Abstract
Backgroud
Osteoporotic vertebral compression fractures (OVCF) cascades (OVCFcs) repeatedly cause vertebral compression to involve multiple vertebra. This study aimed to introduce an accelerated form of OVCFcs: acute multiple OVCF (amOVCF).
Methods
OVCF patients with multiple vertebral augmentations in a spine center between June 2016 and October 2020 were retrospectively studied. Demographics, spine trauma, anatomical distribution, and distribution pattern of OVCF in OVCFcs and amOVCF were summarized and compared.
Results
429 patients with multiple vertebral augmentations in 1164 vertebra were included. There were 210 OVCFcs accumulating 622 OVCF and 219 amOVCF simultaneously involving 542 vertebra. The OVCFcs progressed at 0.48 fractures and 0.56 vertebra per year. Both OVCFcs and amOVCF demonstrated asymmetrical bimodal distribution in spine and most frequently involved L1. The incidence of adjacent OVCF was 40.14% in amOVCF with 2 OVCF and 84.72% in amOVCF with ≥ 3 OVCF, and the distribution pattern of OVCF was not significantly different between amOVCF and OVCFcs. The female/male ratio was 5.56 in OVCFcs and not different from that of 4.34 in amOVCF. The age of females (73.41 ± 8.08 and 76.29 ± 8.25 years old) but not males (77.20 ± 10.13 and 79.75 ± 10.21 years old) was significantly increased from initial to last OVCF in OVCFcs. amOVCF had similar age (72.26 ± 10.09 years old) as OVCFcs at initial OVCF (73.99 ± 8.51 years old) and were significantly younger than OVCFcs at last OVCF (76.82 ± 8.64 years old). 54.29% in OVCFcs and 48.4% in amOVCF reported no evident trauma, and the ratio of apparent spine trauma was higher in amOVCF (43.38%) than in OVCFcs (28.54%).
Conclusions
amOVCF are accelerated form of OVCFcs showing similar anatomical distribution and distribution pattern of OVCF in spine. Both amOVCF and OVCFcs cause multiple fragility fractures without significant spine trauma.
Keywords: Osteoporotic vertebral compression fracture, Multiple fracture, Fragility fracture, Vertebral fracture cascade
Background
Osteoporotic vertebral compression fractures (OVCF) are prevalent disease in elderly populations worldwide, estimated to involve 1.4 million annually [1]. Vertebral fractures are not only diagnostic of osteoporosis but also highly predictive of subsequent vertebral fractures [2–4]. For patients with previous OVCF, the relative risk of having recurrent OVCF would increase more than fourfold [2]. Although not clearly defined in the number of re-fractures and the period of observation, the term “vertebral fractures cascades” was introduced to highlight the escalating risk of new OVCF after OVCF [5–8]. As OVCF cascades (OVCFcs) progress, both mortality risk and health and economic burdens would significantly increase in the elderly [9, 10]. To halt cascading OVCF, a comprehensive understanding of the mechanism underlying fracture cascades is needed.
There is evidence showing that vertebral compression increases flexion movement and shear force in adjacent vertebra [11]. Cement augmentation (vertebroplasty or kyphoplasty) helps to restore vertebral morphology and reduce acute back pain, but potentially causes strain in adjacent vertebra and risks new OVCF [12, 13]. In addition to adjacent biomechanical stress after OVCF, a variety of non-mechanical factors including age [3, 4], gender [14], bone mineral density [4, 15], and osteoporosis medication [16] have been revealed to be associated with subsequent OVCF. Meanwhile, an increasing number of predicting models of OVCF were developed in recent years [17, 18], but few have proved clinically reliable. One obstacle in understanding OVCFcs is lack of model of vertebral fractures and re-fractures.
