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Analysis of predisposing factors in elderly people with Type II odontoid fracture
The Spine Journal
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(2013)
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Clinical Study
Analysis of predisposing factors in elderly people with Type II odontoid fracture Masahiko Watanabe, MD, PhD*, Daisuke Sakai, MD, PhD, Yukihiro Yamamoto, MD, PhD, Toshihiro Nagai, MD, PhD, Masato Sato, MD, PhD, Joji Mochida, MD, PhD Department of Orthopaedic Surgery, Surgical Science, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa 259-1193, Japan Received 30 January 2012; revised 29 May 2013; accepted 10 July 2013
Abstract
BACKGROUND CONTEXT: Type II odontoid fracture is the most frequent individual fracture in elderly people. An older person usually sustains a Type II odontoid fracture in a fall from standing or a seated height. A relationship between osteoarthritis in the upper cervical spine and Type II odontoid fracture has been reported. However, to our knowledge, few reports have investigated statistically whether disproportionate degeneration between joints influences the susceptibility to fracture. PURPOSE: The purpose of this study was to assess predisposition to Type II odontoid fracture in the elderly. STUDY DESIGN: Retrospective review of elderly patients sustained Type II odontoid fracture and other axis fractures. PATIENT SAMPLE: Thirty-eight patients aged 65 years and older with axis fractures. OUTCOME MEASURES: Evaluation of computed tomography findings by focusing on osteoporosis and the disproportion in degeneration between each of the upper cervical joints (atlantooccipital, atlantoodontoid, and lateral atlantoaxial joints). METHODS: Seventeen patients had a Type II odontoid fracture, and 21 patients had other axis fractures. Using the computed tomography findings, we classified osteoporosis at the dens-body junction and the severity of degenerative changes in the atlantoodontoid, atlantooccipital, and lateral atlantoaxial joints as none, mild, moderate, or severe. The proportion of patients with moderate or severe osteoporosis and degenerative changes in each joint and that of patients with disproportionate degenerative changes between joints (difference in grade of $2 levels between joints) were compared statistically. The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this article. RESULTS: Patients with osteoporosis and with disproportionate degenerative changes between the atlantoodontoid and lateral atlantoaxial joints were significantly more likely to have a Type II odontoid fracture than other axis fractures. These two factors were also assessed in multivariate logistic analysis. The disproportionate degenerative change between the atlantoodontoid and lateral atlantoaxial joint remained significant, even after adjusting for osteoporosis. CONCLUSIONS: Older patients with the dens fixed to the atlas because of degeneration of the atlantoodontoid joint and a smooth lateral atlantoaxial joint seem to sustain Type II odontoid fractures because, during a simple fall, the rotation of the head produces torque force on the osteoporotic dens-body junction, which acts as the rotatory center. The presence of the disproportionate osteoarthritic degeneration between the atlantoodontoid and lateral atlantoaxial joints predisposes older people to a Type II odontoid fracture. Ó 2013 Elsevier Inc. All rights reserved.
Keywords:
Upper cervical spine injury; Elderly; Osteoarthritis; Degenerative change; Type II odontoid fracture
FDA device/drug status: Not applicable. Author disclosures: MW: Nothing to disclose. DS: Nothing to disclose. YY: Nothing to disclose. TN: Nothing to disclose. MS: Nothing to disclose. JM: Nothing to disclose. 1529-9430/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.spinee.2013.07.434
* Corresponding author. Department of Orthopaedic Surgery, Surgical Science, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa 259-1193, Japan. Tel.: (81) 463-93-1121x2320; fax: (81) 46396-4404. E-mail address: [email protected] (M. Watanabe)
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M. Watanabe et al. / The Spine Journal
Introduction Data from different parts of the world show a trend toward decreasing neck injury incidence for age groups !65 years, whereas the incidence has remained constant or has increased in people aged 65 years and older [1–3]. In young adults, most trauma causing cervical spine injury involves high-energy injury, such as traffic accidents and falls from a high place. By contrast, in older people, cervical spine injuries are more likely to be caused by a lowenergy injury such as a fall from standing or a seated height [4–11]. In young people, the middle and lower cervical spine is more prone to injury, but in older people, the upper cervical spine is more likely to be injured [7,8,10]. Daffner et al. [12] reported that upper cervical lesions accounted for 68.9% of all cervical injuries in the elderly and 35.8% in young people. Although the middle and lower cervical spine is the most mobile portion in young people, age-related degeneration makes the middle and lower cervical spine stiffer. The accompanying shift of the motion segment to the upper cervical spine is responsible for the increased frequency of upper cervical spine injury in the elderly compared with the middle and lower cervical spine [4,7,9]. We have reported on the aging-related clinical features of upper cervical spine injury [13]. Type II odontoid fracture classified by Anderson and D’Alonso [14] is the most frequent individual fracture in the elderly [4,7–11,13–15]. Lakshmanan et al. [16] reported a significant relationship between upper cervical osteoarthritis and the incidence of Type II odontoid fracture. Severe degenerative changes in the atlantoodontoid joint develop with aging and fix the odontoid to the anterior arch of the atlas. By contrast, the lateral atlantoaxial joint is less affected by osteoarthritis. Low-energy trauma induces forced atlantoaxial rotation, which along with marked limitation of movement at the atlantoodontoid joint can produce a torque force at the base of the osteoporotic odontoid process. However, to our knowledge, few studies have investigated statistically the relationship of Type II odontoid fracture with osteoporosis and with the disproportional degeneration of these joints. The aim of this study was to examine the predisposition in older people toward Type II odontoid fracture compared with other axis fractures, using univariate and multivariate analyses. We focused on osteoporosis and disproportional degenerative changes in adjacent joints of the upper cervical spine and studied their relationship with fracture risk.
