712 C OPYRIGHT Ó 2014
BY
T HE J OURNAL
OF
B ONE
AND J OINT
S URGERY, I NCORPORATED
Association Between Advanced Degenerative Changes of the Atlanto-Dens Joint and Presence of Dens Fracture Matthew S. Shinseki, Natalie L. Zusman, BS, Jayme Hiratzka, MD, Lynn M. Marshall, ScD, and Jung U. Yoo, MD Investigation performed at the Department of Orthopaedics and Rehabilitation, Oregon Health & Science University, Portland, Oregon
Background: Dens fractures in elderly patients are often related to issues associated with aging. We examined the association between degenerative changes of the atlanto-dens joint and the risk of dens fracture. Methods: We conducted a retrospective study of trauma patients, fifty-five years of age or older, who had undergone a computed tomography scan of the cervical spine as part of their admission to a single level-I trauma center. There were 1794 patients who met the inclusion criteria; scans were evaluated for all fifty-six who presented with a dens fracture and for a random sample of 736 without a dens fracture. Intraosseous cyst formation, synovitis, and joint space narrowing were recorded from the scans. The prevalence of degenerative changes was compared between patients with and patients without a dens fracture. Results: An intraosseous cyst in the dens was found in 16.4% of the patients without a dens fracture and in 64.3% of those with a fracture (p < 0.001). The dens fracture extended through the existing cyst in twenty-four (66.7%) of thirty-six patients with a cyst and a dens fracture. Retro-dens synovitis was present in 4.2% of the patients without a dens fracture and 25.0% of those with a fracture (p < 0.001). After adjustment for age and sex, both cysts (odds ratio [OR] = 7.7, 95% confidence interval [CI] = 4.2 to 14.1) and synovitis (OR = 4.6, 95% CI = 2.1 to 10.0) were significantly associated with dens fracture. Conclusions: Intraosseous dens cysts and retro-dens synovitis were associated with dens fracture; those with a dens fracture were nearly eightfold more likely to have an intraosseous cyst and nearly fivefold more likely to have synovitis compared with those without a dens fracture. Because the atlanto-dens joint is a synovial joint, its degeneration can lead to subchondral cyst formation and synovitis and predispose affected individuals to fracture. Level of Evidence: Prognostic Level III. See Instructions for Authors for a complete description of levels of evidence.
Peer Review: This article was reviewed by the Editor-in-Chief and one Deputy Editor, and it underwent blinded review by two or more outside experts. The Deputy Editor reviewed each revision of the article, and it underwent a final review by the Editor-in-Chief prior to publication. Final corrections and clarifications occurred during one or more exchanges between the author(s) and copyeditors.
C
ervical spinal fractures are associated with a high rate of morbidity and mortality1-6. Of all cervical spine fractures, dens fractures are of particular interest because their prevalence is proportionally greater than that of other cervical vertebral fractures2,7,8, the dens has unique anatomy and
Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. One or more of the authors, or his or her institution, has had a financial relationship, in the thirty-six months prior to submission of this work, with an entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. No author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.
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functionality, and treatment strategies are quite different than those used for other cervical vertebral fractures. Dens fractures have a uniquely bimodal age distribution, affecting young active males and elderly males and females. In fact, the second cervical vertebra (C2) is the most commonly A commentary by Ronald W. Lindsey, MD, is linked to the online version of this article at jbjs.org.
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fractured cervical vertebra8 in elderly patients and has a high prevalence of associated mortality2,3,9,10. A recent report demonstrated that the rate of cervical vertebral fractures in the elderly population is increasing faster than the population growth11. Despite the prevalence of dens fractures and their increasing impact on the overall health of the aging population, there has been little research identifying anatomic risk factors, such as degenerative disease. Most of these fractures in elderly individuals occur as the result of low-energy trauma such as a ground-level fall; therefore, dens fractures are thought to be
A S S O C I AT I O N B E T W E E N A D VA N C E D D E G E N E R AT I V E C H A N G E S AT L A N T O - D E N S J O I N T A N D D E N S F R A C T U R E
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related to osteoporosis and balance issues associated with an older population2,4,9,10,12-15. Because the atlanto-dens joint is a synovial joint, its degeneration can lead to subchondral cyst formation and synovitis. We hypothesized that these degenerative changes weaken the dens and predispose it to fracture. Materials and Methods
T
his study was performed with institutional review board approval. We conducted a retrospective study of patients fifty-five years of age or older who had been admitted to our level-I trauma center from January 1, 2008, to December 31,
Fig. 1
Examples of the findings on the sagittal CT scans. Fig. 1-A Normal appearing dens. Fig. 1-B Joint space narrowing and osteophyte formation with no acute fracture. Fig. 1-C A cyst and type-II dens fracture. Fig. 1-D A cyst, synovitis, and type-II dens fracture. Synovitis was defined as a calcified or noncalcified soft-tissue mass posterior to the dens.