While sustaining subsequent OVCF would cumulatively result in multiple vertebral compression, OVCF can simultaneously involve multiple vertebra at initial diagnosis [19]. As compared with cascading OVCF, acute multiple OVCF (amOVCF) potentially accelerates the involvement of vertebra in compression fractures. Besides, amOVCF are free from the biomechanical stress of previous OVCF [11–13], which might provide more cues of non-mechanical mechanism underlying OVCFcs. To better understand the pattern of vertebral involvement in fragility fractures, we performed a retrospective comparative study of OVCFcs and amOVCF in terms of demographics, spine trauma, vertebral fracture location and distribution. We hypothesize amOVCF might be a model of accelerated OVCFcs with similar distribution pattern in spine.
Methods
Study population
The study was approved by Ethic Committee for Clinical Research of Zhongda hospital affiliated to Southeast University (No.2022ZDSYLL016). Medical records, Magnetic Resonance Imaging (MRI), and post-surgery X-ray of patients received vertebroplasty or kyphoplasty from June 2016 to October 2020 in the spine center of Zhongda hospital were retrospectively studied.
Inclusion criteria
(1) aged ≥ 45 years old; (2) diagnosis of acute OVCF based on symptom of back pain and signal of vertebral marrow edema on MRI of thoracic and lumbar spine; (3) post-surgery X-ray of spine showing cement augmentation at multiple vertebra; (4) full medical records detailing demographics and type of spine trauma before hospitalization.
Exclusion criteria
(1) pathologic diagnosis of infection, hemangioma, multiple myeloma, metastatic tumors, and other pathological vertebral fractures; (2) previous spine surgery with internal fixation; (3) prophylactic vertebral augmentation.
Grouping and data collection
Based on the pattern of vertebral involvement in compression fractures, the study population of multiple vertebral augmentation was divided into two groups. Group of OVCFcs: acute vertebral compression with previous OVCF and vertebroplasty or kyphoplasty, and group of amOVCF: acute multiple vertebral compression without previous vertebral augmentation (Fig. 1).
Fig. 1.
OVCFcs and amOVCF. The post-surgery X-ray of OVCFcs (a-c): A 78 years old male experienced initial OVCF and vertebral augmentation in L1 at 72 years old (a). Subsequent OVCF occurred 2.5 years later in L3 (b) and 5.5 years later in L5 (c). The MRI and post-surgery X-ray of amOVCF (d-f): A 72 years old female OVCF showed signal of vertebral marrow edema in L1, L3, and L5 (d: T1-weighted MRI, e: T2-weighted fat suppression MRI). Multiple cement augmentations were performed in the three fractured vertebra (f). OVCF: osteoporotic vertebral compression fractures; OVCFcs: osteoporotic vertebral compression fractures cascades; amOVCF: acute multiple osteoporotic vertebral compression fractures
In each group the demographics (age, gender) and spine trauma were summarized from medical records. Patients’ age was sub-grouped into < 60, 60–70, 70–80, and ≥ 80 years old. For OVCFcs, both the age at initial and last OVCF were collected. Based on the significance of trauma prior to back pain, spine trauma was sub-grouped into apparent trauma: fall on ground or crush injury to spine, uncertain trauma: heavy lifting injury, lumbar sprain, strenuous cough, and no evident trauma. For OVCFcs, the type of spine trauma for each cascade of OVCF was collected.
The amount of vertebral fractures was counted in the augmented vertebra on post-surgery X-ray of spine, and sub-grouped into 2, 3, and ≥ 4 OVCF. The anatomical location of OVCF was defined into thoracic (T1-T10), thoracolumbar (T11-L2), and lumbar (L3-L5) segment, and in case of lumbosacral transitional vertebra reconfirmed by two radiologists. According to the position relation between augmented and intact vertebra, the distribution pattern of vertebral fractures was grouped into two OVCF in adjacent, intermittent with one intact vertebrae, and intermittent with ≥ 2 intact vertebra. For OVCFcs, the amount and distribution pattern of vertebral fractures were collected from the post-surgery X-ray of last OVCF.