Materials and methods Our series included 38 patients aged $65 years who sustained a fracture of the axis between February 2001 and June 2011. Seventeen patients had a Type II odontoid fracture, and 21 patients had other axis fracture types. Other axis fractures included 15 cases of traumatic spondylolisthesis (including three cases of combined hyperextension
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teardrop fracture and one case of combined Type III odontoid fracture), three body fractures, two hyperextension teardrop fractures, and one Type III odontoid fracture. In this study, we compared Type II odontoid fractures with other axis fractures. Data on the injury etiology, neurologic deficit, and complicated injury were obtained from clinical records. We classified osteoporosis at the dens-body junction as none (normal trabecular pattern with normal cortical thickness), mild (decrease in the amount of trabeculae with no areas of absent trabeculae [holes] and normal cortical thickness), moderate (absent trabeculae [holes] involving !50% of the transverse diameter of the bone with cortical thinning), or severe (absent trabeculae [holes] involving O50% of the transverse diameter of the bone with cortical thinning). The severity of degenerative changes in the atlantoodontoid joint was classified as none (normal joint space with no osteophytes), mild (narrowed joint space or normal joint space with osteophyte formation), moderate (obliterated joint space with or without osteophyte formation), or severe (ankylosis of the joint with either excrescences in the joint or transverse ligament calcification, or both). The severity of degenerative changes in the atlantooccipital and lateral atlantoaxial joints was classified similarly as none, mild, moderate, but with some modification in severe (completely obliterated joint space with osteophyte excrescences and/or fusion of the joint). The classifications involving the osteoporosis at the dens-body junction and the degenerative joint changes were made from computed tomography (CT) images according to the method described by Lakshmanan et al. [16] Two reviewers reviewed each CT image in a blinded manner and discussed their findings to arrive at consensus in the case of different views. The data were analysed using PASW Statistics 18 (SPSS Japan Inc., an IBM company, Japan). We categorized a fall from standing or a seated height as a low-energy injury and other falls as a high-energy injury. Chi-square tests were used to compare the patients who sustained a Type II odontoid fracture with those who sustained other axis fractures. Differences in the proportion of patients between the two groups were compared for the following variables: moderate and severe degenerative changes in the atlantoodontoid joint, atlantooccipital joint, and lateral atlantoaxial joint; moderate and severe in the osteoporosis of the axis vertebra; and disproportion in degenerative changes between each joint, defined as a difference in grade of $2 levels between joints. To assess the predisposition to Type II odontoid fractures, multivariate logistic analysis was performed on factors in which a significant difference was detected using Chi-square tests because the number of Type II odontoid fractures was limited. The final model was checked for goodness of fit with the Hosmer and Lemeshow test and by colinearity and residual diagnostics, to ensure they were well specified and fit. Significance was set at p!.05.
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Table 1 Clinical data Severity of degenerative change No. Type II 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Other 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
Age
Sex
Type of fracture
Complicated upper cervical injury
89 87 86 86 83 82 81 80 78 78 77 71 70 67 67 65 66
F F M F M F M F M F F F M F F M F
Type Type Type Type Type Type Type Type Type Type Type Type Type Type Type Type Type
Post arch
85 85 85 81 80 79 79 78 76 76 73 71 71 71 70 70 69 69 68 68 65
M M M M M M M M F M M F M F F F M M F M M
T.S. T.S. T.S. T.S. T.S. T.S. ETF T.S. Type III ETF T.S. T.S. Body fracture Body fracture T.S. Body fracture T.S. T.S. T.S. T.S. T.S.
II II II II II II II II II II II II II II II II II
Jeffeson
Type III ETF
ETF
Anterior arch
ETF
Etiology
Atlantoodontoid joint
Atlantooccipital joint
Lateral atlantoaxial joint
S.F. H.F. S.F. S.F. S.F. H.F. S.F. Neck hanging H.F. H.F. S.F. H.F. H.F. H.F. S.F. H.F. T.A.
Severe Moderate Severe Moderate Severe Severe Severe Severe Severe Mild Severe Mild Severe Moderate Severe Mild None
Moderate Moderate Moderate Moderate Mild Mild
None None Mild None Mild None
Moderate Mild Severe Moderate Moderate Moderate Moderate Mild None
Mild None Mild None Mild None None None None
T.A. H.F. H.F. H.F. H.F. H.F. S.F. T.A. H.F. H.F. H.F. T.A. H.F. H.F. H.F. H.F. T.A. T.A. T.A. H.F. H.F.
Severe Moderate Mild Mild Mild Severe Severe Severe Moderate Moderate Moderate Moderate Moderate Mild Mild Moderate Moderate Severe Mild Mild Severe
Mild Mild Mild Mild Moderate
None None None None None
Mild Moderate Moderate
Mild Mild Mild
Moderate
Mild
Mild Mild Severe Severe Mild Mild Mild
Mild Mild Mild None None None Mild
Osteoporosis Severe Severe Moderate Severe Severe Mild Moderate Moderate Moderate Severe Severe Mild Severe Moderate Mild Moderate Mild Mild Mild Mild Mild Mild Moderate Mild Moderate Moderate Mild Moderate Moderate Moderate Moderate Moderate Severe None Moderate Mild Mild Mild
F, female; Type II, Type II odontoid fracture; S.F., fall from standing or seated height; H.F., fall from high place; Other, other axis fractures; T.S., traumatic spondylolisthesis; T.A., traffic accident; ETF, extension teardrop fracture. Text in italics show the patients with disproportionate degenerative changes between atlantoodontoid and lateral atlantoaxial joint (difference in grade of $2 levels between joints).
