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Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study
Journal of Orthopaedic Science xxx (2016) 1e5
Contents lists available at ScienceDirect
Journal of Orthopaedic Science journal homepage: http://www.elsevier.com/locate/jos
Original Article
Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study Kanji Mori*, Toshiyuki Kasahara, Tomohiro Mimura, Kazuya Nishizawa, Akira Nakamura, Shinji Imai Department of Orthopaedic Surgery, Shiga University of Medical Science, Tsukinowa-cho, Seta, Otsu, Shiga, 520-2192, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 7 July 2016 Received in revised form 29 August 2016 Accepted 9 September 2016 Available online xxx
Background: The epidemiology and etiology of diffuse idiopathic skeletal hyperostosis (DISH) remain obscure. To date, to the best of our knowledge, there is no study that precisely evaluated the prevalence of thoracic DISH based on computed tomography (CT) data in large number of non-operated cohort with wide age distribution. Methods: The participants of this study were the consecutive patients who have undergone chest CT for the examination of pulmonary diseases in our institute. The patients with previous thoracic spine surgery and younger than 15 years old were excluded. Chest CT data were reconstructed in the condition suitable for bone evaluation by the software application. Definitive diagnosis of DISH was determined according to the criteria established by Resnick and Niwayama. Prevalence and distribution of thoracic DISH were reviewed and the data was statistically analyzed. Results: Total 3013 patients (1261 females and 1752 males) with the mean age of 65 years were recruited. The CT-based evidence of thoracic DISH was noted in 261 individuals (31 females and 230 males) (8.7%), and their mean age was 73 years. Statistical analyses revealed that thoracic DISH had a significant male preponderance. The mean age of thoracic DISH positive individuals was significantly higher than that of thoracic DISH negative individuals. There was significant difference of bone mass index (BMI) between thoracic DISH positive and negative individuals. Thoracic DISH was noted after the age of 40s with the highest distribution found at the age of 70s. No thoracic DISH localizes only higher thoracic region was found. Conclusions: The CT-based prevalence of thoracic DISH in Japanese was 8.7%. Thoracic DISH has a significant predisposition to elderly male with high BMI. © 2016 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.
1. Introduction Diffuse idiopathic skeletal hyperostosis (DISH) is a common but poorly understood systemic disease characterized by progressive ossification of anterior longitudinal ligaments (OALL) and peripheral entheses [1,2]. DISH does not directly develop neurological compromise; ankylosed spine due to DISH yields biomechanical change of spinal system and act as long bones, which can develop several manifestations peculiar to DISH [2]. Therefore, many clinicians pay attention to DISH in recent practice [2]. Epidemiological studies have conducted to determine the prevalence of DISH in
several regions [3e9]; however its precise prevalence remains unknown. Recently, we have reported the epidemiological study of thoracic ossification of ligamentum flavum (T-OLF) [10] and thoracic ossification of posterior longitudinal ligament (T-OPLL) [11] using chest CT data over 3000 cases. In the present study, using same cohort, we aimed to investigate the prevalence and distribution of thoracic DISH (T-DISH) and reviewed previously published literature.
2. Methods
* Corresponding author. Fax: þ81 77 548 2254. E-mail address: [email protected] (K. Mori).
This study was performed along with the previously published studies by the same author [10,11]. The local ethics committee approved this study.
http://dx.doi.org/10.1016/j.jos.2016.09.003 0949-2658/© 2016 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
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K. Mori et al. / Journal of Orthopaedic Science xxx (2016) 1e5
2.1. Participants The participants of this study were the patients who have undergone chest CT scanning for the examination of pulmonary diseases (pneumonia or pulmonary cancer and their suspicious) in our institute from January 2010 to September 2010. Total 3013 consecutive patients were recruited for the analysis. Of the total of 3013 patients, there were 1261 females and 1752 males with the mean age of 65 years (range, 16e97 years). The patients with previous thoracic spine surgery and younger than 15 years old were excluded from the study. The presence and distribution of T-DISH as well as clinical parameters such as age, sex and body mass index (BMI) were retrospectively reviewed.
contiguous vertebrae, whereas the lesions with spur like incomplete bridge were excludes. Prior to reviewing images, the testers read the same images of 20 patients to check inter- and intraobserver agreement. Intra-observer agreement was determined with evaluation of the same 20 images at separate time points 2 weeks apart. 2.3. Statistical analysis Student's t test, Welch's test and chi-square test were used when appropriate. An odds ratio (OR) and 95% confidence interval (CI) were calculated by chi-square test. p < 0.05 was considered as statistically significant. The software application used for the analysis was Stata/MP 12.0 (StataCorp LP, TX, USA).