Statistical analysis
Prism software (ver.9.1.2; Graphpad, San Diego, CA, USA) was used to perform statistical analysis. Descriptive statistics with Pearson χ2 were performed to compare the frequencies and percentages of categorical variables between amOVCF and OVCFcs. Continuous quantitative data were presented as means ± standard deviations. Differences between two groups were analyzed by unpaired t test. Differences among multiple groups were analyzed by one-way ANOVA followed by Tukey’s multiple comparisons test. Statistical significance was defined as P value < 0.05.
Results
OVCFcs and amOVCF demonstrated asymmetrical bimodal distribution
A total of 1490 cases of OVCF were treated with cement augmentation from June 2016 to October 2020 in the spine center of Zhongda hospital. 429 cases (28.79%) showing multiple vertebral augmentations on post-surgery X-ray were included in this study. There were 210 OVCFcs experiencing 494 vertebral fractures involving 622 vertebra, and 219 amOVCF simultaneously involving 542 vertebra.
In both OVCFcs and amOVCF, L1 was the most frequently fractured vertebrae. The incidence of OVCF reduced gradually from L1 to L5 and from T12 to T9, then increased at T8 and reduced again from T7 to T4, demonstrating asymmetrical bimodal distribution (Fig. 2). The OVCFcs and amOVCF involved in total 1164 OVCF, of which 634 (54.47%) were located in thoracolumbar, 272 (23.37%) in lumbar, and 258 (22.16%) in thoracic segment. The anatomical distribution of OVCF was not significantly different between OVCFcs and amOVCF (Table 1).
Fig. 2.
Anatomical distribution of OVCFcs and amOVCF.Both OVCFcs and amOVCF showed asymmetrical bimodal distribution peaked at L1 and T8. OVCF: osteoporotic vertebral compression fractures; OVCFcs: osteoporotic vertebral compression fractures cascades; amOVCF: acute multiple osteoporotic vertebral compression fractures
Table 1.
Anatomical distribution of OVCF in OVCFcs and amOVCF
| Spine segment | OVCFcs (N=622) |
amOVCF (N=542) |
P-value |
|---|---|---|---|
| N(%) | N(%) | ||
| 0.131 | |||
| Thoracic (T1-T10) | 140(22.51) | 118(21.77) | |
| Thoracolumbar (T11-L2) | 351(56.43) | 283(52.22) | |
| Lumbar (L3-L5) | 131(21.06) | 141(26.01) |
OVCFcs: osteoporotic vertebral compression fractures cascades
amOVCF: acute multiple osteoporotic vertebral compression fractures
OVCFcs and amOVCF demonstrated similar distribution pattern of OVCF
Of the 429 cases with multiple vertebral augmentations, there were 239 (55.71%) in 2 vertebra, 109 (25.41%) in 3 vertebra, and 81 (18.88%) in ≥ 4 vertebra.
Of the 239 cases with 2 OVCF, there were 92 cases (38.49%) having the two OVCF in adjacent, 64 (26.78%) intermittent with one intact vertebrae, and 83 (34.73%) intermittent with ≥ 2 vertebra. The distribution pattern of 2 OVCF was not significantly different between amOVCF and OVCFcs (Table 2).
Table 2.
Distribution pattern of 2 OVCF in OVCFcs and amOVCF
| Distribution pattern | OVCFcs (N=92) |
amOVCF (N=147) |
P-value |
|---|---|---|---|
| N(%) | N(%) | ||
| 0.80 | |||
| two OVCF in adjacent | 33(35.87) | 59(40.14) | |
| intermittent with one intact vertebrae | 26(28.26) | 38(25.85) | |
| intermittent with two or more intact vertebrae | 33(35.87) | 50(34.01) |
OVCFcs: osteoporotic vertebral compression fractures cascades
amOVCF: acute multiple osteoporotic vertebral compression fractures
Of the 190 cases with ≥ 3 OVCF, there were 158 cases (83.16%) having at least two OVCF in adjacent, 25 (13.16%) intermittent with one intact vertebrae, and 7 (3.68%) intermittent with ≥ 2 vertebra. The distribution pattern of ≥ 3 OVCF was not significantly different between amOVCF and OVCFcs (Table 3).
