Long-Term Posttraumatic Survival of Spinal Fracture Patients in Northern Finland

EPIDEMIOLOGY

Long-term Posttraumatic Survival of Spinal Fracture Patients in Northern Finland

Ville Niemi-Nikkola, BM,,y Nelli Saijets, BM,,y Henriikka Ylipoussu, BM,,y Pietari Kinnunen, MD, PhD,z Juha Pesa¨la¨,MD,z Pirkka Ma¨kela¨,MD,z Markku Alen, MD, PhD,,§ Mauri Kallinen, MD, PhD,,§ and Aki Vainionpa¨a¨, MD, PhD,§,{

age groups of 50 to 64 years and over 65 years, the most Study Design. A retrospective epidemiological study. important risk factors for death were males with hazard ratios of Objective. To reveal the long-term survival and causes of death 3.0 and 1.6, respectively, and low fall as trauma mechanism after traumatic spinal fracture (TSF) and to determine the with hazard ratios of 9.4 and 10.2, respectively. possible factors predicting death. Conclusion. Traumatic spinal fractures are associated with Summary of Background Data. Increased mortality follow- increased mortality compared with the general population, high ing osteoporotic spinal fracture has been represented in several mortality focusing especially on older people and men. The studies. Earlier studies concerning mortality after TSF have increase seems to be comparable to the increase following hip focused on specific types of fractures, or else only the mortality fracture. Patients who sustain spinal fracture due to falling need of the acute phases has been documented. In-hospital mortality special attention in care, due to the observation that low fall as has varied between 0.1% and 4.1%. Methods. The study sample of 947 patients including all trauma mechanism increased the risk of death significantly. Key words: cause of death, epidemiology, falling, long-term patients with TSF admitted to Oulu University Hospital, Finland, survival, mortality, spinal fracture, spinal injury, survival, between January 1, 2007 and December 31, 2011. TSFs were trauma, traumatic spinal fracture, vertebral fracture. identified using International Classification of Diseases 10th Level of Evidence: 3 revision or Nordic Classification of Surgical Procedures codes Spine 2018;43:1657–1663 and all patient records were manually reviewed. Times and causes of death, obtained from Statistics Finland’s Archive of Death Certificates, were available until the end 2016 and 2015, respectively. he annual incidence of traumatic spinal injury in Results. At the end of the follow-up 227 (24.0%) had died. Northern Finland has been documented to be 26/ Mortality was 6.8% after the first year and 19.1% after 5 years. 100,000, with 99.4% of patients sustaining a spinal T 1 Mortality was increased in all age groups compared with the fracture. Existing spinal injury is known to increase mor- general population, 1-year standardized mortality ratios ranging tality in trauma patients.2 The increased mortality following from 3.1 in over 65-year-olds to 19.8 in under 30-year-olds. In osteoporotic spinal fracture as well as after spinal cord injury has been represented in many studies. The standardized mortality ratio (SMR) after a spinal fracture has been From the Department of Medical Rehabilitation, Oulu University Hospital, documented to be between 2.4 and 2.5 for men and 1.7 and Oulu, Finland; yFaculty of Medicine, University of Oulu, Oulu, Finland; 3,4 z 1.9 for women. After spinal cord injury, SMR was 2.7 in a Division of Orthopaedic and Trauma Surgery, Department of Surgery, Oulu 5 University Hospital, Oulu, Finland; §Center for Life Course Epidemiology Finnish 30-year follow-up. Research, University of Oulu, Oulu, Finland; and {Department of Rehabili- Earlier studies about long-term mortality after traumatic tation, Seina¨joki Central Hospital, Seina¨joki, Finland. spinal fractures (TSFs) have focused on specific types of Acknowledgment date: March 8, 2018. Acceptance date: April 2, 2018. fracture, or else only the mortality of acute phases has been The manuscript submitted does not contain information about medical documented. Most studies cover only a specific age group, device(s)/ drug(s). commonly the elderly. In-hospital short-term mortality has The Northern Ostrobothnia Hospital District (State Research Funding; VTR) 6–9 funds were received in support of this work. varied between 0.1% and 4.1% in different studies. It has Relevant financial activities outside the submitted work: payment for been shown that long-term mortality after trauma is signifi- lecture, travel/accommodations/meeting expenses. cant, and must be taken into account when studying 10 Address correspondence and reprint requests to Ville Niemi-Nikkola, BM, mortality. Department of Medical Rehabilitation, Oulu University Hospital, P.O. Box Increased long-term mortality after severe trauma and 21, FI-90029 Oulu, Finland; E-mail: [email protected] hip fracture is well documented. However, knowledge DOI: 10.1097/BRS.0000000000002687 about long-term survival after TSF is limited. The aim of Spine www.spinejournal.com 1657 Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. EPIDEMIOLOGY Posttraumatic Survival of Spinal Fracture Patients in Finland Niemi-Nikkola et al the study was to reveal the long-term survival and causes of etiology was recorded according to ICD-10 external causes death after TSFs in Northern Finland and to determine