Method of measuring facet joints angles from the CT (right) and MRI (left) images showing the FJ angle (in red) of the midsagittal line to the facet line, at 2 different lumbar levels. a ¼ FJ angle.
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Table 2 Summary of FJ angles in the Control and CLBP groups. Control
CLBP
L3-4 Age groups (years)
<40, n ¼ 15 41e50, n ¼ 20 51e60, n ¼ 20 61e70, n ¼ 20 71e80, n ¼ 23
30.38 29.11 33.74 33.62 34.21
L4-5 ± ± ± ± ±
1.7 8.3 3.8 3.7 3.2
35.58 36.56 38.63 40.21 39.28
L5-S1 ± ± ± ± ±
6.4 3.7 8.4 1.8 3.4
40.61 41.43 42.39 32.65 40.91
L3-4 ± ± ± ± ±
8.7 5.6 6.4 7.3 1.2
29.67 31.65 32.91 34.01 33.42
L4-5 ± ± ± ± ±
3.8 8.2 1.2 7.3 6.9
34.85 36.21 37.54 35.65 36.23
L5-S1 ± ± ± ± ±
2.3 7.4 6.3 5.7 4.9
39.37 37.92 37.62 36.26 35.85
± ± ± ± ±
7.2 3.6 6.2 3.8 4.3
Data are measured FJ angles in degrees expressed as mean ± standard deviation. L3-4, L4-5, and L5-S1 refer to lumbar spine levels where FJ levels were measured. CLBP: chronic lower back pain. The "n" in each age groups represents the number of individuals in each Control and CLBP groups.
angles in control groups were 32.21 ± 3.7, 38.01 ± 4.6, and 40.18 ± 6.8 , respectively. There was no significant tropism found in either control or CLBP groups. The FJ angles from upper lumbar spine to lumbar sacral junction demonstrated a gradual more coronal orientation transition in all subjects but this trend was significantly less in CLBP patients (Figs. 3 and 4). The mean FJ angles in the control at age groups A, B, C, D, and E were 33.52 ± 3.8, 35.7 ± 4.5, 38.25 ± 2.4, 35.49 ± 4.1, and 38.13 ± 5.8, respectively, while those in the CLBP groups were 35.63 ± 2.4, 35.26 ± 3.6, 35.99 ± 5.1, 35.3 ± 4.3, and 35.17 ± 6.7, respectively. The sagittal orientation of FJ was more significant (p < 0.05) in CLBP groups for patient at 51e60 year old and >71 year old, when compared to control. The body mass index between control and CLBP at all age groups were not significantly different.
In this study, we investigated the association between FJ orientation and CLBP using both MRI and CT images. The results revealed that changes in FJ orientation had a statistically significant association with CLBP. This study is also the first to demonstrate age-related changes of the FJ orientations
at multiple lumbar vertebral levels by CT and MRI in age matched control and CLBP individuals. Our data demonstrated that with aging, the tendency of more coronal orientation of the lumbar FJs gradually decreased, most noticeably in the lower vertebral segments. And more sagittal FJ orientation in the lower lumbar spine levels was significantly correlated with the incidence of CLBP as illustrated in Fig. 5. There were several possible explanations for this observation. The more sagittally aligned lower lumbar spine FJ permitted a greater degree of FJ movement and, in addition, patient body weight induced shearing stresses could cause injuries to the FJ [1214]. Repetitive injuries to the FJ could destroy the FJ joint hyaline cartilaginous surface leading to direct bony contact of the FJ articulation [17]. Some researchers [18,19] have shown that the repetitive direct bony impactions on the FJ could cause stress related micro-fractures of the facets resulting in pain. Others [19,20] believed that degenerative disc volume loss could induce alteration of FJ orientation as a result of adaptive changes of the facet joints due to chronic weight shifting of axial load onto the FJs [21]. This shift could lead to FJ orientation changes producing CLBP over long duration as described above. This theory is partially supported by previous
Fig. 3. Age related changes of FJ angle at different vertebral levels in the control group. Data are expressed as mean.