Table 3.
Distribution pattern of ≥3 OVCF in OVCFcs and amOVCF
| Distribution pattern | OVCF Cascades (N=118) |
Multiple OVCF (N=72) |
P-value |
|---|---|---|---|
| N(%) | N(%) | ||
| 0.066 | |||
| two OVCF in adjacent | 97(82.21) | 61(84.72) | |
| intermittent with one intact vertebrae | 19(16.10) | 6(8.33) | |
| intermittent with two or more intact vertebrae | 2(1.69) | 5(6.95) |
OVCFcs: osteoporotic vertebral compression fractures cascades
amOVCF: acute multiple osteoporotic vertebral compression fractures
amOVCF had similar gender ratio as OVCFcs and similar age between females and males
The OVCFcs and amOVCF included 356 females and 73 males, with female/male ratio approximating 4.88. The female/male ratio was 4.34 in amOVCF and 5.56 in OVCFcs and not significant different between the two groups (Table 4).
Table 4.
Demographics of OVCFcs and amOVCF
| Demographic variables | OVCFcs (N=210) |
amOVCF (N=219) |
P-value |
|---|---|---|---|
| N(%) | N(%) | ||
| Gender | 0.337 | ||
| Females | 178(84.76) | 178(81.28) | |
| Males | 32(15.24) | 41(18.72) | |
| Age for patients (in years old) | <0.0001 | ||
| <60 | 7(3.33) | 25(11.42) | |
| 60-70 | 35(16.67) | 69(31.51) | |
| 70-80 | 74(35.24) | 61(27.85) | |
| >80 | 94(44.76) | 64(29.22) | |
| Age for females (in years old) | 0.00016 | ||
| <60 | 5(2.81) | 15(8.43) | |
| 60-70 | 31(17.42) | 59(33.15) | |
| 70-80 | 68(38.20) | 55(30.89) | |
| >80 | 74(41.57) | 49(27.53) | |
| Age for males (in years old) | 0.054 | ||
| <60 | 2(6.25) | 10(24.39) | |
| 60-70 | 4(12.50) | 10(24.39) | |
| 70-80 | 6(18.75) | 6(14.63) | |
| >80 | 20(62.50) | 15(36.59) |
OVCFcs: osteoporotic vertebral compression fractures cascades
amOVCF: acute multiple osteoporotic vertebral compression fractures
The OVCFcs were aged 46.5–97.5 (73.99 ± 8.51) years old at initial OVCF and 47–98 (76.82 ± 8.64) years old at last OVCF. Females (73.41 ± 8.08 and 76.29 ± 8.25) were on average 3.79 and 3.46 years younger than males (77.20 ± 10.13 and 79.75 ± 10.21) at initial and last OVCF in OVCFcs respectively (Fig. 3). The amOVCF were aged 46–98 (72.26 ± 10.09) years old and not significantly different in the age between females (72.53 ± 9.37) and males (71.07 ± 12.84) (Fig. 3).
Fig. 3.
Comparison of age between females and males in OVCFcs and amOVCF. Females were younger than males at initial and last OVCF in OVCFcs. Females and males had similar age in amOVCF. *: P < 0.05, NS: not significantly different. OVCF: osteoporotic vertebral compression fractures; OVCFcs: osteoporotic vertebral compression fractures cascades; amOVCF: acute multiple osteoporotic vertebral compression fractures
amOVCF were younger than OVCFcs at last OVCF
The OVCFcs experienced 210 initial vertebral fractures involving 290 vertebra and 284 re-fractures involving 332 new vertebra. The OVCFcs were 2.83 years older at last OVCF than at initial OVCF (Fig. 4), progressing on average at 0.48 vertebral fractures and 0.56 fractured vertebra per year.