the and grouped according to International Spinal Cord Society possible factors predicting death. (ISCoS) Core Dataset modified to differentiate low falls (<1 m) and high falls (>1m).12 Information of associated MATERIALS AND METHODS injuries was gathered according to ISCoS Core Dataset This is a retrospective study of TSFs admitted to Oulu definitions. As a modification, criteria of traumatic brain University Hospital (Oulu UH), Oulu, Finland. Oulu UH is injury were broadened to include cases with diagnostic the only tertiary level trauma center in its own hospital district findings in head computed tomography (CT) or magnetic (population 398 205 in 2011). In addition, Oulu UH is a resonance imaging (MRI) or cases with moderate to severe tertiary level referral center for four other central hospital traumatic brain injury diagnosed in neuropsychological districts (population in total 398,205þ339,475 ¼ 737,680 in testing afterward. Times and causes of deaths were 2011) for the rest of Northern Finland.11 obtained from Statistics Finland’s Archive of Death Certif- The study sample included patients suffering from TSF icates and annual population number, number of deaths, with date of injury between January 1, 2007 and December and death causes of the general population were obtained 31, 2011. Patient information was collected from the hos- from Official Statistics of Finland.13,14 The data acquisition pital care register including all inpatient and outpatient started in January 2014. Times of deaths from Statistics visits and surgical procedures. Traumatic spinal injuries Finland’s Archive of Death Certificates were available until were identified with International Classification of Diseases the end 2016 and causes of deaths until the end 2015, 10th revision (ICD-10) codes or Nordic Classification of providing a maximum and minimum follow up time of 9 Surgical Procedures (NCSP) codes. Study approval was and 5 years for mortality, respectively, and 4 years follow- obtained from Oulu University Hospital administration. up for causes of death. An ethics committee statement was not required for the The observed deaths during the first year after the frac- register study. ture were used in the calculation of SMRs. Expected deaths AnautomatedsearchwithICD-10andNCSPcodes were calculated using the average 1-year mortality accord- (Table 1) revealed 1884 hits with admission dates from ing to gender and age group in the general population of January 1, 2007 to April 31, 2012. Furthermore, an Northern Finland 2007–2011. SMRs were calculated for extended period in automated searchwasusedtoidentify the complete sample and for different age groups. To mini- those patients with delayed referral. After elimination of mize the effect of difference in age distribution of the general duplicates 1310 different patients were identified and population and the study sample, the SMR of the oldest age reviewed to assess eligibility and collect data (patient and group of over 65 years was age-adjusted, dividing it to injury characteristics, associated injuries and length of groups of 65 to 74 years, 75 to 84, and over 85 years stay). During the review, we excluded patients who did old. Student t test was used to analyze group differences not meet the inclusion criteria of TSF (e.g., osteoporotic in continuous and x2 test in categorical variables. Kaplan- fractures without evident trauma or traumatic spinal cord Meier curves were used to determine survival ratios and Cox injury without a fracture) or injury date. A total of 965 proportional hazard regression with forward stepwise patients met the criteria for TSF and after excluding 18 method to determine hazard ratios. SPSS version 23 foreigners (mortality data not available) the study sample (IBM, Armonk, NY) was used to perform all the statistical consisted of 947 patients. Injury characteristics and analyses. RESULTS TABLE 1. Diagnosis and Procedure Codes for Patient characteristics are represented in Table 2. At the end the Inclusion of Subject of the follow-up 227 (24.0%) of the 947 patients had died. ICD-10: traumatic ICD-10: Traumatic The mean age at death was 75.9 (SD 15.2). For men, the spine injuries spinal cord injuries NCSP mean age was 71.1 (SD 15.4, n ¼ 132) and for women 82.6 (SD 12.0, n ¼ 95) (P < 0.01). S12.0–9 S14.0 NAJ00 S13.0–3 S14.1 NAJ10 Survival S17.8–9 S24.0 NAJ12 The 1- and 5-year mortality rates were 6.8% and 19.1% S22.0–1 S24.1 NAJ20 overall, 7.4% and 19.3% for men, 5.8% and 18.8% for S23.0–2 S34.0 NAJ22 women, respectively. Survival in different age groups is S32.0–1 S34.1 NAJ30 represented in Figure 1, which shows that the mortality S32.7–8 T09.3 NAJ32 of over 65-year-olds seems to be at its highest during the first S33.0–1 T91.3 NAJ99 few months. Survival according to gender and fracture level M49.5 are represented in Figures 2 and 3. Patients with spinal cord M49.5 is in the ICD-10 classification and stands for Collapsed vertebra in diseases classified elsewhere. injury had high mortality: 12.8% in 3 months, 17.0% in the ICD-10 indicates International Classification of Diseases 10th revision; first year and 37.2% in 5 years. Compared with the general NCSP, Nordic Classification of Surgical Procedures. population of Northern Finland the excess mortality after