Results The mean age was 77.2 years in patients with Type II odontoid fractures (range, 65–89 years; six men, 11 women) and 74.7 years in those with other axis fractures (range, 65–85 years; 15 men, six women). Age did not differ significantly between groups, but the proportion of women was significantly higher in the Type II fracture group (p!.05). In the Type II fracture group, the causes of fracture were a fall from a high place (n58), a simple fall (n57), neck hanging (n51), and a traffic accident (n51). In the other
fracture group, the causes of fracture were a fall from a high place (n514), traffic accident (n56), and a simple fall (n51). The proportion of fractures caused by a lowenergy trauma (simple fall) was significantly higher in the Type II fracture group (p!.01). In Type II odontoid fractures, complications of injuries included pulmonary injury (n53) and brain injury (n51). The cases with other fractures displayed more severe complications of injuries: subarachnoid haemorrhage (n55), pulmonary injury (n54), cardiac tamponade (n51), and traumatic gastrointestinal perforation (n51). In the 17 patients in the Type II fracture group, one patient died from
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Table 2 Severity of osteoporosis and degenerative change in each group Severity Osteoporosis of dens-body junction None Mild Moderate Severe Atlantoodontoid joint None Mild Moderate Severe Atlantooccipital joint None Mild Moderate Severe Lateral atlantoaxial joint None Mild Moderate Severe
Type II
Other
0 4 6* 7*
1 10 9 1
1 3 3 10
0 7 8 6
1 4 9 1
0 10 4 2
10 5 0 0
8 8 0 0
Type II, Type II odontoid fracture; Other, other axis fractures. The proportion of moderate and severe was significantly higher in Type II odontoid fracture than other axis fractures only in the osteoporosis of dens-body junction. * Statistically significant (p!.05).
myocardial infarction in the acute phase and four patients showed neurologic deficits (one patient with Grade A deficit, one with Grade C, and two with Grade D in Frankel’s classification [17]). In the 21 patients in the other fracture group, three patients had Grade C neurologic deficit and one patient Grade D (Table 1). The severity of osteoporosis of the dens-body junction and the degeneration of the atlantoodontoid joint were evaluated in all patients. Degeneration of the atlantooccipital and lateral atlantoaxial joints was evaluated in 15 of the 17 patients with a Type II odontoid fracture and in 16 of the 21 patients with other fractures. The proportion of patients with moderate or severe osteoporosis was significantly higher in the Type II fracture group than in the other fracture group (p!.05). When the atlantoodontoid, atlantooccipital, and lateral atlantoaxial joints were evaluated individually, the proportion of patients with moderate or severe degeneration in each joint did not differ between the two groups (Table 2). We investigated the disproportion in degeneration between joints, which was defined as a difference in grade
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of $2 between joints. Two of 15 patients with Type II fractures and one of 16 with other fractures showed disproportionate degeneration between the atlantoodontoid and atlantooccipital joints. Seven of 15 patients with Type II fractures and three of 16 with other fractures showed disproportionate degeneration between the atlantooccipital and lateral atlantoaxial joints. Eleven of 15 patients with Type II fractures and four of 16 with other fractures showed disproportionate degeneration between the atlantoodontoid and lateral atlantoaxial joints. Only the disproportionate change between the atlantoodontoid and lateral atlantoaxial joints was significant (p!.05) (Table 1). Osteoporosis and the disproportionate degenerative change between the atlantoodontoid and lateral atlantoaxial joint were included in a multivariate logistic analysis. The disproportionate degenerative change between the atlantoodontoid and lateral atlantoaxial joint remained significant, even after adjusting for osteoporosis (odds ratio, 6.15; 95% CI, 1.15–32.92; p5.034). The model had good predictive ability, with the Hosmer and Lemeshow goodness of fit chi-squared p5.558 (2 degrees of freedom) and the Nagelkerke R250.344 (Table 3).
Discussion In a younger individual, C4–C7 is the most mobile segment of the cervical spine. With degenerative changes, this segment becomes stiffer and the C1–C2 segment becomes the most mobile portion of the cervical spine in older people, predisposing the upper cervical spine to injury [4,7,9]. Axis fractures are frequent among elderly people, and a Type II odontoid fracture is the most frequent individual fracture of the cervical spine in people aged $65 years [4,7–11,13–15]. The incidence of degenerative changes in the atlantoodontoid joint in healthy older people is high—42% in the seventh decade and 60.9% in the eighth decade—and these changes contribute to the obliteration of the atlantoodontoid joint space [18]. The incidence of degenerative changes in the lateral atlantoaxial joint is 4% to 18.2% in normal adults [19,20]. Osteoarthritis in the atlantoodontoid joint occurs frequently and can cause fixation of the dens to the anterior arch of the atlas. By contrast, the lateral atlantoaxial joint is hardly affected by aging-related degeneration. In the people with the disproportionate degenerative change between
Table 3 Multivariate logistic model of predisposing factor of Type II odontoid fracture Risk factors
Other
Type II
Odds ratio (95% confidence intervals)
p
Porosis Disproportion between atlantoodontoid and lateral atlantoaxial joint
10/21 4/16
13/17 11/15
3.19 (0.55–18.62) 6.15 (1.15–32.92)
.198 .034
Type II, Type II odontoid fracture; Other, other axis fractures. The Hosmer and Lemeshow goodness of fit chi-squared p5.558 (2 degrees of freedom) and the Nagelkerke R250.344.