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TABLE I Associations of Age, Sex, Cysts, and Synovitis with Dens Fracture Status Among 792 Adults Ages Fifty-five to 103 Years Old No. (%) of Patients Characteristic
No Dens Fracture (N = 736)
With Dens Fracture (N = 56)
Unadjusted OR (95% CI)
Multivariable OR* (95% CI)
Age group 55-69 yr 70-79 yr ‡80 yr
385 (52.3) 140 (19.0) 211 (29.0)
22 (39.3) 9 (16.1) 25 (45.0)
1.0 (referent) 1.1 (0.5-2.5) 2.1 (1.1-3.8)
1.0 (referent) 0.8 (0.3-1.9) 1.0 (0.5-2.0)
Sex Male Female
398 (54.1) 338 (46.0)
22 (39.3) 34 (61.0)
1.0 (referent) 1.8 (1.0-3.2)
1.0 (referent) 1.7 (0.9-3.1)
No cysts
615 (84.0)
20 (36.0)
1.0 (referent)
1.0 (referent)
Cysts
121 (16.4)
36 (64.3)
9.2 (5.1-16.3)
7.7 (4.2-14.1)
No synovitis
705 (96.0)
42 (75.0)
1.0 (referent)
1.0 (referent)
31 (4.2)
14 (25.0)
7.6 (3.8-15.3)
4.6 (2.1-10.0)
Synovitis
*Adjusted for all variables in the table.
2011. As part of our routine protocol, a cervical computed tomography (CT) scan, in lieu of radiographs, was performed for all trauma patients. There were 1794 patients who met the study’s inclusion criteria; all of them were admitted under the trauma system, received a cervical CTscan, and were evaluated by a trauma team (Fig. 1). Of these, fifty-six had a dens fracture. From the remaining group of 1738 patients without a dens fracture, we selected 736 at random, using a random-number generator, as a comparison group. Patients who sustained a C2 fracture other than a dens fracture, such as pedicle or spinous process or inferior body fracture, were included as part of the comparison group. Age, sex, date of admission, type of fracture, and mechanism of injury were collected from electronic medical records. Degenerative changes, including intraosseous cyst formation, synovitis, and joint space narrowing, were recorded from the CT scans in an electronic database of radiographs. Degenerative changes were qualitatively assessed on both sagittal and coronal CT scans of the cervical spine (Fig. 1). An intraosseous cyst was diagnosed when there was a clear lytic defect within the dens. The senior author (J.U.Y.) estimated cyst size by measuring the diameter of the cyst at its midpoint on the sagittal image and recorded whether this diameter was greater than or less than 40% of the diameter of the dens at that location. Synovitis was diagnosed when a calcified or noncalcified soft-tissue mass was noted posterior to the dens and transverse ligament. Joint space narrowing was defined as an anterior atlanto-axial joint space of 94%) for each condition, so the lower kappa statistic observed for synovitis is likely due to its lower prevalence. Association of Age and Sex with Degenerative Changes In the sample of 736 patients without a dens fracture, 121 (16.4%) had an intraosseous cyst and thirty-one (4.2%) had synovitis (Table I). The prevalence of each condition increased with age, with the prevalence of intraosseous cysts increasing
Source of Funding There was no external funding for this study.
Results atient age ranged from fifty-five to 103 years. The study cohort included 420 men (53.0%), with an average age
P
Fig. 2
Prevalences of cysts and synovitis within age groups and according to sex in 736 adults with no dens fracture.
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Discussion dens fracture is associated with notable morbidity and mortality in elderly patients4,16,17. Not only are nonoperative treatments such as halo immobilization not well tolerated by the elderly, but the efficacy of these treatments is poor16-20. Moreover, there is a high rate of medical complications associated with surgical treatments in this population19,20. The lack of safe and effective treatment options and the increase in the incidence of fracture in elderly persons makes this an important public health issue. Despite the increasing incidence and detrimental health consequences in the elderly population, few reports describe anatomic risk factors, beyond osteoporosis and balance, for sustaining a dens fracture12-15. Although these factors may be important, our findings demonstrate that certain degenerative, morphologic changes to the atlanto-dens joint are also associated with the occurrence of dens fractures. Arthritis of the synovial joints is associated with joint space narrowing, subchondral cyst formation, and synovial hypertrophy. When we analyzed these conditions separately, joint space narrowing was not, by itself, associated with dens fracture. While joint space narrowing may contribute to the development of cysts, the narrowing itself did not contribute to the fracture risk. Lakshmanan et al.12 examined the effect of osteoporosis and joint space narrowing in twenty-three patients with a dens fracture and thirteen patients without a dens fracture. In this study with a small number of control patients without a dens fracture, they reported a significant (p < 0.05) effect of joint space narrowing on the prevalence of dens fracture. A larger sample of patients without a dens fracture may have resulted in a different finding. Their study also did not account for the presence of more important changes associated with degeneration, such as cyst formation. Our study clearly demonstrates that degenerative changes consisting of a subchondral cyst within the dens and synovitis surrounding the dens were associated with a dens fracture in this sample of trauma patients. Intraosseous cysts were nearly eightfold more common among those with a dens fracture, as compared with patients without such a fracture, and peri-dens synovitis was nearly fivefold more common. Our data suggest the possibility that cysts and synovitis together have an additive effect on the risk of a dens fracture. However, the number of patients with both a cyst and synovitis was small; thus, this comparison lacked statistical power for multivariable analysis. Surprisingly, cyst size in the sagittal plane on the CT scan did not appear to have an important impact on dens fracture prevalence. As most dens fractures occur with sagittal head motion, we thought that the size of the cyst in the sagittal plane would be the more relevant measurement. However, other factors such as the location of the cyst and direction of the trauma force may play an important role. Because of the small number of patients in our study, we could not analyze the extent to which these factors had an effect. In a literature review, we found case reports of intraosseous cysts in the cervical spine below the level of C2, usually associated with facet joints21-23. Finn et al.24 described
A
Fig. 3
Prevalences of cysts, synovitis, and joint space narrowing in adults with a dens fracture and those with no dens fracture.