Fig. 4. Age related changes of FJ angle at different vertebral levels in the CLBP group. Data are expressed as mean.
4. Discussion
G.X. Gong et al. / Radiology of Infectious Diseases 6 (2019) 15e20
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Fig. 5. Representative FJ angles images in control (upper row) and CLBP (lower row) individuals.
report that there is indeed higher stress in the anteromedial facet joint and a higher degree of abrasion during flexion and rotation [22] by biomechanical modulations. This study also demonstrated age-related changes of FJ orientations at multiple lumbar vertebral levels in age matched control and CLBP individuals (Fig. 6). Our data showed that with aging, the coronal orientation of the lumbar FJs gradually decreased, most dramatically in the lower vertebral segments. With aging there is gradual decrease in intervertebral disc volume causing reduced disc height. As a result, there was an
Fig. 6. Age related changes of FJ angle at the same L5-S1 level in the CLBP group. Data are expressed as mean.
increased FJ weight burden [22] as the vertical load upon the disc was being shifted to the posterior elements mainly the FJs. For this reason, it is tempting to explain this finding by FJ articular process remodeling from biomechanical point of view. Over time, the FJ alignment would change adaptively from more coronal to more sagittal orientations. Interestingly, this age related change in FJ orientation in the control group was relatively milder as compared to CLBP group. One possible explanation was that the individuals in control group were more resistant to the possible adaptive remodeling. This was likely not related to individual body weight as the body mass index, which was positively correlated to axial weight load on the intervertebral discs and FJs, in our CLBP group was not significantly higher than that in the control group. Another hypothetical explanation is that those who would later develop CLBP have a congenital or developmental variant of reduced lumbar spine sagittal FJ angles. If the latter is true, this radiographic evidence of more sagittal FJ orientation could be used as an imaging marker to predict possible eventual development of CLBP. This hypothesis will need further investigation in a larger sample longitudinal study. Using axial CT scans for measurement of the FJ angle was previously demonstrated to be effective and precise [23]. The measurements were straight forward using a well-established technique, and the measurements were performed by experienced radiologists, therefore, we did not test the intra- or interobserver variability. One of the strength of this study was the combined evaluation of MRI images on the same patient. This excluded other causes of facetogenic CLBP. By adding MRI analysis to exclude any underlying compounding factors, our data extended and confirmed previous reports that in the
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thoracolumbar junction (T12eL2), there was a more sagittal orientation of the FJs than in the lower lumbar spine [16]. More recent study also demonstrated this association with severity of FJ arthritis using CT [https://doi.org/10.1155/2013/ 693971]. We did not examine the correlation of the degree of FJ arthropathy in relation to changes in FJ orientation using MRI as MRI was less accurate in grading the severity of hypertrophic bony arthritic changes associated with CLBP. This study could not determine whether the change in FJ orientation represented a pre-existing phenotypic morphology or whether it actually should be considered a result of secondary remodeling. 5. Conclusion The current combined CT and MRI study measured the FJ angles on axial images using large samples of CLBP patients compared with age and sex matched asymptomatic controls. The data demonstrated a significant association between a more sagittal FJ orientation of the lower lumbar spine and facetogenic CLBP. In addition, there was also a gradual decrease of the FJ angles in sagittal orientation with age in both control and CLBP individuals. In CLBP patients this negative correlation of sagittal FJ angle with age was significantly more pronounced at lower lumbar vertebral segments. This study, however, could not determine whether the change in FJ orientation represented a pre-existing phenotypic morphology of certain individuals, or whether the change was due to adaptive remodeling of the FJ from chronically increased axial loading induced by disc volume loss. Further large sample longitudinal studies for better understanding of the age related changes in FJ orientation are needed. References [1] Hoy D, Bain C, Williams G, March L, Brooks P, Blyth F, et al. A systematic review of the global prevalence of low back pain. Arthritis Rheum 2012;64(6):2028e37. [2] Dahlhamer J, Lucas J, Zelaya C, Nahin R, Mackey S, DeBar L, et al. Prevalence of chronic pain and high-impact chronic pain among adults d United States, 2016. MMWR Morb Mortal Wkly Rep 2018;67: 1001e6. [3] DePalma MJ, Ketchum JM, Saullo T. What is the source of chronic low back pain and does age play a role? Pain Med 2011;12:224e33. [4] Manchikanti L, Manchikanti KN, Cash KA, Singh V, Giordano J. Agerelated prevalence of facet-joint involvement in chronic neck and low back pain. Pain Physician 2008;11:67e75.