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Figure. (Left) Sagittal and (Middle) axial plane computed tomography (CT) of a 67-year-old woman (Type II odontoid fracture, Case 15) showed obliteration of atlantoodontoid joint (moderate). (Right) Three-dimensional CT showed the atlantoaxial rotatory subluxation (arrow) and no degenerative change of lateral atlantoaxial joint.
atlantoodontoid and lateral atlantoaxial joint, head rotation creates a torque force on the dens-body junction. Analyzing the CT evaluations of 21 patients with Type II odontoid fracture, Lakshmanan et al. found a significant relationship between upper cervical osteoarthritis and the incidence of Type II odontoid fracture [16]. However, their statistical analysis focused only on obliteration of the atlantoodontoid joint and compared these data with those of 15 elderly patients with no Type II odontoid fractures. In our study, to confirm the predisposition proposed by Lakshmanan et al., we compared osteoporosis in the dens-body junction and the disproportionate aging-related degenerative changes between joints in older patients with different types of axis fractures. Few studies have analyzed statistically the relationship between aging-related degeneration in each upper cervical joint. We defined disproportionate degeneration between the joints as a grade difference of $2, and we included the atlantoodontoid, atlantooccipital, and lateral atlantoaxial joints in our analysis. Patients with osteoporosis and with disproportionate degenerative changes between the atlantoodontoid and lateral atlantoaxial joints were significantly more likely to have a Type II odontoid fracture than other fractures. Osteoporosis was more frequent in patients with a Type II odontoid fracture, which might reflect the higher proportion of women in this group. Moreover, a multivariate logistic analysis of these two factors revealed that the disproportion of the osteoarthritis was significantly related to the Type II odontoid fracture, even after adjusting for osteoporosis. The rotation of the head produces torque force on the osteoporotic dens-body junction, which acts as the rotatory center and contributes to a Type II odontoid fracture. This type of fracture will occur if an older person with a degenerative and fixed atlantoodontoid joint and a smooth lateral atlantoaxial joint experiences a simple fall involving a force to one side of the head. Figure shows the rotatory fixation and Type II odontoid fracture in a 67-year-old woman (Type II fracture group, Case 15), who fell from her bed. She represents a typical case of Type II odontoid fracture in the elderly. The results of our study show that the disproportionate degeneration between atlantoodontoid and lateral atlantoaxial joints are predisposing factors for Type
II odontoid fracture in the elderly; this type of injury occurs frequently in a fall from a standing or a seated height.
Conclusions The files of 17 elderly patients with a Type II odontoid fracture were reviewed with a focus on disproportionate degeneration of joints, and these findings were compared with those from elderly patients with other axis fractures. Univariate analysis showed that patients with osteoporosis and disproportionate degenerative changes between the atlantoodontoid and lateral atlantoaxial joints were significantly more likely to have a Type II odontoid fracture than other axis fractures. Moreover, disproportionate degeneration between the atlantoodontoid and lateral atlantoaxial joints was significantly more frequent in patients with a Type II odontoid fracture; this difference remained significant after adjusting for osteoporosis in a multivariate analysis. Type II odontoid fracture is a common injury among elderly people who experience a simple fall. The combination of a degenerative and fixed atlantoodontoid joint with a smooth lateral atlantoaxial joint predisposes an older person to this type of fracture because the rotation of the head produces torque force on the osteoporotic dens-body junction, which acts as the rotatory center.
Acknowledgments The authors gratefully acknowledge Prof. Hiroyuki Kobayashi (Department of Clinical Pharmacology, Tokai University School of Medicine) for his advice in statistical analysis. References [1] Brolin K, von Holst H. Cervical injuries in Sweden, a national survey of patient data from 1987 to 1999. Inj Control Saf Promot 2002;9: 40–52. [2] Bub LD, Blackmore CC, Mann FA, Lomoschitz FM. Cervical spine fractures in patients 65 years and older: a clinical prediction rule for blunt trauma. Radiology 2005;234:143–9.
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[3] Hoskin AF. Trends in unintentional-injury deaths during the 20th century. Stat Bull Metrop Insur Co 2000;81:18–26. [4] Brolin K. Neck injuries among the elderly in Sweden. Inj Control Saf Promot 2003;10:155–64. [5] Damadi AA, Saxe AW, Fath JJ, Apelgren KN. Cervical spine fractures in patients 65 years or older: a 3-year experience at a level I trauma center. J Trauma 2008;64:745–8. [6] Kiwerski JE. Injuries to the spinal cord in elderly patients. Injury 1992;23:397–400. [7] 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;178:573–7. [8] 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;17:585–91. [9] Olerud C, Andersson S, Svensson B, Bring J. Cervical spine fractures in the elderly: factors influencing survival in 65 cases. Acta Orthop Scand 1999;70:509–13. [10] Ryan MD, Henderson JJ. The epidemiology of fractures and fracturedislocations of the cervical spine. Injury 1992;23:38–40. [11] Spivak JM, Weiss MA, Cotler JM, Call M. Cervical spine injuries in patients 65 and older. Spine 1994;19:2302–6.