from 11.2% in the youngest group (fifty-five to sixty-nine-years old) to 24.6% in the oldest group (eighty years of age or older) (p < 0.0001) and the prevalence of synovitis increasing from 1.5% to 9.5% (p < 0.0001) (Fig. 2). Neither the prevalence of intraosseous cysts (p = 0.28) nor the synovitis prevalence (p = 0.31) differed between sexes (Fig. 2). Association of Dens Fracture with Degenerative Changes Of the fifty-six patients with a dens fracture, forty (71.4%) sustained the injury as a result of a ground-level fall. Forty-six patients (82.1%) had a type-II dens fracture1 and ten (17.9%), type III. Thirty-six (64.3%) of the fifty-six patients with a dens fracture had an intraosseous dens cyst, a percentage that was a significantly greater (p < 0.0001) than that in the group without a dens fracture (16.4%) (Table I). Retro-dens synovitis was present in fourteen patients (25.0%) with a dens fracture compared with thirty-one (4.2%) without a dens fracture (p < 0.0001). Anterior atlanto-dens interval narrowing was present in twenty-eight patients (50.0%) with a dens fracture compared with 330 (44.8%) without a dens fracture (p > 0.05). In unadjusted analyses, patients with a dens fracture were more likely to be eighty years of age or older and female and to have an intraosseous cyst or synovitis compared with those in the random sample of patients without a dens fracture (Table I). In the multivariable analysis with all four variables in the model, those with a dens fracture were nearly eightfold more likely to have an intraosseous cyst and nearly fivefold more likely to have synovitis compared with those without a dens fracture (Fig. 3, Table I). Twenty-two (18.2%) of 121 cysts in patients without a dens fracture and twelve (33.3%) of thirty-six cysts in patients with a dens fracture measured >40% of the dens width (p > 0.05). The dens fracture extended through the existing cyst in twenty-four (66.7%) of the thirty-six patients with a cyst and a dens fracture. Of those with a dens fracture, ten (17.9%) had both a cyst and synovitis compared with twelve (1.6%) of those without a dens fracture (p < 0.0001).
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both cysts and pannus at C1 and C2, mostly around the facet joints but a few around the atlanto-dens joint as well. The authors did not describe fractures associated with these changes but rather described the changes as a source of pain. The actual rate of cyst formation in the dens is not known, but our study revealed that 19.8% (157) of 792 patients fifty-five years of age or older had this condition. It is generally thought that intraosseous bone cysts substantially affect osseous stability21,25. The importance of cysts on dens fracture risk is underscored by the fact that 66.7% of our patients sustained the fracture through a cyst. Prophylactic treatment with screw fixation of the dens may be considered for elderly patients with a high risk for falls as well as a large cyst, but the effectiveness of such treatment is unknown. Research is needed to evaluate the potential effectiveness of prophylactic treatments for cysts in preventing dens fracture in populations at risk for this type of fracture. Pseudogout leading to inflammation and synovitis has also been described at the atlanto-dens joint26-28. Many of our patients had calcified changes of soft tissue surrounding the dens suggestive of calcium pyrophosphate deposition disease, or pseudogout. However, we did not perform a biopsy in any of these patients to determine if pseudogout was present. We are not aware of any previous report of the association between these soft-tissue calcifications and dens fracture. However, synovial inflammation leading to calcification, as occurs in pseudogout, is a possible pathophysiologic mechanism of dens weakening and an increase in the risk of dens fracture. In this study, we defined synovitis as the presence of softtissue calcification or a clear soft-tissue mass extending beyond the dens and the transverse ligament. One limitation of our study is that the sample was drawn from a trauma population. It is unknown if the prevalence of cysts and synovitis in the comparison group is representative of the prevalence of these
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degenerative elements in a general population of adults fiftyfive years of age and older. Epidemiologic studies with cervical spine imaging are needed to address this issue. Another limitation is that we utilized CT scans, which potentially underestimate the presence of the synovitis. In many synovial joints, synovitis has been associated with juxta-articular osteopenia and weakening of the subchondral bone. Given the study’s limitations, we cannot suggest an increased prevalence of fracture attributable to osteopenia related to synovitis; however, we believe that this study demonstrates a strong association between the presence of synovitis and an increased prevalence of dens fracture. The literature suggests that the factors contributing to a dens fracture are osteoporosis and associated diagnoses related to aging. Our results suggest that, when accounting for the increased development of cysts and synovitis, the presence of a dens fracture no longer varies by age. We believe that dens fractures in the elderly are an important health issue whose frequency is underappreciated. Additional studies aimed at understanding factors contributing to dens cyst formation and synovitis could help to prevent this devastating injury. n NOTE: The authors thank Marie Kane, MS, and Sabina Blizzard, BA, for editorial assistance.