Fig. 4.
Comparison of age between amOVCF and OVCFcs at initial and last OVCF. The age of females but not males were significantly increased in OVCFcs from initial to last OVCF. amOVCF had similar age as OVCFcs at initial OVCF. amOVCF were significantly younger than OVCFcs at last OVCF in both females and males. **: P < 0.01, ***:P < 0.005, NS: not significantly different .OVCF: osteoporotic vertebral compression fractures; OVCFcs: osteoporotic vertebral compression fractures cascades; amOVCF: acute multiple osteoporotic vertebral compression fractures
The females and males in amOVCF had similar age as OVCFcs at initial OVCF, and were significantly younger than OVCFcs at last OVCF. The age of males was not significantly increased from initial to last OVCF in OVCFcs (Fig. 4). The ratio of females aged < 60 and 60–70 years older were higher in amOVCF than in OVCFcs at last OVCF. The age ratio of males was not significantly different between amOVCF and OVCFcs at last OVCF (Table 4).
amOVCF reported higher ratio of apparent spine trauma than OVCFcs
Of the 494 fracture cascades in OVCFcs, 396 records (80.16%) of spine trauma were collected. Both OVCFcs and amOVCF reported higher ratio of no evident trauma than apparent and uncertain trauma. The ratio of apparent spine trauma was significantly higher in amOVCF than in OVCFcs (Table 5).
Table 5.
Spine trauma of OVCFcs and amOVCF
| Spine trauma | OVCF Cascades (N=396) |
Multiple OVCF (N=219) |
P-value |
|---|---|---|---|
| N(%) | N(%) | ||
| 0.00011 | |||
| apparent trauma | 113(28.54) | 95(43.38) | |
| uncertain trauma | 68(17.17) | 18(8.22) | |
| no evident trauma | 215(54.29) | 106(48.40) |
OVCFcs: osteoporotic vertebral compression fractures cascades
amOVCF: acute multiple osteoporotic vertebral compression fractures
Discussion
OVCFcs are severe complication of osteoporosis characteristic of sustaining re-fractures in spine [5–8]. Our study showed that OVCFcs progressed at 0.48 vertebral fractures and 0.56 fractured vertebra per year to involve multiple vertebra. Meanwhile, we noticed an accelerated form of OVCFcs as amOVCF that simultaneously involved multiple vertebra. Based on the finding that both OVCFcs and amOVCF showed asymmetrical bimodal distribution in spine, and that both the fractured 2 and ≥ 3 vertebra in amOVCF showed similar distribution pattern as that in OVCFcs, we can propose two forms of multiple vertebral involvement in fragility fractures: one is accumulative OVCFcs, the other one is accelerative amOVCF. Comparison of the two forms of OVCF spreading may provide a new approach to understand the mechanism underlying vertebral fractures and re-fractures.
Increasing age was previously identified as risk factor of re-fractures [3, 4]. Our study supported this notion by showing that OVCFcs were on average 2.83 years older at last OVCF than at initial OVCF. Besides, we found that the age of females rather than males was significantly increased from initial to last OVCF, suggesting the age-driven OVCFcs were comparatively faster in males. Fragility fractures occur more commonly and at earlier ages among females than males [14, 20]. We found that both OVCFcs and amOVCF included more females than males, suggesting the risk of fragility fractures in multiple vertebra also increased in females. Interestingly, while females were younger than males both at initial and last OVCF in OVCFcs, no significant difference was detected in the age of amOVCF between females and males, nor between the age of amOVCF and the OVCFcs at initial OVCF. These findings indicate female and increasing age as risk factors of OVCFcs, but in males the OVCFcs are potentially accelerated and tend to involve multiple vertebra faster as in amOVCF. The older age (averaged 77.20 years old) at initial OVCF might contribute to the acceleration of OVCFcs in males, probably in part by reduced balance control and elevated fall risk with ageing [5, 7].