2.2. Radiologic examination 3. Results All chest CT scans were axial, 0.5 mm thick, sequential and obtained in supine position without gantry tilt (120 kV, 160 mA, 0.5 s) using a Toshiba Aquilion CX (Toshiba Medical Systems Corporation, Japan). These data were reconstructed in the condition suitable for bone evaluation by the software application (AquariusNet Viewer, TeraRecon, Inc., CA) (Fig. 1). This software application allows us to reconstruct optimal sagittal, coronal and axial views to identify the ossification of the spinal ligaments. On CT scans, typical lesions of DISH are seen as flowing paravertebral ossified masses in anterior aspect of the vertebra (Fig. 1B). Definitive diagnosis of T-DISH was determined according to the criteria established by Resnick and Niwayama [1]. That is, flowing ligamentous ossification in at least four contiguous vertebrae of thoracic spine, preserved intervertebral disc space, as well as the absence of apophyseal joints or sacroiliac inflammatory changes [1]. Since chest CT does not cover sacroiliac joints, involvement of sacroiliac joints was not evaluated in the present study. All CT scans were evaluated by two of the authors; differences were settled by consensus to minimize intra- and inter-observer bias and errors. That is, we counted the lesions with complete bony bridge at least 4
The Kappa coefficient of inter- and intra-observer agreements were was 0.79 and 0.94, respectively. 3.1. Prevalence of T-DISH We could not find the patients with systemic inflammatory/ autoimmune diseases that might cause spinal manifestations in this cohort. The CT-based evidence of T-DISH was noted in 261 individuals (31 females and 230 males) (8.7%), and their mean age was 73 years (range, 47e97 years, Table 1). Statistical analyses revealed that prevalence of T-DISH was significantly higher in males (13%) than in females (2.5%) (p < 0.001). In addition, they also revealed that the mean age of T-DISH positive individuals was significantly higher than that of T-DISH negative individuals, 73 and 64 for the T-DISH positive and negative individuals, respectively (p < 0.001, Table 1). Furthermore, there was significant difference of mean BMI between T-DISH positive and negative males (mean; 23 vs. 22, p < 0.001, Table 1), and that of females demonstrated same trend but did not reached significant statistical
Fig. 1. Reconstructed sagittal computed tomography images of representative case of diffuse idiopathic skeletal hyperostosis. (A) Original condition suitable for pulmonary evaluation, (B) converted image suitable for bone evaluation.
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
K. Mori et al. / Journal of Orthopaedic Science xxx (2016) 1e5
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Table 1 Characterization of DISH positive and negative individuals. Male (n ¼ 1752)
Number (%) Age (yr) (mean ± SD) p BMI (kg/m2) (mean ± SD) p
Female (n ¼ 1261)
Total (n ¼ 3013)
DISH (þ)
DISH ()
DISH (þ)
DISH ()
DISH (þ)
DISH ()
230 (13) 73 ± 8.6 <0.001 23 ± 3.1 <0.001
1522 (87) 65 ± 14
31 (2.5) 70 ± 8.3 <0.001 24 ± 6.0 0.064
1230 (98) 64 ± 15
261 (8.7) 73 ± 8.6 <0.001 23 ± 3.6 <0.001
2752 (91) 64 ± 15
22 ± 3.4
22 ± 3.6
22 ± 3.5
DISH: diffuse idiopathic skeletal hyperostosis, BMI: body mass index, SD: standard deviation, DISH (þ): presence of DISH, DISH (): absence of DISH. Age and BMI were presented as mean ± SD.
difference (mean; 24 vs. 22, p ¼ 0.064, Table 1). We then compared the prevalence of T-DISH among each 10-year age group. We found that T-DISH was noted after the age of 40s and the prevalence of TDISH rose rapidly with age until its peak distribution, the age of 70s (Fig. 2).
3.2. Distribution of T-DISH The number of intervertebral level involved by OALL in T-DISH (minimum 3, maximum 11) was evaluated (Fig. 3). As the assessment of higher thoracic region upper than T5 by standard radiographs is difficult, we evaluated the T-DISH extending to higher thoracic region. We found no T-DISH that localizes only higher thoracic region upper than T5. Among 261 T-DISH positive individuals, T-OPLL positive and TOLF positive individuals were found in 20 (7.7%) and 98 individuals (38%), respectively. Fourteen T-DISH positive individuals (5.4%) had concomitant involvement of both T-OPLL and T-OLF.
4. Discussion DISH recently attracts much attention from both clinicians and researchers. Although DISH has been considered as a largely asymptomatic condition with most affected individuals not aware of its presence [2], accumulating results show that DISH is an indicator for underlining pathological conditions [12e15]. In addition, ankylosed spine yields biomechanical change of musculoskeletal system, which can develop several clinical concerns such as post traumatic paralysis [2,16e19]. In spite of the
Fig. 2. The age-oriented prevalence of diffuse idiopathic skeletal hyperostosis (DISH). The figure indicates the percentage of the DISH positive individuals in each 10-year age group. M: male, F: female.