Matthew S. Shinseki Natalie L. Zusman, BS Jayme Hiratzka, MD Lynn M. Marshall, ScD Jung U. Yoo, MD Department of Orthopaedics and Rehabilitation, Oregon Health & Science University, 3181 S.W. Sam Jackson Park Road, OP 31, Portland, OR 97239. E-mail address for J.U. Yoo: [email protected]
References 1. Anderson LD, D’Alonzo RT. Fractures of the odontoid process of the axis. J Bone Joint Surg Am. 1974 Dec;56(8):1663-74. 2. Lomoschitz FM, Blackmore CC, Mirza SK, Mann FA. Cervical spine injuries in patients 65 years old and older: epidemiologic analysis regarding the effects of age and injury mechanism on distribution, type, and stability of injuries. AJR Am J Roentgenol. 2002 Mar;178(3):573-7. 3. Levi AD, Hurlbert RJ, Anderson P, Fehlings M, Rampersaud R, Massicotte EM, France JC, Le Huec JC, Hedlund R, Arnold P. Neurologic deterioration secondary to unrecognized spinal instability following trauma—a multicenter study. Spine (Phila Pa 1976). 2006 Feb 15;31(4):451-8. 4. Malik SA, Murphy M, Connolly P, O’Byrne J. Evaluation of morbidity, mortality and outcome following cervical spine injuries in elderly patients. Eur Spine J. 2008 Apr;17(4):585-91. Epub 2008 Jan 15. 5. Vanderlan WB, Tew BE, Seguin CY, Mata MM, Yang JJ, Horst HM, Obeid FN, McSwain NE. Neurologic sequelae of penetrating cervical trauma. Spine (Phila Pa 1976). 2009 Nov 15;34(24):2646-53. 6. O’Malley KF, Ross SE. The incidence of injury to the cervical spine in patients with craniocerebral injury. J Trauma. 1988 Oct;28(10):1476-8. 7. Smith HE, Kerr SM, Fehlings MG, Chapman J, Maltenfort M, Zavlasky J, Harris E, Albert TJ, Harrop J, Hilibrand AS, Anderson DG, Vaccaro AR. Trends in epidemiology and management of type II odontoid fractures: 20-year experience at a model system spine injury tertiary referral center. J Spinal Disord Tech. 2010 Dec;23(8):501-5. 8. Ryan MD, Henderson JJ. The epidemiology of fractures and fracture-dislocations of the cervical spine. Injury. 1992;23(1):38-40. 9. Ngo B, Hoffman JR, Mower WR. Cervical spine injury in the very elderly. Emerg Radiol. 2000;7:287-91.
10. M¨uller EJ, Wick M, Russe O, Muhr G. Management of odontoid fractures in the elderly. Eur Spine J. 1999;8(5):360-5. 11. Zusman NL, Ching AC, Hart RA, Yoo JU. Incidence of second cervical vertebral fractures far surpassed the rate predicted by the changing age distribution and growth among elderly United States’ persons (2005-2008). Spine (Phila Pa 1976). 2012 Nov 2. Epub 2012 Nov 2. 12. Lakshmanan P, Jones A, Howes J, Lyons K. CT evaluation of the pattern of odontoid fractures in the elderly—relationship to upper cervical spine osteoarthritis. Eur Spine J. 2005 Feb;14(1):78-83. Epub 2004 Jun 15. 13. Watanabe M, Sakai D, Yamamoto Y, Sato M, Mochida J. Upper cervical spine injuries: age-specific clinical features. J Orthop Sci. 2010 Jul;15(4):485-92. Epub 2010 Aug 19. 14. Amling M, Hahn M, Wening VJ, Grote HJ, Delling G. The microarchitecture of the axis as the predisposing factor for fracture of the base of the odontoid process. A histomorphometric analysis of twenty-two autopsy specimens. J Bone Joint Surg Am. 1994 Dec;76(12):1840-6. 15. Amling M, P¨osl M, Wening VJ, Ritzel H, Hahn M, Delling G. Structural heterogeneity within the axis: the main cause in the etiology of dens fractures. A histomorphometric analysis of 37 normal and osteoporotic autopsy cases. J Neurosurg. 1995 Aug;83(2):330-5. 16. Dailey AT, Hart D, Finn MA, Schmidt MH, Apfelbaum RI. Anterior fixation of odontoid fractures in an elderly population. J Neurosurg Spine. 2010 Jan;12(1): 1-8. 17. Harrop JS, Przybylski GJ, Vaccaro AR, Yalamanchili K. Efficacy of anterior odontoid screw fixation in elderly patients with Type II odontoid fractures. Neurosurg Focus. 2000;8(6):e6. Epub 2000 Jun 15.