OVCF are often caused by low-energy spine trauma [5–7]. Our results showed that both OVCFcs and amOVCF reported higher ratio of no evident spine trauma than apparent and uncertain trauma, suggesting a facilitation of fragility fracture in multiple vertebra. As cement augmentation causes strain in adjacent vertebra and risks new OVCF [12, 13], the non-traumatic re-fractures in OVCFcs might be facilitated in part by the mechanical stress after repeated fractures and augmentation. Evidence accumulates that OVCF is related to fat infiltration of paravertebral muscles [21] and sagittal imbalance of spine [22, 23]. Increased paravertebral muscles degeneration [24] and kyphosis [25] after repeated OVCF might also facilitate the non-traumatic re-fractures in OVCFcs. It was previously reported that high-energy trauma such as traffic accidents, falling from a high place, and sliding frequently caused continuous multiple OVCF, whereas discontinuous multiple OVCF were often caused by mild outer force such as falling while walking, farm work, and lifting injury [19]. Here we found that as compared to OVCFcs with preexisting mechanical stress in spine, the ratio of apparent trauma such as falling and crush injury to the spine was higher in amOVCF. Although we were unable to determine whether the amOVCF occurred at same time after single apparent spine trauma or caused by multiple uncertain or undetectable spine trauma, the increased ratio of falling and crush injury suggested a role of trauma severity in the acceleration of OVCFcs as amOVCF. In addition to spine trauma, the contribution of paravertebral muscles degeneration and sagittal imbalance to amOVCF also deserves future prospective study.
Our study had several limitations. First, the design of retrospective study in single spine center would unavoidably yield bias in patient selection and data collection. 98 records (19.84%) of spine trauma were unavailable in the 494 fracture cascades of OVCFcs, failing to fully understand the role of trauma severity in promoting subsequent OVCF. Secondly, other factors related to vertebral fractures and re-fractures including bone mineral density [4, 15, 26, 27], osteoporosis medication [16, 28–30], and biochemical markers of bone turnover [31, 32] were not evaluated to identify the risk factors of OVCFcs and amOVCF. Thirdly, asymptomatic chronic vertebra compression was not included in OVCFcs, in which initial vertebral fractures and re-fractures might also include a portion of amOVCF. Prospective studies with stratified participants and long-term follow-up are warranted for a better understanding of the pattern of multiple vertebral involvement in fragility fractures.
Conclusions
amOVCF can be viewed as accelerated form of OVCFcs showing similar anatomical distribution and pattern of OVCF in spine. Both amOVCF and OVCFcs feature a facilitation of multiple fragility fractures without significant spine trauma.
Acknowledgements
The authors would like to acknowledge Ji-Yang Jin and Zhong-Jiang Wang, from the radiology department of Zhongda Hospital, for their aids in identifying lumbosacral transitional vertebra.
Abbreviations
- OVCF
Osteoporotic vertebral compression fractures
- OVCFcs
Osteoporotic vertebral compression fractures cascades
- amOVC
acute multiple osteoporotic vertebral compression fractures
Author contributions
All authors contributed to the study conception and design. Materials preparation, data collection and analysis were performed by FW and RS. The first draft of manuscript was written by FW and all authors commented on previous version of the manuscript.
Funding
This study was supported by the National Natural Science Foundation of China (No. 82372473), Jiangsu Commission of Health (M2022084), and Jiangsu Provincial Medical Key Discipline(Laboratory) Cultivation Unit (JSDW202222).
Data availability
No datasets were generated or analysed during the current study.
Declarations
Ethics approval and consent to participate
This study was approved by Ethic Committee for Clinical Research of Zhongda hospital affiliated to Southeast University (No.2022ZDSYLL016).
Consent for publication
The authors affirm that human research participant provided informed consent for publication of the images in Fig. 1.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
No datasets were generated or analysed during the current study.