Fig. 3. The number of intervertebral level bridged by ossification of anterior longitudinal ligament (OALL) in diffuse idiopathic skeletal hyperostosis positive individuals (minimum 3, maximum 11). The figure indicates the number of intervertebral level bridged by OALL.
increasing interest, pathophysiology, course and epidemiology of DISH largely remain unknown [2]. Several studies have reported the prevalence of DISH in several regions, but not covered all over the world [3e9] (Table 2). Most of these reports uniformly documented a significant preponderance of male (in a ratio of 1.3e7:1) and elderly individuals; however the prevalence of DISH in these reports is quite variable ranging from 2.6% to 28% [3e9]. It has been reported that difference of diagnostic criteria employed, race, genetic or hereditary backgrounds and frequency of examination using advanced diagnostic modality in advanced countries were the likely explanations for this discrepancy [2,6,8,9]. Weinfeld et al. recently advocated the importance of genetic or hereditary difference in susceptibility for DISH [6]. They reported that Asian, black and Native American populations had a remarkably lower prevalence of DISH; however the sample size of their study was small [6] (Table 2). More recent two studies reported obviously different prevalence of DISH in Asian [8,9]. The prevalence of DISH in Korean (2.9%) reported by Kim et al. [8] was remarkably lower than that of Japanese (10.8%) reported by Kagotani et al. [9], which was almost similar prevalence of white in Weinfield's report [6]. These two studies employed same diagnostic criteria established by Resnick and Niwayama as in the present study. Prevalence of DISH in the present study (8.7%) was comparable as that of Kagotani et al. These findings indicate that genetic factors might have more impact than race on susceptibility for DISH. Our forgoing two studies revealed that CT scan has contributed to the higher prevalence of T-OLF [10] and T-OPLL [11] due to its high ability to identify the ossified lesions regardless of the anatomical region. In the present CT-based study, however, the prevalence of T-DISH was comparable as that of standard radiographs-based report by Kagotani et al. [9]. CT-based study has
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
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K. Mori et al. / Journal of Orthopaedic Science xxx (2016) 1e5
Table 2 Previously reported prevalence of DISH. Authors/reported year
Country
Sample size
Target
Age (years)
Diagnostic criteria
Modality
Prevalence (%)
Julkunen et al. [3]/1975
Finland
GP
>40
Julkunen
Chest Xp (L)
M: 3.8, F: 2.6, T: 2.6
Boachie-Adjei et al. [4]/1987
USA
P
>45
Forestier
Autopsy, Chest Xp (AP, L, Ob), CT
M:31, F: 23, T: 28
Cassim et al. [5]/1990
South Africa
P
>40
Resnick and Bloom
Chest Xp (L)
M: 3.8, F: 4.2, T: 3.9
Weinfeld et al. [6]/1997
USA
P
>50
Resnick
Chest Xp (PA, L)
M: 25, F: 15, T: NA
Kiss et al. [7]/2002
Hungary
GP
>50
Resnick
Chest Xp (PA, L), dorsal Xp, lumbar Xp
M: 3.8, F: 4.2, T: 3.9
Kim et al. [8]/2004
Korea
P
>50
Resnick
Chest Xp (L) (PACS)
M: 5.4, F: 0.8, T: 2.9
Kim et al. [8]/2004
Korea
P
>50
Julknen
Chest Xp (L) (PACS)
M: 7.1, F: 1.6, T: 4.1
Kagotani et al. [9]/2015
Japan
GP
>23
Resnick
Whole spine Xp (AP, L)
M: 22, F 4.8, T: 11
Mori et al./present study
Japan
T: 8993 M: 4225 F: 4768 T: 75 M: 45 F: 30 T: 1500 M: 1092 F: 408 T: 2364 M: 1107 F: 1257 T: 635 M: 307 F: 328 T: 3595 M: 1616 F: 1979 T: 3595 M: 1616 F: 1979 T: 1647 M: 573 F: 1074 T: 3013 M: 1752 F: 1261
Pa
>16
Resnick
Chest CTb
M: 13, F 2.5, T: 8.7
T: total, M: male, F: female, GP: general population, P: patients, Xp: standard radiographs, AP: anterior-posterior, PA: posterior-anterior, L: lateral, Ob: oblique, PACS: Picture Archiving and Communication System, NA: not available, CT: computed tomography, USA: United States of America. a Patients who have undergone chest CT scanning for the examination of pulmonary diseases. b The data were reconstructed in the condition suitable for bone evaluation by the software application.