1658 www.spinejournal.com December 2018 Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. EPIDEMIOLOGY Posttraumatic Survival of Spinal Fracture Patients in Finland Niemi-Nikkola et al

TABLE 2. Patient Characteristics (95% CI 1.3–2.9) and after 2 years 1.5 (95% CI 0.9–2.4), indicating that mortality approaches the mortality of the TSF 2007-2011 general population 2 years after the injury. Hazard ratios for Number of cases 947 death in age groups 50 to 64 and over 65 years are repre- Gender; n (male)/n (female) 565/382 sented in Table 3. Age; mean SD 53 21.9 Invasive treatment; n (%) Causes of Death Spinal surgery 364 (38.4%) The most common causes of death in a 4-year follow-up were Vertebro-/kyphoplasty 40 (4.2%) circulatory diseases (54 patients, 36.7% of all deaths), acci- Level of injury; n (%) dents (32 patients, 21.8%) and neoplasms (20 patients, Cervical 279 (29.5%) 13.6%). Causes of death after TSFs compared with deaths Thoracic 176 (18.6%) in the general population are represented in Table 4. Lumbar 315 (33.3%) Accident or suicide was the cause of death for 32 patients Sacrum 62 (6.5%) (21.8%), and for these patients an ICD-10 diagnosis code was Cervical þ thoracic 41 (4.3%) recorded to describe the injury leading to death. The ICD-10 Cervical þ lumbar 5 (0.5%) code was a spinal injury code for 24 patients (16.3%), cervical Thoracic þ lumbar 64 (6.8%) in 19 cases and thoracolumbar in five. In addition, spinal Cervical þ thoracic þ 5 (0.5%) injury was a contributory death cause for 14 patients, cervical lumbar in 10 patients and thoracolumbar in four. This indicates that Spinal cord injury; n (%) 94 (9.9%) the spinal fracture was regarded as a significant factor in the Traumatic brain injury; n (%) 69 (7.3%) chain of death for these 38 patients (25.9% of the 147 patients Associated injury; n (%) 232 (24.5%) who had died after 4 years). The immediate death causes of SD indicates standard deviation. Associated injury includes intra-abdominal injury, lung injury, limb fracture and other remarkable injury excluding these 38 patients were pneumonia in 20 cases (52.6%), brain spinal cord and brain injury. injury due to lack of oxygen and myocardial infarction both in three cases (7.9%), respiratory distress syndrome and sepsis TSF was 0.9% both in age groups up to 29 years and 30 to both in two cases (5.3%) and interstitial lung disease in one 49 years, 4.0% in the 50 to 64 years group and 11.2% in the case (2.6%). Data were missing for seven patients. oldest age group over 65 years. Age adjusted 1-year SMR was 4.1 (95% CI 3.2–5.3). DISCUSSION According to age, the 1-year SMRs were 19.8 (95% CI 3.3– First-year mortality after TSF was 6.8% and after 5 years 65.4) in the age group up to 29 years, 5.9 (95% CI 0.98– mortality had risen to 19.1%. Traumatic spinal fracture 19.4) in the group 30 to 49 years, 7.2 (95% CI 3.8–12.5) in increased mortality in all age groups compared with the the group 50 to 64 years and 3.1 (95% CI 2.3–4.0) in the age general population. SMRs were age dependent