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[12] Daffner RH, Goldberg AL, Evans TC, et al. Cervical vertebral injuries in the elderly: a 10-year study. Emerg Radiol 1998;5:38–42. [13] Watanabe M, Sakai D, Yamamoto Y, et al. Upper cervical spine injuries: age-specific clinical features. J Orthop Sci 2010;15: 485–92. [14] Anderson LD, D’Alonzo RT. Fractures of the odontoid process of the axis. J Bone Joint Surg Am 1974;56:1663–74. [15] Pepin JW, Bourne RB, Hawkins RJ. Odontoid fractures, with special reference to the elderly patient. Clin Orthop Relat Res 1985;193: 178–83. [16] 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;14:78–83. [17] Frankel HL, Hancock DO, Hyslop G, et al. The value of postural reduction in the initial management of closed injuries of the spine with paraplegia and tetraplegia. I. Paraplegia 1969;7:179–92. [18] Zapletal J, Hekster RE, Straver JS, Wilmink JT. Atlanto-odontoid osteoarthritis. Appearance and prevalence at computed tomography. Spine 1995;20:49–53. [19] Halla JT, Hardin JG Jr. Atlantoaxial (C1-C2) facet joint osteoarthritis: a distinctive clinical syndrome. Arthritis Rheum 1987;30:577–82. [20] Zapletal J, de Valois JC. Radiologic prevalence of advanced lateral C1-C2 osteoarthritis. Spine 1997;22:2511–3.
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Clinical Study
Analysis of predisposing factors in elderly people with Type II odontoid fracture Masahiko Watanabe, MD, PhD*, Daisuke Sakai, MD, PhD, Yukihiro Yamamoto, MD, PhD, Toshihiro Nagai, MD, PhD, Masato Sato, MD, PhD, Joji Mochida, MD, PhD Department of Orthopaedic Surgery, Surgical Science, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa 259-1193, Japan Received 30 January 2012; revised 29 May 2013; accepted 10 July 2013
Abstract
BACKGROUND CONTEXT: Type II odontoid fracture is the most frequent individual fracture in elderly people. An older person usually sustains a Type II odontoid fracture in a fall from standing or a seated height. A relationship between osteoarthritis in the upper cervical spine and Type II odontoid fracture has been reported. However, to our knowledge, few reports have investigated statistically whether disproportionate degeneration between joints influences the susceptibility to fracture. PURPOSE: The purpose of this study was to assess predisposition to Type II odontoid fracture in the elderly. STUDY DESIGN: Retrospective review of elderly patients sustained Type II odontoid fracture and other axis fractures. PATIENT SAMPLE: Thirty-eight patients aged 65 years and older with axis fractures. OUTCOME MEASURES: Evaluation of computed tomography findings by focusing on osteoporosis and the disproportion in degeneration between each of the upper cervical joints (atlantooccipital, atlantoodontoid, and lateral atlantoaxial joints). METHODS: Seventeen patients had a Type II odontoid fracture, and 21 patients had other axis fractures. Using the computed tomography findings, we classified osteoporosis at the dens-body junction and the severity of degenerative changes in the atlantoodontoid, atlantooccipital, and lateral atlantoaxial joints as none, mild, moderate, or severe. The proportion of patients with moderate or severe osteoporosis and degenerative changes in each joint and that of patients with disproportionate degenerative changes between joints (difference in grade of $2 levels between joints) were compared statistically. The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this article. RESULTS: Patients with osteoporosis and with disproportionate degenerative changes between the atlantoodontoid and lateral atlantoaxial joints were significantly more likely to have a Type II odontoid fracture than other axis fractures. These two factors were also assessed in multivariate logistic analysis. The disproportionate degenerative change between the atlantoodontoid and lateral atlantoaxial joint remained significant, even after adjusting for osteoporosis. CONCLUSIONS: Older patients with the dens fixed to the atlas because of degeneration of the atlantoodontoid joint and a smooth lateral atlantoaxial joint seem to sustain Type II odontoid fractures because, during a simple fall, the rotation of the head produces torque force on the osteoporotic dens-body junction, which acts as the rotatory center. The presence of the disproportionate osteoarthritic degeneration between the atlantoodontoid and lateral atlantoaxial joints predisposes older people to a Type II odontoid fracture. Ó 2013 Elsevier Inc. All rights reserved.