most advantageous in the assessment of higher thoracic region, where anatomical complexity prevents accurate evaluation by standard radiographs. Indeed, Kagotani et al. excluded this region, i.e., from C7/T1 to T3/4 from their assessment by standard radiographs [9]. Thus, we carefully evaluated the distribution of T-DISH especially extending to higher thoracic segment in the present study and found that no T-DISH localizes only higher thoracic region upper than T5. In addition, anterior aspect of vertebral body is easier to detect the ossified lesions compared to posterior segment due to its anatomical simplicity. Accordingly, we believe that the prevalence of T-DISH in the present CT-based study was comparable that of previously reported standard radiographs-based study. The results of Kappa coefficient of inter- and intra-observer agreement by reviewing the same images of 20 patients indicated a substantial and excellent agreement [20]; we believe that the present data was reliable. Natural course of the development of DISH is far from complete understanding. Yaniv et al. evaluate the natural progression of bridging OALL in DISH on CT [21], however the site where it start remain undetermined. The finding of the present study suggested that it is likely that T-DISH arises at mid to lower thoracic region and extends upper thoracic region. Thus, CT-based study has no advantage over standard radiographs-based study in DISH? Standard radiographs may be a reliable and safe screening method for DISH [22]; however it is not enough for the evaluation of concomitant involvement of OLF, OPLL and spinal fracture/dislocation. CT can clearly identify these lesions and may be a most suitable modality for the evaluation of these conditions. The etiology and pathophysiology of DISH largely remains unknown [2]; however several constitutional and metabolic derangements have been reported to be associated with DISH. Previous reports advocated possible association of DISH with
endocrine [12e15], metabolic [12,23] and genetic factors [24e26]. Consistent with previous reports, we found a significant association between DISH and high BMI. Significant effects on bone metabolism of altered glucose tolerance as well as many of fat-derived cytokine-like hormones are likely explanations of this association [27]. We could not investigate the association between previously reported the other factors and DISH since clinical information except for age, gender and BMI was not available in the present retrospective study. The present study imposes several limitations. The present study is a patient-based study, not a population-based study. This is the inescapable limitation of the present study; however the protocol of the present study does not impose further radiologic exposure on the participants. Realistically, it appears impossible to perform CT on more than 3000 normal subjects. Our review of the literature failed to find previous report addressing relationship between pulmonary diseases and ossification of the spinal ligaments including DISH. However taking into account of possible association between DISH and systemic disorders, it does not totally cancel the possible association between these two conditions and remains to be elucidated. We cannot evaluate whole spine; however the criteria of DISH originally advocated by Resnick and Niwayama determined the lesions about thoracic spine. Moreover, previous reports uniformly documented that DISH has a significant predisposition to thoracic spine [1,2,8,9]. In addition, sacroiliac joints involvement, one of the diagnostic criteria of DISH by Resnick and Niwayama [1] used in this study, was not evaluated; however we could not find the patients with systemic inflammatory/auto-immune diseases such as ankylosing spondylitis that might cause spinal manifestations in this cohort. Another limitation of the present study is that we cannot evaluate whether clinical manifestations such as pain, stiffness and impaired mobility are significantly associated with DISH. Thus, whether radiological
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
K. Mori et al. / Journal of Orthopaedic Science xxx (2016) 1e5
presence of DISH yields clinical symptoms remains unknown. Further studies that illustrate these concerns are warranted. In conclusion, in the present study, we revealed that the CTbased prevalence of T-DISH in Japanese was 8.7%. T-DISH has a significant predisposition to elderly male with high BMI.
[11]
[12]
Conflict of interest [13]
The authors declare that they have no conflict of interest. Acknowledgment This work was supported by Health and Labour Science Research Grants. No other financial associations that may be relevant or seen as relevant to the submitted manuscript. The authors wish to thank Professor Yoshitaka Murakami, Department of Medical Statistics, Toho University for his kind assistance for statistical analyses.
[14]
[15]
[16]
[17]
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ligament in Japanese: results of CT-based cross-sectional study. Spine (Phila Pa 1976) 2013 Sep 1;38(19):E1216e22. Mori K, Imai S, Kasahara T, Nishizawa K, Mimura T, Matsusue Y. Prevalence, distribution, and morphology of thoracic ossification of the posterior longitudinal ligament in Japanese: results of CT-based cross-sectional study. Spine (Phila Pa 1976) 2014 Mar 1;39(5):394e9. gyi M, Paksy A, Poo r G. Risk factors for diffuse idiopathic skeletal Kiss C, Szila hyperostosis: a case-control study. Rheumatology (Oxford) 2002 Jan;41(1): 27e30. Sahin G, Polat G, Bagis S, Milcan A, Erdogan C. Study of axial bone mineral density in postmenopausal women with diffuse idiopathic skeletal hyperostosis related to type 2 diabetes mellitus. J Womens Health (Larchmt) 2002 Nov;11(9):801e4. Coaccioli S, Fatati G, Di Cato L, Marioli D, Patucchi E, Pizzuti C, Ponteggia M, Puxeddu A. Diffuse idiopathic skeletal hyperostosis in diabetes mellitus, impaired glucose tolerance and obesity. Panminerva Med 2000 Dec;42(4): 247e51. el Miedany YM, Wassif G, el Baddini M. Diffuse