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18. Campbell PG, Malone J, Yadla S, Maltenfort MG, Harrop JS, Sharan AD, Ratliff JK. Early complications related to approach in thoracic and lumbar spine surgery: a single center prospective study. World Neurosurg. 2010 Apr;73(4):395-401. 19. Longo UG, Denaro L, Campi S, Maffulli N, Denaro V. Upper cervical spine injuries: indications and limits of the conservative management in Halo vest. A systematic review of efficacy and safety. Injury. 2010 Nov;41(11): 1127-35. 20. Mayer M, Zenner J, Auffarth A, Atzwanger J, Romeder F, Hitzl W, Lederer S, Resch H, Koller H. Efficacy of anterior odontoid screw fixation in the elderly patient: a CT-based biometrical analysis of odontoid fractures. Eur Spine J. 2011 Sep;20(9): 1441-9. Epub 2011 May 24. 21. Jost SC, Hsien Tu P, Wright NM. Symptomatic intraosseous synovial cyst in the cervical spine: a case report. Spine (Phila Pa 1976). 2003 Sep 1;28(17): E344-6. 22. Costa F, Menghetti C, Cardia A, Fornari M, Ortolina A. Cervical synovial cyst: case report and review of literature. Eur Spine J. 2010 Jul;19(Suppl 2):S100-2. Epub 2009 Jul 15.
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23. Lyons MK, Birch BD, Krauss WE, Patel NP, Nottmeier EW, Boucher OK. Subaxial cervical synovial cysts: report of 35 histologically confirmed surgically treated cases and review of the literature. Spine (Phila Pa 1976). 2011 Sep 15;36(20):E1285-9. 24. Finn M, Fassett DR, Apfelbaum RI. Surgical treatment of nonrheumatoid atlantoaxial degenerative arthritis producing pain and myelopathy. Spine (Phila Pa 1976). 2007 Dec 15;32(26):3067-73. 25. Leclet H, Adamsbaum C. Intraosseous cyst injection. Radiol Clin North Am. 1998 May;36(3):581-7. 26. Unlu Z, Tarhan S, Ozmen EM. An idiopathic case of calcium pyrophosphate dihydrate crystal deposition disease with crowned dens syndrome in a young patient. South Med J. 2009 Sep;102(9):949-51. 27. Ozolek JA, Chu CT. Pseudogout of the craniocervical junction. Arch Pathol Lab Med. 2003 Jul;127(7):895. 28. Kakitsubata Y, Boutin RD, Theodorou DJ, Kerr RM, Steinbach LS, Chan KK, Pathria MN, Haghighi P, Resnick D. Calcium pyrophosphate dihydrate crystal deposition in and around the atlantoaxial joint: association with type 2 odontoid fractures in nine patients. Radiology. 2000 Jul;216(1):213-9.
BY
T HE J OURNAL
OF
B ONE
AND J OINT
S URGERY, I NCORPORATED
Association Between Advanced Degenerative Changes of the Atlanto-Dens Joint and Presence of Dens Fracture Matthew S. Shinseki, Natalie L. Zusman, BS, Jayme Hiratzka, MD, Lynn M. Marshall, ScD, and Jung U. Yoo, MD Investigation performed at the Department of Orthopaedics and Rehabilitation, Oregon Health & Science University, Portland, Oregon
Background: Dens fractures in elderly patients are often related to issues associated with aging. We examined the association between degenerative changes of the atlanto-dens joint and the risk of dens fracture. Methods: We conducted a retrospective study of trauma patients, fifty-five years of age or older, who had undergone a computed tomography scan of the cervical spine as part of their admission to a single level-I trauma center. There were 1794 patients who met the inclusion criteria; scans were evaluated for all fifty-six who presented with a dens fracture and for a random sample of 736 without a dens fracture. Intraosseous cyst formation, synovitis, and joint space narrowing were recorded from the scans. The prevalence of degenerative changes was compared between patients with and patients without a dens fracture. Results: An intraosseous cyst in the dens was found in 16.4% of the patients without a dens fracture and in 64.3% of those with a fracture (p < 0.001). The dens fracture extended through the existing cyst in twenty-four (66.7%) of thirty-six patients with a cyst and a dens fracture. Retro-dens synovitis was present in 4.2% of the patients without a dens fracture and 25.0% of those with a fracture (p < 0.001). After adjustment for age and sex, both cysts (odds ratio [OR] = 7.7, 95% confidence interval [CI] = 4.2 to 14.1) and synovitis (OR = 4.6, 95% CI = 2.1 to 10.0) were significantly associated with dens fracture. Conclusions: Intraosseous dens cysts and retro-dens synovitis were associated with dens fracture; those with a dens fracture were nearly eightfold more likely to have an intraosseous cyst and nearly fivefold more likely to have synovitis compared with those without a dens fracture. Because the atlanto-dens joint is a synovial joint, its degeneration can lead to subchondral cyst formation and synovitis and predispose affected individuals to fracture. Level of Evidence: Prognostic Level III. See Instructions for Authors for a complete description of levels of evidence.