and ranged group of over 65 years (age-adjusted). The SMRs of the from 3.1 in the elderly over 65 years to 19.8 in those under oldest age groups according to gender are represented in 30 years. Circulatory diseases, accidents and neoplasms Figure 4. We also calculated the age-adjusted 1-year SMRs were the most common death causes after 4 years. at different time points in the oldest age group: after 0.5 In the literature, there are only limited data comparable years the SMR was 2.3 (95% CI 1.6–3.2), after 1 year 1.9 to our study concerning long-term mortality after TSF.

100

40 Survival (%) 0-29 years 30-49 years 20 50-64 years 65- years

Figure 1. Survival after traumatic spinal fracture in differ- 0 1 2 3 4 5 ent age groups. Time (years)

Spine www.spinejournal.com 1659 Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. EPIDEMIOLOGY Posttraumatic Survival of Spinal Fracture Patients in Finland Niemi-Nikkola et al

100

40 Survival (%)

20 Female Male

0 0 1 2 3 4 5 Time (years) Figure 2. Survival after traumatic spinal fracture according to gender.

Most of the earlier data deals with mortality after osteopo- our 1-year SMRs in over 50-year-olds for isolated thora- rotic spinal fractures.3,4,15 SMRswere1.7to1.8in columbar fractures were 3.3 and 2.9 in men and women and 2.4 in men for the first 5 years after osteoporotic women, respectively. spinal fracture resulting from low-energy trauma in The risk for death in the first year after TSF is quite two prospective studies with the same Australian cohort.3,4 similar as after a hip fracture. A meta-analysis of prospective In South Korea, the 1-year mortality rate and 1-year cohort studies revealed a 1-year pooled risk for death of 2.9 SMRs after spinal fracture in the over 50-year-olds were for women and 3.7 for men after hip fracture.17 In a study 14.6% and 3.5 in men and 7.2% and 2.5 in women.16 The combining eight cohorts from the USA and Europe, 1-year study included only thoracolumbar fractures but no dis- SMR was 2.8 in over 60 years old.18 The results are in the tinction was made between low and high energy fractures. If same level with the SMRs of 2.2 for women and 3.8 for men the two oldest age groups of our study population are in the elderly over 65 years. In Canada, a study comparing combined, the 1-year mortality ratios after thoracolumbar mortality after different fractures in people over 50 years fractures are 8.5% for men and 9.0% for women, showing showed that only vertebral and hip fractures increased that the mortality was lower in men and higher in women in mortality in follow-up.19 It may be that the increase in our study than in South Korea. SMRs in our study popula- mortality, in both TSF and hip fracture patients, results tion were comparable to the results from South Korea, as from the same factors, such as age, morbidity and frailty,

100

40 Survival (%) Cervical Thoracic 20 Lumbar Sacral

0 1 2 3 4 5 Time (years) Figure 3. Survival after traumatic spinal fracture according to the highest fractured level.