idiopathic skeletal hyperostosis (DISH): is it of vascular aetiology? Clin Exp Rheumatol 2000 MareApr;18(2):193e200. Liu P, Yao Y, Liu MY, Fan WL, Chao R, Wang ZG, Liu YC, Zhou JH, Zhao JH. Spinal trauma in mainland China from 2001 to 2007: an epidemiological study based on a nationwide database. Spine (Phila Pa 1976) 2012 Jul 1;37(15):1310e5. Caron T, Bransford R, Nguyen Q, Agel J, Chapman J, Bellabarba C. Spine fractures in patients with ankylosing spinal disorders. Spine (Phila Pa 1976) 2010 May 15;35(11):E458e64. Westerveld LA, van Bemmel JC, Dhert WJ, Oner FC, Verlaan JJ. Clinical outcome after traumatic spinal fractures in patients with ankylosing spinal disorders compared with control patients. Spine J 2014 May 1;14(5):729e40. Westerveld LA, Verlaan JJ, Oner FC. Spinal fractures in patients with ankylosing spinal disorders: a systematic review of the literature on treatment, neurological status and complications. Eur Spine J 2009 Feb;18(2):145e56. Karanicolas PJ, Bhandari M, Kreder H, Moroni A, Richardson M, Walter SD, Norman GR, Guyatt GH. Collaboration for outcome assessment in surgical trials (COAST) musculoskeletal group. Evaluating agreement: conducting a reliability study. J Bone Joint Surg Am 2009 May;91(Suppl. 3):99e106. Yaniv G, Bader S, Lidar M, Herman A, Shazar N, Aharoni D, Eshed I. The natural course of bridging osteophyte formation in diffuse idiopathic skeletal hyperostosis: retrospective analysis of consecutive CT examinations over 10 years. Rheumatology (Oxford) 2014 Nov;53(11):1951e7. Mata S, Hill RO, Joseph L, Kaplan P, Dussault R, Watts CS, Fitzcharles MA, Shiroky JB, Fortin PR, Esdaile JM. Chest radiographs as a screening test for diffuse idiopathic skeletal hyperostosis. J Rheumatol 1993 Nov;20(11): 1905e10. Mader R, Novofestovski I, Adawi M, Lavi I. Metabolic syndrome and cardiovascular risk in patients with diffuse idiopathic skeletal hyperostosis. Semin Arthritis Rheum 2009 Apr;38(5):361e5. Shapiro RF, Utsinger PD, Wiesner KB, Resnick D, Bryan BL, Castles JL. The association of HL-A B27 with Forestier's disease (vertebral ankylosing hyperostosis). J Rheumatol 1976 Mar;3(1):4e8. Rosenthal M, Bahous I, Muller W. Increased frequency of HLA B8 in hyperostotic spondylosis. J Rheumatol Suppl 1977;3:94e6. Brigode M, Francois RJ. Histocompatibility antigens in vertebral ankylosing hyperostosis. J Rheumatol 1977;4(4):429e34. Winter. Pillai S, Littlejohn G. Metabolic factors in diffuse idiopathic skeletal hyperostosis e a review of clinical data. Open Rheumatol J 2014 Dec 19;8:116e28.
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
Contents lists available at ScienceDirect
Journal of Orthopaedic Science journal homepage: http://www.elsevier.com/locate/jos
Original Article
Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study Kanji Mori*, Toshiyuki Kasahara, Tomohiro Mimura, Kazuya Nishizawa, Akira Nakamura, Shinji Imai Department of Orthopaedic Surgery, Shiga University of Medical Science, Tsukinowa-cho, Seta, Otsu, Shiga, 520-2192, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 7 July 2016 Received in revised form 29 August 2016 Accepted 9 September 2016 Available online xxx
Background: The epidemiology and etiology of diffuse idiopathic skeletal hyperostosis (DISH) remain obscure. To date, to the best of our knowledge, there is no study that precisely evaluated the prevalence of thoracic DISH based on computed tomography (CT) data in large number of non-operated cohort with wide age distribution. Methods: The participants of this study were the consecutive patients who have undergone chest CT for the examination of pulmonary diseases in our institute. The patients with previous thoracic spine surgery and younger than 15 years old were excluded. Chest CT data were reconstructed in the condition suitable for bone evaluation by the software application. Definitive diagnosis of DISH was determined according to the criteria established by Resnick and Niwayama. Prevalence and distribution of thoracic DISH were reviewed and the data was statistically analyzed. Results: Total 3013 patients (1261 females and 1752 males) with the mean age of 65 years were recruited. The CT-based evidence of thoracic DISH was noted in 261 individuals (31 females and 230 males) (8.7%), and their mean age was 73 years. Statistical analyses revealed that thoracic DISH had a significant male preponderance. The mean age of thoracic DISH positive individuals was significantly higher than that of thoracic DISH negative individuals. There was significant difference of bone mass index (BMI) between thoracic DISH positive and negative individuals. Thoracic DISH was noted after the age of 40s with the highest distribution found at the age of 70s. No thoracic DISH localizes only higher thoracic region was found. Conclusions: The CT-based prevalence of thoracic DISH in Japanese was 8.7%. Thoracic DISH has a significant predisposition to elderly male with high BMI. © 2016 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.
1. Introduction Diffuse idiopathic skeletal hyperostosis (DISH) is a common but poorly understood systemic disease characterized by progressive ossification of anterior longitudinal ligaments (OALL) and peripheral entheses [1,2]. DISH does not directly develop neurological compromise; ankylosed spine due to DISH yields biomechanical change of spinal system and act as long bones, which can develop several manifestations peculiar to DISH [2]. Therefore, many clinicians pay attention to DISH in recent practice [2]. Epidemiological studies have conducted to determine the prevalence of DISH in
several regions [3e9]; however its precise prevalence remains unknown. Recently, we have reported the epidemiological study of thoracic ossification of ligamentum flavum (T-OLF) [10] and thoracic ossification of posterior longitudinal ligament (T-OPLL) [11] using chest CT data over 3000 cases. In the present study, using same cohort, we aimed to investigate the prevalence and distribution of thoracic DISH (T-DISH) and reviewed previously published literature.
