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Association of lumbar fractures, abdominal aortic calcification, and osteopenia
Clinical Imaging xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Clinical Imaging journal homepage: http://www.clinicalimaging.org
Original Article
Association of lumbar fractures, abdominal aortic calcification, and osteopenia☆ Tarek N. Hanna a,⁎, Matthew E. Zygmont a, Elie Harmouche b, Ninad Salastekar c, Jamlik-Omari Johnson a, Faisal Khosa a,1 a b c
Division of Emergency Radiology, Department of Radiology and Imaging Sciences, Emory University School of Medicine, Atlanta, GA Division of Musculoskeletal Radiology, Department of Radiology and Imaging Sciences, Emory University School of Medicine, Atlanta, GA Rollins School of Public Health, Emory University, Atlanta, GA
a r t i c l e
i n f o
Article history: Received 24 September 2014 Received in revised form 11 November 2014 Accepted 30 November 2014 Available online xxxx Keywords: Osteoporosis Emergency department Aortic calcifications Lumbar spine Vertebral fracture
a b s t r a c t Purpose: The purpose was to assess if abdominal aortic calcification (AAC) and low bone mineral density (BMD) are associated with fractures on lumbar spine radiographs in trauma patients. Methods: Retrospectively, 303 consecutive lumbar radiographs were independently reviewed by two radiologists for AAC, low BMD, and traumatic findings. Results: Thirty-one percent of patients had low BMD, 34% had AAC, and 24% had both. Eleven percent of radiographs showed traumatic findings. Seventy-six percent of positive cases had low BMD (Pb .001), and 64% had AAC (Pb.001). Conclusion: A higher index of suspicion for fractures is warranted when AAC and low BMD are present.
© 2014 Elsevier Inc. All rights reserved.
1. Introduction There is a long-established association between low bone mineral density (BMD) and fragility fractures. More recently, studies have shown that abdominal aortic calcification (AAC) has an association with vertebral fractures [1–7]. In a prior study by Szulc et al., the severity of aortic calcification was associated with a higher prevalence and number of vertebral fractures even after adjusting for BMD and other confounding variables [3]. AAC is an important marker of overall atherosclerotic burden [1,8,9] and readily identifiable on radiographs. Similarly, radiologists are able to subjectively identify low BMD on lumbar spine radiographs, which is a strong predictor of osteopenia or osteoporosis [10–13]. The association of AAC with low BMD has been documented in a variety of populations [1,2,8,14,15], and there is evidence that women with the most severe AAC demonstrate the greatest magnitude of bone loss after controlling for age and other confounding variables [14]. Although AAC and low BMD are radiologic ☆ Disclosure: Dr. Khosa is the American Roentgen Ray Society Scholar (2013–2015). No financial disclosures or conflict of interest on behalf of the authors. There was no commercial funding for this study. The authors have full control over all the data. The study will not be published elsewhere in any language without the consent of the copyright owners. ⁎ Corresponding author. Division of Emergency Radiology, Department of Radiology and Imaging Sciences, Emory University Midtown Hospital, 550 Peachtree Road, Atlanta GA 30308. Fax: +1 404 686 5709. E-mail address: [email protected] (T.N. Hanna). 1 Dr. Khosa is at the American Roentgen Ray Society Scholar (2013–2015).
diagnoses, a preponderance of the literature on the significance of these findings in the trauma setting is nonradiological. It is unclear how often radiologists document these findings, which may be dismissed as incidental. To our knowledge, the association between AAC, low BMD, and vertebral fractures as assessed by lumbar spine radiographs has not been explored in the acute setting. In addition to exploring the association of these three variables in emergency department (ED) trauma patients, we analyzed the original radiology reports to see how frequently these findings are being documented for clinicians. Could the identification and understanding of AAC and low BMD make radiologists more accurate at detecting lumbar fractures? 2. Materials and methods This retrospective investigation was conducted with institutional review board approval and was compliant with the Health Insurance Portability and Accountability Act. The requirement for written informed consent was waived because of the retrospective nature of the investigation. 2.1. Study population Our investigation was conducted at two university-affiliated teaching hospitals, which are both level 2 trauma centers. Our initial cohort included 844 consecutive ED patients receiving a standard three-view lumbosacral spine radiographic series from February 2011 to February
http://dx.doi.org/10.1016/j.clinimag.2014.11.021 0899-7071/© 2014 Elsevier Inc. All rights reserved.
Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021
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T.N. Hanna et al. / Clinical Imaging xxx (2014) xxx–xxx
2014. An initial power analysis suggested the necessary sample size for statistical significance, which determined the length of this time period. We defined the standard views as anteroposterior, lateral, and conedlateral views. Patients were included if there was a history of trauma within 48 h prior to presentation. Patients were excluded if they had less than three views, history of trauma or back pain for more than 48 h, history of known prior lumbar spinal surgery, or incomplete documentation related to current visit. These criteria yielded 315 patients. Age, gender, mechanism of injury, impact velocity, and follow-up imaging results done within 1 month were recorded through chart review. High-impact injury was defined as any motorized vehicle collision, falls from a height above 1 m or more than five stairs, crush injuries, or pedestrian versus automobile accidents. Low-impact injury was defined as ground-level fall, assault, or if the patient was found on the ground. Of the 315 cases, 12 were excluded during radiographic review, as three-view lumbar spine images were not available in the picture archiving and communication system for these patients, yielding a final cohort of 303 examinations. 2.2. Lumbar spine radiograph review Examinations that met study inclusion criteria were reviewed by two board-certified fellowship-trained radiologists (musculoskeletal radiology and neuroradiology). During radiographic review, no patient demographic information was displayed on the images. The reviewers were blinded to the original radiology report. Data were collected via a standard electronic data entry form. Bone mineralization was subjectively characterized by the radiologist as normal or decreased. This BMD assessment was not standardized or objective; rather, it was an observational data point of clinical practice based on previously published literature that a radiological report of low BMD is a strong predictor of osteopenia or osteoporosis [10–13]. The presence or absence of AAC was recorded. The examinations were interpreted for the presence and location of fractures. All discrepancies between the two primary reviewers were adjudicated by a third board-certified fellowship-trained radiologist (neuroradiology and emergency radiology). With regard to fractures, findings were also compared with follow-up imaging including computed tomography (CT) or magnetic resonance (MR) when available. 2.2.1. Report review Original radiology reports were screened for documentation of AAC and low BMD. In this assessment for AAC, any mention of aortic calcification, aortic atherosclerosis, or prevertebral vascular calcifications was included. Similarly, in assessing the radiology reports for low BMD, any mention of osteopenia, osteoporosis, low BMD, bone demineralization, or other synonymous descriptors was included. Following the radiograph review, the reports for those cases, which were documented as traumatic, were reviewed to see if the original radiology report documented the traumatic findings. 2.3. Statistical analysis Continuous variables were expressed as mean±standard deviation, and categorical variables were expressed as frequency n (%). Age was categorized into four categories—less than or equal to 50 years, 51–65 years, 66–80 years, and greater than 80 years—for the purpose of this analysis. Comparison between levels of categorical variables was carried out using Fisher’s Exact Test. Odds ratios with 95% confidence interval (CI) were reported using multivariate logistic analyses to estimate the association of the presence of aortic calcification with the presence of low BMD, adjusting for patient age, gender, and velocity of impact. Collinearity and interaction were assessed. Also, confounding was said to be present if the estimate for the effect of osteopenia changed by more than 10% after dropping the confounder (age, gender). Cohen’s kappa (unweighted) was used to assess interobserver agreement