1660 www.spinejournal.com December 2018 Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. EPIDEMIOLOGY Posttraumatic Survival of Spinal Fracture Patients in Finland Niemi-Nikkola et al

Figure 4. One-year standardized mortality ratio (SMR) and their 95% confidence intervals according to gender in the two oldest age groups.

leading to prolonged confinement to bed and a decrease in with higher mortality in follow up in the two age groups health condition after the fracture. Both types of injuries over 50 years. Low fall has also previously been shown to be often decrease the functional capacity and mobility of a risk factor for death in elderly trauma patients.10,22 The the patient. significance of this finding is emphasized by the fact that low Low fall induced deaths in people over 50 years has been fall is also the most common trauma mechanism of TSF in increasing remarkably over the past decades in Finland.20,21 the elderly.1 One reason behind this may be that the health In our study, low fall as a trauma mechanism was correlated of people who sustain a severe injury due to a low energy trauma mechanism may be worse than their counterparts. Previously, low fall induced injuries have been suggested as a TABLE 3. Hazard Ratios for Death and Their frailty marker and the frailty could explain the increased 22 95% Confidence Intervals in the mortality after low falls. Two Oldest Age Groups The risk of death was increased more in males than females in age groups of 50 to 64 years and over 65 years. Age Group HR 95% CI P The higher mortality of men has been represented in several studies of osteoporotic fractures but also in a study with a 50 to 64 years (n ¼ 206) < study sample of both low and high energy trauma mecha- Male 2.97 1.35–6.51 0.01 3,4,16 Mechanism of injury nisms. One study showed that the effect of age on Road traffic 1 (ref.) mortality after trauma begins at 55 for men and 70 for < women, which might be one of the explanations for the Low fall 9.39 3.10–28.46 0.01 22 High fall 2.15 0.66–7.04 0.21 gender difference. Associated injury 2.70 1.31–5.56 <0.01 Traumatic spinal injury was regarded as a significant Over 65 years (n ¼ 306) factor for one-fourth of the patients who died in the first Male 1.63 1.18–2.25 <0.01 4 years, most of which were cervical level injuries. Also, Mechanism of injury cervical fractures had higher mortality compared with thor- High fall 1 (ref.) acolumbar fractures in our study. Both these findings indi- Low fall 10.18 3.74–27.70 <0.01 cate that cervical injuries are often more severe, and the Road traffic 4.01 1.34–12.01 0.01 injury itself is fatal more often. Previously it has been shown Spinal cord injury 1.83 1.16–2.89 <0.01 that fatal cervical injuries have been increasing in Finland 23 Patients with violence, sports, other, or unknown as a trauma mechanism over the last decades. A Swedish study suggested that 28% were excluded from the analysis in both groups (n ¼ 28 in 50–64 years; of deaths after spinal fracture may be related to the fracture n ¼ 12 in over 65 years). Covariates used in analysis: gender, mechanism of injury, fracture level, spinal cord injury, brain injury, associated injury itself, which is on a par with our findings concerning the 24 (intra-abdominal injury, lung injury, limb fracture, and other remarkable cause of death. Cervical fractures alone are not sufficient injury excluding spinal cord and brain injury). to explain the increased mortality and further studies are CI indicates confidence interval; HR, hazard ratio. needed to explain the excess mortality. As previously stated, Spine www.spinejournal.com 1661 Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. EPIDEMIOLOGY Posttraumatic Survival of Spinal Fracture Patients in Finland Niemi-Nikkola et al