2. Methods
* Corresponding author. Fax: þ81 77 548 2254. E-mail address: [email protected] (K. Mori).
This study was performed along with the previously published studies by the same author [10,11]. The local ethics committee approved this study.
http://dx.doi.org/10.1016/j.jos.2016.09.003 0949-2658/© 2016 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
2
K. Mori et al. / Journal of Orthopaedic Science xxx (2016) 1e5
2.1. Participants The participants of this study were the patients who have undergone chest CT scanning for the examination of pulmonary diseases (pneumonia or pulmonary cancer and their suspicious) in our institute from January 2010 to September 2010. Total 3013 consecutive patients were recruited for the analysis. Of the total of 3013 patients, there were 1261 females and 1752 males with the mean age of 65 years (range, 16e97 years). The patients with previous thoracic spine surgery and younger than 15 years old were excluded from the study. The presence and distribution of T-DISH as well as clinical parameters such as age, sex and body mass index (BMI) were retrospectively reviewed.
contiguous vertebrae, whereas the lesions with spur like incomplete bridge were excludes. Prior to reviewing images, the testers read the same images of 20 patients to check inter- and intraobserver agreement. Intra-observer agreement was determined with evaluation of the same 20 images at separate time points 2 weeks apart. 2.3. Statistical analysis Student's t test, Welch's test and chi-square test were used when appropriate. An odds ratio (OR) and 95% confidence interval (CI) were calculated by chi-square test. p < 0.05 was considered as statistically significant. The software application used for the analysis was Stata/MP 12.0 (StataCorp LP, TX, USA).
2.2. Radiologic examination 3. Results All chest CT scans were axial, 0.5 mm thick, sequential and obtained in supine position without gantry tilt (120 kV, 160 mA, 0.5 s) using a Toshiba Aquilion CX (Toshiba Medical Systems Corporation, Japan). These data were reconstructed in the condition suitable for bone evaluation by the software application (AquariusNet Viewer, TeraRecon, Inc., CA) (Fig. 1). This software application allows us to reconstruct optimal sagittal, coronal and axial views to identify the ossification of the spinal ligaments. On CT scans, typical lesions of DISH are seen as flowing paravertebral ossified masses in anterior aspect of the vertebra (Fig. 1B). Definitive diagnosis of T-DISH was determined according to the criteria established by Resnick and Niwayama [1]. That is, flowing ligamentous ossification in at least four contiguous vertebrae of thoracic spine, preserved intervertebral disc space, as well as the absence of apophyseal joints or sacroiliac inflammatory changes [1]. Since chest CT does not cover sacroiliac joints, involvement of sacroiliac joints was not evaluated in the present study. All CT scans were evaluated by two of the authors; differences were settled by consensus to minimize intra- and inter-observer bias and errors. That is, we counted the lesions with complete bony bridge at least 4
The Kappa coefficient of inter- and intra-observer agreements were was 0.79 and 0.94, respectively. 3.1. Prevalence of T-DISH We could not find the patients with systemic inflammatory/ autoimmune diseases that might cause spinal manifestations in this cohort. The CT-based evidence of T-DISH was noted in 261 individuals (31 females and 230 males) (8.7%), and their mean age was 73 years (range, 47e97 years, Table 1). Statistical analyses revealed that prevalence of T-DISH was significantly higher in males (13%) than in females (2.5%) (p < 0.001). In addition, they also revealed that the mean age of T-DISH positive individuals was significantly higher than that of T-DISH negative individuals, 73 and 64 for the T-DISH positive and negative individuals, respectively (p < 0.001, Table 1). Furthermore, there was significant difference of mean BMI between T-DISH positive and negative males (mean; 23 vs. 22, p < 0.001, Table 1), and that of females demonstrated same trend but did not reached significant statistical
Fig. 1. Reconstructed sagittal computed tomography images of representative case of diffuse idiopathic skeletal hyperostosis. (A) Original condition suitable for pulmonary evaluation, (B) converted image suitable for bone evaluation.
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
K. Mori et al. / Journal of Orthopaedic Science xxx (2016) 1e5
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Table 1 Characterization of DISH positive and negative individuals. Male (n ¼ 1752)
Number (%) Age (yr) (mean ± SD) p BMI (kg/m2) (mean ± SD) p
Female (n ¼ 1261)
Total (n ¼ 3013)
DISH (þ)
DISH ()
DISH (þ)
DISH ()
DISH (þ)
DISH ()
230 (13) 73 ± 8.6 <0.001 23 ± 3.1 <0.001
1522 (87) 65 ± 14
31 (2.5) 70 ± 8.3 <0.001 24 ± 6.0 0.064
1230 (98) 64 ± 15
261 (8.7) 73 ± 8.6 <0.001 23 ± 3.6 <0.001
2752 (91) 64 ± 15
22 ± 3.4
22 ± 3.6
22 ± 3.5
DISH: diffuse idiopathic skeletal hyperostosis, BMI: body mass index, SD: standard deviation, DISH (þ): presence of DISH, DISH (): absence of DISH. Age and BMI were presented as mean ± SD.
difference (mean; 24 vs. 22, p ¼ 0.064, Table 1). We then compared the prevalence of T-DISH among each 10-year age group. We found that T-DISH was noted after the age of 40s and the prevalence of TDISH rose rapidly with age until its peak distribution, the age of 70s (Fig. 2).