[5] Manchikanti L, Singh V, Pampati V, Damron KS, Barnhill RC, Beyer C, et al. Evaluation of the relative contributions of various structures in chronic low back pain. Pain Physician 2001;4(4):308e16. [6] Adams MA, Hutton WC. The effect of posture on the role of the apophysial joints in resisting intervertebral compressive forces. J Bone Joint Surg 1980;62(3):358e62. British. [7] Kalichman L, Hunter DJ. Lumbar facet joint osteoarthritis: a review. Semin Arthritis Rheum 2007;37(2):69e80. [8] Cohen SP, Raja SN. Pathogenesis, diagnosis, and treatment of lumbar zygapophysial (facet) joint pain. Anesthesiology 2007;106(3):591e614. [9] Kalichman L, Suri P, Guermazi A, Li L, Hunter DJ. Facet orientation and tropism: associations with facet joint osteoarthritis and degeneratives. Spine 2009;34(16):E579e85. [10] Noren R, Trafimow J, Andersson GB, Huckman MS. The role of facet joint tropism and facet angle in disc degeneration. Spine 1991;16:530e2. [11] Kalichman L, Suri P, Guermazi A, Li L, Hunter DJ. Facet orientation and tropism: associations with facet joint osteoarthritis and degenerative spondylolisthesis. Spine (Phila Pa 1976) 2009;34:E579e85. [12] Hanney WJ, Kolber MJ, Beekhuizen KS. Implications for physical activity in the population with low back pain. Am J Lifestyle Med 2009;3: 63e70. [13] Katz JN. Lumbar disc disorders and low-back pain: socioeconomic factors and consequences. J Bone Joint Surg Am 2006;88(Suppl. 2): 21e4. [14] Heneweer H, Staes F, Aufdemkampe G, van Rijn M, Vanhees L. Physical activity and low back pain: a systematic review of recent literature. Eur Spine J 2011;20:826e45. [15] Jaumard NV, Welch WC, Winkelstein BA. Spinal facet joint biomechanics and mechanotransduction in normal, injury and degenerative conditions. J Biomech Eng 2011 Jul;133(7):071010e31. [16] Steven P, Cohen A, Raja S. Pathogenesis, diagnosis, and treatment of lumbar zygapophysial (facet) joint pain. Anesthesiology 2007;106: 591e614. [17] Benoist M. Natural history of the aging spine. Eur Spine J 2003;12(suppl 2):S86e9. [18] Sengupta DK, Herkowitz HN. Degenerative spondylolisthesis: review of current trends and controversies. Spine 2005;30:S71e81. [19] Fujiwara A, Tamai K, An HS, Lim TH, Yoshida H, Kurihashi A, et al. Orientation and osteoarthritis of the lumbar facet joint. Clin Orthop Relat Res 2001:88e94. [20] Boden SD, Riew KD, Yamaguchi K, Branch TP, Schellinger D, Wiesel SW. Orientation of the lumbar facet joints: association with degenerative disc disease. J Bone Joint Surg Am 1996;78:403e11. [21] Garfin SR, Herkowitz HN. Lumbar disc degeneration: normal aging or a disease process? In: Wiesel SW, Weinstein JN, Herkowitz HN, et al., editors. The lumbar spine. Philadelphia, PA: WB Saunders; 1996. p. 458e73. [22] Dunlop RB, Adams MA, Hutton WC. Disc space narrowing and the lumbar facet joints. J Bone Joint Surg Br 1984;66:706e10. [23] Gunzburg R1, Sandhu A, Fraser RD. The value of computerized tomography in determining lumbar facet joint orientation. J Spinal Disord 1989 Sep;2(3):170e5.