Keywords:
Upper cervical spine injury; Elderly; Osteoarthritis; Degenerative change; Type II odontoid fracture
FDA device/drug status: Not applicable. Author disclosures: MW: Nothing to disclose. DS: Nothing to disclose. YY: Nothing to disclose. TN: Nothing to disclose. MS: Nothing to disclose. JM: Nothing to disclose. 1529-9430/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.spinee.2013.07.434
* Corresponding author. Department of Orthopaedic Surgery, Surgical Science, Tokai University School of Medicine, 143 Shimokasuya, Isehara, Kanagawa 259-1193, Japan. Tel.: (81) 463-93-1121x2320; fax: (81) 46396-4404. E-mail address: [email protected] (M. Watanabe)
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M. Watanabe et al. / The Spine Journal
Introduction Data from different parts of the world show a trend toward decreasing neck injury incidence for age groups !65 years, whereas the incidence has remained constant or has increased in people aged 65 years and older [1–3]. In young adults, most trauma causing cervical spine injury involves high-energy injury, such as traffic accidents and falls from a high place. By contrast, in older people, cervical spine injuries are more likely to be caused by a lowenergy injury such as a fall from standing or a seated height [4–11]. In young people, the middle and lower cervical spine is more prone to injury, but in older people, the upper cervical spine is more likely to be injured [7,8,10]. Daffner et al. [12] reported that upper cervical lesions accounted for 68.9% of all cervical injuries in the elderly and 35.8% in young people. Although the middle and lower cervical spine is the most mobile portion in young people, age-related degeneration makes the middle and lower cervical spine stiffer. The accompanying shift of the motion segment to the upper cervical spine is responsible for the increased frequency of upper cervical spine injury in the elderly compared with the middle and lower cervical spine [4,7,9]. We have reported on the aging-related clinical features of upper cervical spine injury [13]. Type II odontoid fracture classified by Anderson and D’Alonso [14] is the most frequent individual fracture in the elderly [4,7–11,13–15]. Lakshmanan et al. [16] reported a significant relationship between upper cervical osteoarthritis and the incidence of Type II odontoid fracture. Severe degenerative changes in the atlantoodontoid joint develop with aging and fix the odontoid to the anterior arch of the atlas. By contrast, the lateral atlantoaxial joint is less affected by osteoarthritis. Low-energy trauma induces forced atlantoaxial rotation, which along with marked limitation of movement at the atlantoodontoid joint can produce a torque force at the base of the osteoporotic odontoid process. However, to our knowledge, few studies have investigated statistically the relationship of Type II odontoid fracture with osteoporosis and with the disproportional degeneration of these joints. The aim of this study was to examine the predisposition in older people toward Type II odontoid fracture compared with other axis fractures, using univariate and multivariate analyses. We focused on osteoporosis and disproportional degenerative changes in adjacent joints of the upper cervical spine and studied their relationship with fracture risk.
Materials and methods Our series included 38 patients aged $65 years who sustained a fracture of the axis between February 2001 and June 2011. Seventeen patients had a Type II odontoid fracture, and 21 patients had other axis fracture types. Other axis fractures included 15 cases of traumatic spondylolisthesis (including three cases of combined hyperextension
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teardrop fracture and one case of combined Type III odontoid fracture), three body fractures, two hyperextension teardrop fractures, and one Type III odontoid fracture. In this study, we compared Type II odontoid fractures with other axis fractures. Data on the injury etiology, neurologic deficit, and complicated injury were obtained from clinical records. We classified osteoporosis at the dens-body junction as none (normal trabecular pattern with normal cortical thickness), mild (decrease in the amount of trabeculae with no areas of absent trabeculae [holes] and normal cortical thickness), moderate (absent trabeculae [holes] involving !50% of the transverse diameter of the bone with cortical thinning), or severe (absent trabeculae [holes] involving O50% of the transverse diameter of the bone with cortical thinning). The severity of degenerative changes in the atlantoodontoid joint was classified as none (normal joint space with no osteophytes), mild (narrowed joint space or normal joint space with osteophyte formation), moderate (obliterated joint space with or without osteophyte formation), or severe (ankylosis of the joint with either excrescences in the joint or transverse ligament calcification, or both). The severity of degenerative changes in the atlantooccipital and lateral atlantoaxial joints was classified similarly as none, mild, moderate, but with some modification in severe (completely obliterated joint space with osteophyte excrescences and/or fusion of the joint). The classifications involving the osteoporosis at the dens-body junction and the degenerative joint changes were made from computed tomography (CT) images according to the method described by Lakshmanan et al. [16] Two reviewers reviewed each CT image in a blinded manner and discussed their findings to arrive at consensus in the case of different views. The data were analysed using PASW Statistics 18 (SPSS Japan Inc., an IBM company, Japan). We categorized a fall from standing or a seated height as a low-energy injury and other falls as a high-energy injury. Chi-square tests were used to compare the patients who sustained a Type II odontoid fracture with those who sustained other axis fractures. Differences in the proportion of patients between the two groups were compared for the following variables: moderate and severe degenerative changes in the atlantoodontoid joint, atlantooccipital joint, and lateral atlantoaxial joint; moderate and severe in the osteoporosis of the axis vertebra; and disproportion in degenerative changes between each joint, defined as a difference in grade of $2 levels between joints. To assess the predisposition to Type II odontoid fractures, multivariate logistic analysis was performed on factors in which a significant difference was detected using Chi-square tests because the number of Type II odontoid fractures was limited. The final model was checked for goodness of fit with the Hosmer and Lemeshow test and by colinearity and residual diagnostics, to ensure they were well specified and fit. Significance was set at p!.05.
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Table 1 Clinical data Severity of degenerative change No. Type II 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Other 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
Age
Sex
Type of fracture
Complicated upper cervical injury
89 87 86 86 83 82 81 80 78 78 77 71 70 67 67 65 66
F F M F M F M F M F F F M F F M F
Type Type Type Type Type Type Type Type Type Type Type Type Type Type Type Type Type
Post arch
85 85 85 81 80 79 79 78 76 76 73 71 71 71 70 70 69 69 68 68 65
M M M M M M M M F M M F M F F F M M F M M
T.S. T.S. T.S. T.S. T.S. T.S. ETF T.S. Type III ETF T.S. T.S. Body fracture Body fracture T.S. Body fracture T.S. T.S. T.S. T.S. T.S.
II II II II II II II II II II II II II II II II II
Jeffeson
Type III ETF
ETF
Anterior arch
ETF
Etiology
Atlantoodontoid joint
Atlantooccipital joint
Lateral atlantoaxial joint
S.F. H.F. S.F. S.F. S.F. H.F. S.F. Neck hanging H.F. H.F. S.F. H.F. H.F. H.F. S.F. H.F. T.A.