3.2. Distribution of T-DISH The number of intervertebral level involved by OALL in T-DISH (minimum 3, maximum 11) was evaluated (Fig. 3). As the assessment of higher thoracic region upper than T5 by standard radiographs is difficult, we evaluated the T-DISH extending to higher thoracic region. We found no T-DISH that localizes only higher thoracic region upper than T5. Among 261 T-DISH positive individuals, T-OPLL positive and TOLF positive individuals were found in 20 (7.7%) and 98 individuals (38%), respectively. Fourteen T-DISH positive individuals (5.4%) had concomitant involvement of both T-OPLL and T-OLF.
4. Discussion DISH recently attracts much attention from both clinicians and researchers. Although DISH has been considered as a largely asymptomatic condition with most affected individuals not aware of its presence [2], accumulating results show that DISH is an indicator for underlining pathological conditions [12e15]. In addition, ankylosed spine yields biomechanical change of musculoskeletal system, which can develop several clinical concerns such as post traumatic paralysis [2,16e19]. In spite of the
Fig. 2. The age-oriented prevalence of diffuse idiopathic skeletal hyperostosis (DISH). The figure indicates the percentage of the DISH positive individuals in each 10-year age group. M: male, F: female.
Fig. 3. The number of intervertebral level bridged by ossification of anterior longitudinal ligament (OALL) in diffuse idiopathic skeletal hyperostosis positive individuals (minimum 3, maximum 11). The figure indicates the number of intervertebral level bridged by OALL.
increasing interest, pathophysiology, course and epidemiology of DISH largely remain unknown [2]. Several studies have reported the prevalence of DISH in several regions, but not covered all over the world [3e9] (Table 2). Most of these reports uniformly documented a significant preponderance of male (in a ratio of 1.3e7:1) and elderly individuals; however the prevalence of DISH in these reports is quite variable ranging from 2.6% to 28% [3e9]. It has been reported that difference of diagnostic criteria employed, race, genetic or hereditary backgrounds and frequency of examination using advanced diagnostic modality in advanced countries were the likely explanations for this discrepancy [2,6,8,9]. Weinfeld et al. recently advocated the importance of genetic or hereditary difference in susceptibility for DISH [6]. They reported that Asian, black and Native American populations had a remarkably lower prevalence of DISH; however the sample size of their study was small [6] (Table 2). More recent two studies reported obviously different prevalence of DISH in Asian [8,9]. The prevalence of DISH in Korean (2.9%) reported by Kim et al. [8] was remarkably lower than that of Japanese (10.8%) reported by Kagotani et al. [9], which was almost similar prevalence of white in Weinfield's report [6]. These two studies employed same diagnostic criteria established by Resnick and Niwayama as in the present study. Prevalence of DISH in the present study (8.7%) was comparable as that of Kagotani et al. These findings indicate that genetic factors might have more impact than race on susceptibility for DISH. Our forgoing two studies revealed that CT scan has contributed to the higher prevalence of T-OLF [10] and T-OPLL [11] due to its high ability to identify the ossified lesions regardless of the anatomical region. In the present CT-based study, however, the prevalence of T-DISH was comparable as that of standard radiographs-based report by Kagotani et al. [9]. CT-based study has
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
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K. Mori et al. / Journal of Orthopaedic Science xxx (2016) 1e5
Table 2 Previously reported prevalence of DISH. Authors/reported year
Country
Sample size
Target
Age (years)
Diagnostic criteria
Modality
Prevalence (%)
Julkunen et al. [3]/1975
Finland
GP
>40
Julkunen
Chest Xp (L)
M: 3.8, F: 2.6, T: 2.6
Boachie-Adjei et al. [4]/1987
USA
P
>45
Forestier
Autopsy, Chest Xp (AP, L, Ob), CT
M:31, F: 23, T: 28
Cassim et al. [5]/1990
South Africa
P
>40
Resnick and Bloom
Chest Xp (L)
M: 3.8, F: 4.2, T: 3.9
Weinfeld et al. [6]/1997
USA
P
>50
Resnick
Chest Xp (PA, L)
M: 25, F: 15, T: NA
Kiss et al. [7]/2002
Hungary
GP
>50
Resnick
Chest Xp (PA, L), dorsal Xp, lumbar Xp
M: 3.8, F: 4.2, T: 3.9
Kim et al. [8]/2004
Korea
P
>50
Resnick
Chest Xp (L) (PACS)
M: 5.4, F: 0.8, T: 2.9
Kim et al. [8]/2004
Korea
P
>50
Julknen
Chest Xp (L) (PACS)
M: 7.1, F: 1.6, T: 4.1
Kagotani et al. [9]/2015
Japan
GP
>23
Resnick
Whole spine Xp (AP, L)
M: 22, F 4.8, T: 11
Mori et al./present study
Japan
T: 8993 M: 4225 F: 4768 T: 75 M: 45 F: 30 T: 1500 M: 1092 F: 408 T: 2364 M: 1107 F: 1257 T: 635 M: 307 F: 328 T: 3595 M: 1616 F: 1979 T: 3595 M: 1616 F: 1979 T: 1647 M: 573 F: 1074 T: 3013 M: 1752 F: 1261
Pa
>16
Resnick
Chest CTb
M: 13, F 2.5, T: 8.7
T: total, M: male, F: female, GP: general population, P: patients, Xp: standard radiographs, AP: anterior-posterior, PA: posterior-anterior, L: lateral, Ob: oblique, PACS: Picture Archiving and Communication System, NA: not available, CT: computed tomography, USA: United States of America. a Patients who have undergone chest CT scanning for the examination of pulmonary diseases. b The data were reconstructed in the condition suitable for bone evaluation by the software application.