TABLE 4. Causes of Death in a 4-Year Follow- up After Traumatic Spinal Fracture Key Points Compared With the general population of Northern Finland The mortality after TSF was 6.8% after the first year and 19.1% after 5 years. Cause of Death Number of Patients (%) P SMRs ranged from 3.1 in over 65-years-olds to Spinal Frac- General 19.8 in under 30-years-old ture Patients Population The most important risk factors for death were Disease of the 54 (36.7%) 13 344 (41.0%) 0.30 males and low fall as trauma mechanism. circulatory Among elderly, the increase in mortality seems to system be comparable to the increase following Accident 32 (21.8%) 1765 (5.4%) <0.01 hip fracture. Cancer or tumor 20 (13.6%) 7352 (22.6%) <0.01 Patients who sustain spinal fracture due to falling Dementia, 11 (7.5%) 3596 (11.0%) 0.17 need special attention in care. Alzheimer disease Alcohol related 10 (6.8%) 1218 (3.7%) 0.05 diseases Acknowledgments Suicide 5 (3.4%) 725 (2.2%) 0.34 The authors thank Dr John Braidwood, PhD, for language Disease of the 4 (2.7%) 840 (2.6%) 0.91 digestive system revision and Mr Pasi Ohtonen, MSc, for statistical Other disease of 3 (2%) 769 (2.4%) 0.80 assistance. the nervous system Diabetes 3 (2%) 377 (1.2%) 0.32 References 1. Niemi-Nikkola V, Saijets N, Ylipoussu H, et al. Traumatic spinal Disease of the 2 (1.4%) 1378 (4.2%) 0.08 injuries in Northern Finland. Spine (Phila Pa 1976) 2018;43: respiratory E51–E51. system 2. Akmal M, Trivedi R, Sutcliffe J. Functional outcome in trauma Other 3 (2.0%) 1197 (3.7%) 0.29 patients with spinal injury. Spine (Phila Pa 1976) 2003;28:180–5. Total 147 (100%) 32 561 (100%) 3. Center JR, Nguyen TV, Schneider D, et al. Mortality after all major types of osteoporotic fracture in men and women: An observa- General population. All deaths 2007–2011 in the population of Northern tional study. Lancet 1999;353:878–82. Finland. Alcohol-related diseases include accidental poisoning by alcohol. 4. Bliuc D, Nguyen ND, Milch VE, et al. Mortality risk associated with low-trauma osteoporotic fracture and subsequent fracture in men and women. JAMA 2009;301:513–21. low fall was found to be a significant risk factor for death, 5. Ahoniemi E, Pohjolainen T, Kautiainen H. Survival after spinal and frailty could explain the increased mortality. Also, cord injury in Finland. J Rehabil Med 2011;43:481–5. decreased mobility and other consequences of the fracture 6. Williams BJ, Smith JS, Saulle D, et al. Complications associated may partly explain the mortality. with surgical treatment of traumatic spinal fractures: a review of the Scoliosis Research Society morbidity and mortality database. A retrospective study design has its own limitations. World Neurosurg 2014;81:818–24. However, the Finnish Hospital discharge register has proved 7. Hu R, Mustard CA, Burns C. Epidemiology of incident spinal to be reliable.25 In addition, all medical records were man- fracture in a complete population. Spine (Phila Pa 1976) 1996; ually reviewed by the researchers. Statistics Finland’s 21:492–9. 8. Kattail D, Furlan JC, Fehlings MG. Epidemiology and clinical Archive of Death Certificates covers the persons who have outcomes of acute spine trauma and spinal cord injury: Experience died in Finland or abroad and who at the time of death were from a specialized spine trauma center in Canada in comparison domiciled in Finland.14 The correlation between spinal with a large national registry. J Trauma 2009;67:936–43. 9. Wang H, Zhang Y, Xiang Q, et al. Epidemiology of traumatic fracture and death may not be causal because, as previously spinal fractures: Experience from medical university-affiliated stated, the elderly who fall tend to be more fragile and in a hospitals in Chongqing, China, 2001-2010. J Neurosurg Spine poorer medical condition. We did not have access to the 2012;17:459–68. information about the previous health condition of the 10. Davidson GH, Hamlat CA, Rivara FP, et al. Long-term survival of adult trauma patients. JAMA 2011;305:1001–7. patients, which could have had a causal relationship 11. Official Statistics of Finland (OSF): Population structure [e-publi- to mortality. cation]. ISSN U 1797-5395. Helsinki: Statistics Finland. Traumatic spinal fractures are associated with increased Available at: http://www.stat.fi/til/vaerak/index_en.html. Accessed mortality as compared to the general population, with high November 14, 2016. 12. DeVivo M, Biering-Sorensen F, Charlifue S, et al., Executive mortality focusing especially on older people and men. It Committee for the International SCI Data Sets Committees. Inter- seems that the increase in mortality after TSF is comparable national Spinal Cord Injury Core Data Set. Spinal Cord 2006; to the increase after hip fracture. Patients who sustain a 44:535–40. U spinal fracture due to falling need special attention in care, 13. Official Statistics of Finland (OSF): Deaths [e-publication]. ISSN 1798-2545. Helsinki: Statistics Finland. Available at: Access as low fall as trauma mechanism increased the risk of death method: http://www.stat.fi/til/kuol/index_en.html. Accessed significantly. November 14, 2016.