Severe Moderate Severe Moderate Severe Severe Severe Severe Severe Mild Severe Mild Severe Moderate Severe Mild None
Moderate Moderate Moderate Moderate Mild Mild
None None Mild None Mild None
Moderate Mild Severe Moderate Moderate Moderate Moderate Mild None
Mild None Mild None Mild None None None None
T.A. H.F. H.F. H.F. H.F. H.F. S.F. T.A. H.F. H.F. H.F. T.A. H.F. H.F. H.F. H.F. T.A. T.A. T.A. H.F. H.F.
Severe Moderate Mild Mild Mild Severe Severe Severe Moderate Moderate Moderate Moderate Moderate Mild Mild Moderate Moderate Severe Mild Mild Severe
Mild Mild Mild Mild Moderate
None None None None None
Mild Moderate Moderate
Mild Mild Mild
Moderate
Mild
Mild Mild Severe Severe Mild Mild Mild
Mild Mild Mild None None None Mild
Osteoporosis Severe Severe Moderate Severe Severe Mild Moderate Moderate Moderate Severe Severe Mild Severe Moderate Mild Moderate Mild Mild Mild Mild Mild Mild Moderate Mild Moderate Moderate Mild Moderate Moderate Moderate Moderate Moderate Severe None Moderate Mild Mild Mild
F, female; Type II, Type II odontoid fracture; S.F., fall from standing or seated height; H.F., fall from high place; Other, other axis fractures; T.S., traumatic spondylolisthesis; T.A., traffic accident; ETF, extension teardrop fracture. Text in italics show the patients with disproportionate degenerative changes between atlantoodontoid and lateral atlantoaxial joint (difference in grade of $2 levels between joints).
Results The mean age was 77.2 years in patients with Type II odontoid fractures (range, 65–89 years; six men, 11 women) and 74.7 years in those with other axis fractures (range, 65–85 years; 15 men, six women). Age did not differ significantly between groups, but the proportion of women was significantly higher in the Type II fracture group (p!.05). In the Type II fracture group, the causes of fracture were a fall from a high place (n58), a simple fall (n57), neck hanging (n51), and a traffic accident (n51). In the other
fracture group, the causes of fracture were a fall from a high place (n514), traffic accident (n56), and a simple fall (n51). The proportion of fractures caused by a lowenergy trauma (simple fall) was significantly higher in the Type II fracture group (p!.01). In Type II odontoid fractures, complications of injuries included pulmonary injury (n53) and brain injury (n51). The cases with other fractures displayed more severe complications of injuries: subarachnoid haemorrhage (n55), pulmonary injury (n54), cardiac tamponade (n51), and traumatic gastrointestinal perforation (n51). In the 17 patients in the Type II fracture group, one patient died from
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Table 2 Severity of osteoporosis and degenerative change in each group Severity Osteoporosis of dens-body junction None Mild Moderate Severe Atlantoodontoid joint None Mild Moderate Severe Atlantooccipital joint None Mild Moderate Severe Lateral atlantoaxial joint None Mild Moderate Severe
Type II
Other
0 4 6* 7*
1 10 9 1
1 3 3 10
0 7 8 6
1 4 9 1
0 10 4 2
10 5 0 0
8 8 0 0
Type II, Type II odontoid fracture; Other, other axis fractures. The proportion of moderate and severe was significantly higher in Type II odontoid fracture than other axis fractures only in the osteoporosis of dens-body junction. * Statistically significant (p!.05).
myocardial infarction in the acute phase and four patients showed neurologic deficits (one patient with Grade A deficit, one with Grade C, and two with Grade D in Frankel’s classification [17]). In the 21 patients in the other fracture group, three patients had Grade C neurologic deficit and one patient Grade D (Table 1). The severity of osteoporosis of the dens-body junction and the degeneration of the atlantoodontoid joint were evaluated in all patients. Degeneration of the atlantooccipital and lateral atlantoaxial joints was evaluated in 15 of the 17 patients with a Type II odontoid fracture and in 16 of the 21 patients with other fractures. The proportion of patients with moderate or severe osteoporosis was significantly higher in the Type II fracture group than in the other fracture group (p!.05). When the atlantoodontoid, atlantooccipital, and lateral atlantoaxial joints were evaluated individually, the proportion of patients with moderate or severe degeneration in each joint did not differ between the two groups (Table 2). We investigated the disproportion in degeneration between joints, which was defined as a difference in grade
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of $2 between joints. Two of 15 patients with Type II fractures and one of 16 with other fractures showed disproportionate degeneration between the atlantoodontoid and atlantooccipital joints. Seven of 15 patients with Type II fractures and three of 16 with other fractures showed disproportionate degeneration between the atlantooccipital and lateral atlantoaxial joints. Eleven of 15 patients with Type II fractures and four of 16 with other fractures showed disproportionate degeneration between the atlantoodontoid and lateral atlantoaxial joints. Only the disproportionate change between the atlantoodontoid and lateral atlantoaxial joints was significant (p!.05) (Table 1). Osteoporosis and the disproportionate degenerative change between the atlantoodontoid and lateral atlantoaxial joint were included in a multivariate logistic analysis. The disproportionate degenerative change between the atlantoodontoid and lateral atlantoaxial joint remained significant, even after adjusting for osteoporosis (odds ratio, 6.15; 95% CI, 1.15–32.92; p5.034). The model had good predictive ability, with the Hosmer and Lemeshow goodness of fit chi-squared p5.558 (2 degrees of freedom) and the Nagelkerke R250.344 (Table 3).