most advantageous in the assessment of higher thoracic region, where anatomical complexity prevents accurate evaluation by standard radiographs. Indeed, Kagotani et al. excluded this region, i.e., from C7/T1 to T3/4 from their assessment by standard radiographs [9]. Thus, we carefully evaluated the distribution of T-DISH especially extending to higher thoracic segment in the present study and found that no T-DISH localizes only higher thoracic region upper than T5. In addition, anterior aspect of vertebral body is easier to detect the ossified lesions compared to posterior segment due to its anatomical simplicity. Accordingly, we believe that the prevalence of T-DISH in the present CT-based study was comparable that of previously reported standard radiographs-based study. The results of Kappa coefficient of inter- and intra-observer agreement by reviewing the same images of 20 patients indicated a substantial and excellent agreement [20]; we believe that the present data was reliable. Natural course of the development of DISH is far from complete understanding. Yaniv et al. evaluate the natural progression of bridging OALL in DISH on CT [21], however the site where it start remain undetermined. The finding of the present study suggested that it is likely that T-DISH arises at mid to lower thoracic region and extends upper thoracic region. Thus, CT-based study has no advantage over standard radiographs-based study in DISH? Standard radiographs may be a reliable and safe screening method for DISH [22]; however it is not enough for the evaluation of concomitant involvement of OLF, OPLL and spinal fracture/dislocation. CT can clearly identify these lesions and may be a most suitable modality for the evaluation of these conditions. The etiology and pathophysiology of DISH largely remains unknown [2]; however several constitutional and metabolic derangements have been reported to be associated with DISH. Previous reports advocated possible association of DISH with
endocrine [12e15], metabolic [12,23] and genetic factors [24e26]. Consistent with previous reports, we found a significant association between DISH and high BMI. Significant effects on bone metabolism of altered glucose tolerance as well as many of fat-derived cytokine-like hormones are likely explanations of this association [27]. We could not investigate the association between previously reported the other factors and DISH since clinical information except for age, gender and BMI was not available in the present retrospective study. The present study imposes several limitations. The present study is a patient-based study, not a population-based study. This is the inescapable limitation of the present study; however the protocol of the present study does not impose further radiologic exposure on the participants. Realistically, it appears impossible to perform CT on more than 3000 normal subjects. Our review of the literature failed to find previous report addressing relationship between pulmonary diseases and ossification of the spinal ligaments including DISH. However taking into account of possible association between DISH and systemic disorders, it does not totally cancel the possible association between these two conditions and remains to be elucidated. We cannot evaluate whole spine; however the criteria of DISH originally advocated by Resnick and Niwayama determined the lesions about thoracic spine. Moreover, previous reports uniformly documented that DISH has a significant predisposition to thoracic spine [1,2,8,9]. In addition, sacroiliac joints involvement, one of the diagnostic criteria of DISH by Resnick and Niwayama [1] used in this study, was not evaluated; however we could not find the patients with systemic inflammatory/auto-immune diseases such as ankylosing spondylitis that might cause spinal manifestations in this cohort. Another limitation of the present study is that we cannot evaluate whether clinical manifestations such as pain, stiffness and impaired mobility are significantly associated with DISH. Thus, whether radiological
Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003
K. Mori et al. / Journal of Orthopaedic Science xxx (2016) 1e5
presence of DISH yields clinical symptoms remains unknown. Further studies that illustrate these concerns are warranted. In conclusion, in the present study, we revealed that the CTbased prevalence of T-DISH in Japanese was 8.7%. T-DISH has a significant predisposition to elderly male with high BMI.
[11]
[12]
Conflict of interest [13]
The authors declare that they have no conflict of interest. Acknowledgment This work was supported by Health and Labour Science Research Grants. No other financial associations that may be relevant or seen as relevant to the submitted manuscript. The authors wish to thank Professor Yoshitaka Murakami, Department of Medical Statistics, Toho University for his kind assistance for statistical analyses.
[14]
[15]
[16]
[17]
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Please cite this article in press as: Mori K, et al., Prevalence of thoracic diffuse idiopathic skeletal hyperostosis (DISH) in Japanese: Results of chest CT-based cross-sectional study, Journal of Orthopaedic Science (2016), http://dx.doi.org/10.1016/j.jos.2016.09.003