Peer Review: This article was reviewed by the Editor-in-Chief and one Deputy Editor, and it underwent blinded review by two or more outside experts. The Deputy Editor reviewed each revision of the article, and it underwent a final review by the Editor-in-Chief prior to publication. Final corrections and clarifications occurred during one or more exchanges between the author(s) and copyeditors.
C
ervical spinal fractures are associated with a high rate of morbidity and mortality1-6. Of all cervical spine fractures, dens fractures are of particular interest because their prevalence is proportionally greater than that of other cervical vertebral fractures2,7,8, the dens has unique anatomy and
Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. One or more of the authors, or his or her institution, has had a financial relationship, in the thirty-six months prior to submission of this work, with an entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. No author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.
J Bone Joint Surg Am. 2014;96:712-7
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http://dx.doi.org/10.2106/JBJS.M.00814
functionality, and treatment strategies are quite different than those used for other cervical vertebral fractures. Dens fractures have a uniquely bimodal age distribution, affecting young active males and elderly males and females. In fact, the second cervical vertebra (C2) is the most commonly A commentary by Ronald W. Lindsey, MD, is linked to the online version of this article at jbjs.org.
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fractured cervical vertebra8 in elderly patients and has a high prevalence of associated mortality2,3,9,10. A recent report demonstrated that the rate of cervical vertebral fractures in the elderly population is increasing faster than the population growth11. Despite the prevalence of dens fractures and their increasing impact on the overall health of the aging population, there has been little research identifying anatomic risk factors, such as degenerative disease. Most of these fractures in elderly individuals occur as the result of low-energy trauma such as a ground-level fall; therefore, dens fractures are thought to be
A S S O C I AT I O N B E T W E E N A D VA N C E D D E G E N E R AT I V E C H A N G E S AT L A N T O - D E N S J O I N T A N D D E N S F R A C T U R E
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related to osteoporosis and balance issues associated with an older population2,4,9,10,12-15. Because the atlanto-dens joint is a synovial joint, its degeneration can lead to subchondral cyst formation and synovitis. We hypothesized that these degenerative changes weaken the dens and predispose it to fracture. Materials and Methods
T
his study was performed with institutional review board approval. We conducted a retrospective study of patients fifty-five years of age or older who had been admitted to our level-I trauma center from January 1, 2008, to December 31,
Fig. 1
Examples of the findings on the sagittal CT scans. Fig. 1-A Normal appearing dens. Fig. 1-B Joint space narrowing and osteophyte formation with no acute fracture. Fig. 1-C A cyst and type-II dens fracture. Fig. 1-D A cyst, synovitis, and type-II dens fracture. Synovitis was defined as a calcified or noncalcified soft-tissue mass posterior to the dens.
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TABLE I Associations of Age, Sex, Cysts, and Synovitis with Dens Fracture Status Among 792 Adults Ages Fifty-five to 103 Years Old No. (%) of Patients Characteristic
No Dens Fracture (N = 736)
With Dens Fracture (N = 56)
Unadjusted OR (95% CI)
Multivariable OR* (95% CI)
Age group 55-69 yr 70-79 yr ‡80 yr
385 (52.3) 140 (19.0) 211 (29.0)
22 (39.3) 9 (16.1) 25 (45.0)
1.0 (referent) 1.1 (0.5-2.5) 2.1 (1.1-3.8)
1.0 (referent) 0.8 (0.3-1.9) 1.0 (0.5-2.0)
Sex Male Female
398 (54.1) 338 (46.0)
22 (39.3) 34 (61.0)
1.0 (referent) 1.8 (1.0-3.2)
1.0 (referent) 1.7 (0.9-3.1)
No cysts
615 (84.0)
20 (36.0)
1.0 (referent)
1.0 (referent)
Cysts
121 (16.4)
36 (64.3)
9.2 (5.1-16.3)
7.7 (4.2-14.1)
No synovitis
705 (96.0)
42 (75.0)
1.0 (referent)
1.0 (referent)
31 (4.2)
14 (25.0)
7.6 (3.8-15.3)
4.6 (2.1-10.0)
Synovitis
*Adjusted for all variables in the table.