Discussion In a younger individual, C4–C7 is the most mobile segment of the cervical spine. With degenerative changes, this segment becomes stiffer and the C1–C2 segment becomes the most mobile portion of the cervical spine in older people, predisposing the upper cervical spine to injury [4,7,9]. Axis fractures are frequent among elderly people, and a Type II odontoid fracture is the most frequent individual fracture of the cervical spine in people aged $65 years [4,7–11,13–15]. The incidence of degenerative changes in the atlantoodontoid joint in healthy older people is high—42% in the seventh decade and 60.9% in the eighth decade—and these changes contribute to the obliteration of the atlantoodontoid joint space [18]. The incidence of degenerative changes in the lateral atlantoaxial joint is 4% to 18.2% in normal adults [19,20]. Osteoarthritis in the atlantoodontoid joint occurs frequently and can cause fixation of the dens to the anterior arch of the atlas. By contrast, the lateral atlantoaxial joint is hardly affected by aging-related degeneration. In the people with the disproportionate degenerative change between
Table 3 Multivariate logistic model of predisposing factor of Type II odontoid fracture Risk factors
Other
Type II
Odds ratio (95% confidence intervals)
p
Porosis Disproportion between atlantoodontoid and lateral atlantoaxial joint
10/21 4/16
13/17 11/15
3.19 (0.55–18.62) 6.15 (1.15–32.92)
.198 .034
Type II, Type II odontoid fracture; Other, other axis fractures. The Hosmer and Lemeshow goodness of fit chi-squared p5.558 (2 degrees of freedom) and the Nagelkerke R250.344.
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Figure. (Left) Sagittal and (Middle) axial plane computed tomography (CT) of a 67-year-old woman (Type II odontoid fracture, Case 15) showed obliteration of atlantoodontoid joint (moderate). (Right) Three-dimensional CT showed the atlantoaxial rotatory subluxation (arrow) and no degenerative change of lateral atlantoaxial joint.
atlantoodontoid and lateral atlantoaxial joint, head rotation creates a torque force on the dens-body junction. Analyzing the CT evaluations of 21 patients with Type II odontoid fracture, Lakshmanan et al. found a significant relationship between upper cervical osteoarthritis and the incidence of Type II odontoid fracture [16]. However, their statistical analysis focused only on obliteration of the atlantoodontoid joint and compared these data with those of 15 elderly patients with no Type II odontoid fractures. In our study, to confirm the predisposition proposed by Lakshmanan et al., we compared osteoporosis in the dens-body junction and the disproportionate aging-related degenerative changes between joints in older patients with different types of axis fractures. Few studies have analyzed statistically the relationship between aging-related degeneration in each upper cervical joint. We defined disproportionate degeneration between the joints as a grade difference of $2, and we included the atlantoodontoid, atlantooccipital, and lateral atlantoaxial joints in our analysis. Patients with osteoporosis and with disproportionate degenerative changes between the atlantoodontoid and lateral atlantoaxial joints were significantly more likely to have a Type II odontoid fracture than other fractures. Osteoporosis was more frequent in patients with a Type II odontoid fracture, which might reflect the higher proportion of women in this group. Moreover, a multivariate logistic analysis of these two factors revealed that the disproportion of the osteoarthritis was significantly related to the Type II odontoid fracture, even after adjusting for osteoporosis. The rotation of the head produces torque force on the osteoporotic dens-body junction, which acts as the rotatory center and contributes to a Type II odontoid fracture. This type of fracture will occur if an older person with a degenerative and fixed atlantoodontoid joint and a smooth lateral atlantoaxial joint experiences a simple fall involving a force to one side of the head. Figure shows the rotatory fixation and Type II odontoid fracture in a 67-year-old woman (Type II fracture group, Case 15), who fell from her bed. She represents a typical case of Type II odontoid fracture in the elderly. The results of our study show that the disproportionate degeneration between atlantoodontoid and lateral atlantoaxial joints are predisposing factors for Type
II odontoid fracture in the elderly; this type of injury occurs frequently in a fall from a standing or a seated height.
Conclusions The files of 17 elderly patients with a Type II odontoid fracture were reviewed with a focus on disproportionate degeneration of joints, and these findings were compared with those from elderly patients with other axis fractures. Univariate analysis showed that patients with osteoporosis and disproportionate degenerative changes between the atlantoodontoid and lateral atlantoaxial joints were significantly more likely to have a Type II odontoid fracture than other axis fractures. Moreover, disproportionate degeneration between the atlantoodontoid and lateral atlantoaxial joints was significantly more frequent in patients with a Type II odontoid fracture; this difference remained significant after adjusting for osteoporosis in a multivariate analysis. Type II odontoid fracture is a common injury among elderly people who experience a simple fall. The combination of a degenerative and fixed atlantoodontoid joint with a smooth lateral atlantoaxial joint predisposes an older person to this type of fracture because the rotation of the head produces torque force on the osteoporotic dens-body junction, which acts as the rotatory center.
Acknowledgments The authors gratefully acknowledge Prof. Hiroyuki Kobayashi (Department of Clinical Pharmacology, Tokai University School of Medicine) for his advice in statistical analysis. References [1] Brolin K, von Holst H. Cervical injuries in Sweden, a national survey of patient data from 1987 to 1999. Inj Control Saf Promot 2002;9: 40–52. [2] Bub LD, Blackmore CC, Mann FA, Lomoschitz FM. Cervical spine fractures in patients 65 years and older: a clinical prediction rule for blunt trauma. Radiology 2005;234:143–9.
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