1662 www.spinejournal.com December 2018 Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. EPIDEMIOLOGY Posttraumatic Survival of Spinal Fracture Patients in Finland Niemi-Nikkola et al

14. Official Statistics of Finland (OSF): Causes of death [e-publication]. 19. Ioannidis G, Papaioannou A, Hopman WM, et al. Relation ISSN U 1799-5078. Helsinki: Statistics Finland. Available at: http:// between fractures and mortality: results from the Canadian multi- www.stat.fi/til/ksyyt/meta_en.html. Accessed January 25, 2018. centre osteoporosis study. CMAJ 2009;181:265–71. 15. Hasserius R, Karlsson MK, Nilsson BE, et al., European Vertebral 20. Korhonen N, Kannus P, Niemi S, et al. Fall-induced deaths among Osteoporosis Study. Prevalent vertebral deformities predict older adults: nationwide statistics in Finland between 1971 and increased mortality and increased fracture rate in both men and 2009 and prediction for the future. Injury 2013;44:867–71. women: a 10-year population-based study of 598 individuals from 21. Kannus P, Parkkari J, Niemi S, et al. Fall-induced deaths among the Swedish cohort in the European Vertebral Osteoporosis Study. elderly people. Am J Public Health 2004;95:422–4. Osteoporos Int 2003;14:61–8. 22. Wong TH, Nguyen HV, Chiu MT, et al. The low fall as a surrogate 16. Lee YK, Jang S, Jang S, et al. Mortality after vertebral fracture in marker of frailty predicts long-term mortality in older trauma Korea: analysis of the National Claim Registry. Osteoporosis Int patients. PLoS One 2015;10:e0137127. 2012;23:1859–65. 23. Thesleff T, Niskakangas T, Luoto TM, et al. Fatal cervical spine 17. Haentjens P, Magaziner J, Colon-Emeric CS, et al. Meta-analysis: injuries: a Finnish nationwide register-based epidemiologic study excess mortality after hip fracture among older women and men. on data from 1987 to 2010. Spine J 2016;16:918–26. Ann Intern Med 2010;152:380–90. 24. Kanis JA, Oden A, Johnell O, et al. Excess mortality after hospital- 18. Katsoulis M, Benetou V, Karapetyan T, et al. Excess mortality after isation for vertebral fracture. Osteoporos Int 2004;15:108–12. hip fracture in elderly persons from Europe and the USA: the 25. Sund R. Quality of the Finnish Hospital Discharge Register: a CHANCES project. J Intern Med 2017;281:300–10. systematic review. Scand J Public Health 2012;40:505–15.