2011. As part of our routine protocol, a cervical computed tomography (CT) scan, in lieu of radiographs, was performed for all trauma patients. There were 1794 patients who met the study’s inclusion criteria; all of them were admitted under the trauma system, received a cervical CTscan, and were evaluated by a trauma team (Fig. 1). Of these, fifty-six had a dens fracture. From the remaining group of 1738 patients without a dens fracture, we selected 736 at random, using a random-number generator, as a comparison group. Patients who sustained a C2 fracture other than a dens fracture, such as pedicle or spinous process or inferior body fracture, were included as part of the comparison group. Age, sex, date of admission, type of fracture, and mechanism of injury were collected from electronic medical records. Degenerative changes, including intraosseous cyst formation, synovitis, and joint space narrowing, were recorded from the CT scans in an electronic database of radiographs. Degenerative changes were qualitatively assessed on both sagittal and coronal CT scans of the cervical spine (Fig. 1). An intraosseous cyst was diagnosed when there was a clear lytic defect within the dens. The senior author (J.U.Y.) estimated cyst size by measuring the diameter of the cyst at its midpoint on the sagittal image and recorded whether this diameter was greater than or less than 40% of the diameter of the dens at that location. Synovitis was diagnosed when a calcified or noncalcified soft-tissue mass was noted posterior to the dens and transverse ligament. Joint space narrowing was defined as an anterior atlanto-axial joint space of 94%) for each condition, so the lower kappa statistic observed for synovitis is likely due to its lower prevalence. Association of Age and Sex with Degenerative Changes In the sample of 736 patients without a dens fracture, 121 (16.4%) had an intraosseous cyst and thirty-one (4.2%) had synovitis (Table I). The prevalence of each condition increased with age, with the prevalence of intraosseous cysts increasing
Source of Funding There was no external funding for this study.
Results atient age ranged from fifty-five to 103 years. The study cohort included 420 men (53.0%), with an average age
P
Fig. 2
Prevalences of cysts and synovitis within age groups and according to sex in 736 adults with no dens fracture.
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Discussion dens fracture is associated with notable morbidity and mortality in elderly patients4,16,17. Not only are nonoperative treatments such as halo immobilization not well tolerated by the elderly, but the efficacy of these treatments is poor16-20. Moreover, there is a high rate of medical complications associated with surgical treatments in this population19,20. The lack of safe and effective treatment options and the increase in the incidence of fracture in elderly persons makes this an important public health issue. Despite the increasing incidence and detrimental health consequences in the elderly population, few reports describe anatomic risk factors, beyond osteoporosis and balance, for sustaining a dens fracture12-15. Although these factors may be important, our findings demonstrate that certain degenerative, morphologic changes to the atlanto-dens joint are also associated with the occurrence of dens fractures. Arthritis of the synovial joints is associated with joint space narrowing, subchondral cyst formation, and synovial hypertrophy. When we analyzed these conditions separately, joint space narrowing was not, by itself, associated with dens fracture. While joint space narrowing may contribute to the development of cysts, the narrowing itself did not contribute to the fracture risk. Lakshmanan et al.12 examined the effect of osteoporosis and joint space narrowing in twenty-three patients with a dens fracture and thirteen patients without a dens fracture. In this study with a small number of control patients without a dens fracture, they reported a significant (p < 0.05) effect of joint space narrowing on the prevalence of dens fracture. A larger sample of patients without a dens fracture may have resulted in a different finding. Their study also did not account for the presence of more important changes associated with degeneration, such as cyst formation. Our study clearly demonstrates that degenerative changes consisting of a subchondral cyst within the dens and synovitis surrounding the dens were associated with a dens fracture in this sample of trauma patients. Intraosseous cysts were nearly eightfold more common among those with a dens fracture, as compared with patients without such a fracture, and peri-dens synovitis was nearly fivefold more common. Our data suggest the possibility that cysts and synovitis together have an additive effect on the risk of a dens fracture. However, the number of patients with both a cyst and synovitis was small; thus, this comparison lacked statistical power for multivariable analysis. Surprisingly, cyst size in the sagittal plane on the CT scan did not appear to have an important impact on dens fracture prevalence. As most dens fractures occur with sagittal head motion, we thought that the size of the cyst in the sagittal plane would be the more relevant measurement. However, other factors such as the location of the cyst and direction of the trauma force may play an important role. Because of the small number of patients in our study, we could not analyze the extent to which these factors had an effect. In a literature review, we found case reports of intraosseous cysts in the cervical spine below the level of C2, usually associated with facet joints21-23. Finn et al.24 described
A
Fig. 3
Prevalences of cysts, synovitis, and joint space narrowing in adults with a dens fracture and those with no dens fracture.
from 11.2% in the youngest group (fifty-five to sixty-nine-years old) to 24.6% in the oldest group (eighty years of age or older) (p < 0.0001) and the prevalence of synovitis increasing from 1.5% to 9.5% (p < 0.0001) (Fig. 2). Neither the prevalence of intraosseous cysts (p = 0.28) nor the synovitis prevalence (p = 0.31) differed between sexes (Fig. 2). Association of Dens Fracture with Degenerative Changes Of the fifty-six patients with a dens fracture, forty (71.4%) sustained the injury as a result of a ground-level fall. Forty-six patients (82.1%) had a type-II dens fracture1 and ten (17.9%), type III. Thirty-six (64.3%) of the fifty-six patients with a dens fracture had an intraosseous dens cyst, a percentage that was a significantly greater (p < 0.0001) than that in the group without a dens fracture (16.4%) (Table I). Retro-dens synovitis was present in fourteen patients (25.0%) with a dens fracture compared with thirty-one (4.2%) without a dens fracture (p < 0.0001). Anterior atlanto-dens interval narrowing was present in twenty-eight patients (50.0%) with a dens fracture compared with 330 (44.8%) without a dens fracture (p > 0.05). In unadjusted analyses, patients with a dens fracture were more likely to be eighty years of age or older and female and to have an intraosseous cyst or synovitis compared with those in the random sample of patients without a dens fracture (Table I). In the multivariable analysis with all four variables in the model, those with a dens fracture were nearly eightfold more likely to have an intraosseous cyst and nearly fivefold more likely to have synovitis compared with those without a dens fracture (Fig. 3, Table I). Twenty-two (18.2%) of 121 cysts in patients without a dens fracture and twelve (33.3%) of thirty-six cysts in patients with a dens fracture measured >40% of the dens width (p > 0.05). The dens fracture extended through the existing cyst in twenty-four (66.7%) of the thirty-six patients with a cyst and a dens fracture. Of those with a dens fracture, ten (17.9%) had both a cyst and synovitis compared with twelve (1.6%) of those without a dens fracture (p < 0.0001).
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both cysts and pannus at C1 and C2, mostly around the facet joints but a few around the atlanto-dens joint as well. The authors did not describe fractures associated with these changes but rather described the changes as a source of pain. The actual rate of cyst formation in the dens is not known, but our study revealed that 19.8% (157) of 792 patients fifty-five years of age or older had this condition. It is generally thought that intraosseous bone cysts substantially affect osseous stability21,25. The importance of cysts on dens fracture risk is underscored by the fact that 66.7% of our patients sustained the fracture through a cyst. Prophylactic treatment with screw fixation of the dens may be considered for elderly patients with a high risk for falls as well as a large cyst, but the effectiveness of such treatment is unknown. Research is needed to evaluate the potential effectiveness of prophylactic treatments for cysts in preventing dens fracture in populations at risk for this type of fracture. Pseudogout leading to inflammation and synovitis has also been described at the atlanto-dens joint26-28. Many of our patients had calcified changes of soft tissue surrounding the dens suggestive of calcium pyrophosphate deposition disease, or pseudogout. However, we did not perform a biopsy in any of these patients to determine if pseudogout was present. We are not aware of any previous report of the association between these soft-tissue calcifications and dens fracture. However, synovial inflammation leading to calcification, as occurs in pseudogout, is a possible pathophysiologic mechanism of dens weakening and an increase in the risk of dens fracture. In this study, we defined synovitis as the presence of softtissue calcification or a clear soft-tissue mass extending beyond the dens and the transverse ligament. One limitation of our study is that the sample was drawn from a trauma population. It is unknown if the prevalence of cysts and synovitis in the comparison group is representative of the prevalence of these
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degenerative elements in a general population of adults fiftyfive years of age and older. Epidemiologic studies with cervical spine imaging are needed to address this issue. Another limitation is that we utilized CT scans, which potentially underestimate the presence of the synovitis. In many synovial joints, synovitis has been associated with juxta-articular osteopenia and weakening of the subchondral bone. Given the study’s limitations, we cannot suggest an increased prevalence of fracture attributable to osteopenia related to synovitis; however, we believe that this study demonstrates a strong association between the presence of synovitis and an increased prevalence of dens fracture. The literature suggests that the factors contributing to a dens fracture are osteoporosis and associated diagnoses related to aging. Our results suggest that, when accounting for the increased development of cysts and synovitis, the presence of a dens fracture no longer varies by age. We believe that dens fractures in the elderly are an important health issue whose frequency is underappreciated. Additional studies aimed at understanding factors contributing to dens cyst formation and synovitis could help to prevent this devastating injury. n NOTE: The authors thank Marie Kane, MS, and Sabina Blizzard, BA, for editorial assistance.
Matthew S. Shinseki Natalie L. Zusman, BS Jayme Hiratzka, MD Lynn M. Marshall, ScD Jung U. Yoo, MD Department of Orthopaedics and Rehabilitation, Oregon Health & Science University, 3181 S.W. Sam Jackson Park Road, OP 31, Portland, OR 97239. E-mail address for J.U. Yoo: [email protected]
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