among the reviewing radiologists for low BMD and AAC. Significance was assessed at two-sided α error of 0.05. All analyses were carried out using SAS 9.3 (SAS Institute Inc., Cary, NC, USA). 3. Results Table 1 summarizes the distribution of demographic and clinical variables in the 303 patients comprising the study population. The mean age of study participants was 53±22 years. Fifty-three percent of the patients were less than 50 years of age, and 67% were women. Based on the clinical history, 58% patients were categorized as having suffered trauma with a low-velocity of impact. Our population demographics differ from the typical trauma population in that patients are older and more likely to be female, which may represent an inherent modality selection bias, as trauma patients imaged by radiographs are older and more likely to have suffered lower-impact trauma. Based on radiographic review, low BMD was present in 31% (n=95/303) of the patients. AAC was present in 34% (n=103/303) of the study population. There was a high degree of radiologist agreement for both low BMD and AAC, with Cohen’s kappa (unweighted) of 0.75 (0.64–0.86) and 0.86 (0.75–0.97) respectively. AAC was present in 76% of patients with low BMD as compared to just 15% of patients with normal BMD (Pb.001). The percentage of patients with AAC increased with increasing age and was present in 91% of patients above 80 years of age. The difference in the proportion of patients with AAC among men and women was not statistically significant (P= .156). An analysis of the distribution of demographic and clinical variables categorized by the presence or absence of AAC is presented in Table 2. Multivariate logistic analyses revealed that the association between AAC and low BMD was not significant after adjusting for patient age, gender, and velocity of impact (Table 3). Age and velocity of impact were, however, were associated with AAC (Pb .001 and P=.046 respectively). The odds for the presence of AAC in the age groups of 51–65, 66–80, and N 80 years were 17, 63, and 135 times greater than those for patients less than or equal to 50 years of age. The age-adjusted odds for the presence of AAC in patients who suffered low-impact trauma were 2.4 times greater than those in patients with highimpact trauma. Gender neither was significantly associated with the presence of AAC nor was a significant confounder. Hence, gender was excluded from the model before calculating the adjusted estimates. Of the 303 cases, 11% (n= 33) were considered to have traumatic findings based on lumbar spine radiographs (“positive-trauma” cases). Distribution of variables categorized by the presence and absence of radiographic traumatic findings is shown in Table 4. Trauma was correlated with age (Pb.001) and also with low-impact velocity (Pb.001). In 76% (n= 25/33) of positive-trauma cases, low BMD was present Table 1 Distribution of demographic and clinical variables in the study population (n=303) N (%) Age ≤50 years 51–65 years 66–80 years N80 years Gender Male Female No. of traumatic cases Velocity of impact High impact Low impact Osteopenia/low BMD Absent Present Aortic calcification Absent Present
162 (53) 55 (18) 32 (11) 54 (18) 99 (33) 203 (67) 33 (11) 126 (42) 176 (58) 208 (69) 95 (31) 200 (66) 103 (34)
Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021
T.N. Hanna et al. / Clinical Imaging xxx (2014) xxx–xxx Table 2 Distribution of demographic and clinical variables categorized by presence/absence of aortic calcification (n=303)
Table 4 Distribution of variables categorized by the presence and absence of radiographic trauma Trauma n (%)
Aortic calcification n (%)
Age ≤50 years 51–65 years 66–80 years N80 years Gender Male Female Velocity of impact High impact Low impact Osteopenia/low BMD Absent Present
Present
Absent
P value
5 (3) 24 (44) 25 (78) 49 (91)
157 (97) 31 (56) 7 (22) 5 (9)
b.001
28 (28) 75 (37)
71 (72) 128 (63)
.156
13 (10) 90 (51)
113 (90) 86 (49)
b.001
31 (15) 72 (76)
177 (85) 23 (24)
b.001
(Pb.001). In 64% (n=21/33) of positive-trauma cases, AAC was present (Pb.001). The vast majority of positive-trauma cases (88%, n=28) were wedge compression fractures, and the majority (76%, n= 25/33) of positive-trauma examinations had only one traumatic finding. There were five patients with two traumatic findings (2%), two patients with three traumatic findings (1%), and one patient with four traumatic findings (0.3%). The remaining positive-trauma cases consisted of bursttype vertebral body fracture (2%, n= 1), transverse process fractures (2%, n=1), sacral fracture (2%, n=1), and possible acute ligamentous/ disc injury (2%, n=1). Only 5 of these 33 cases proceeded to advanced imaging, which confirmed the radiographic findings; the majority of the remaining patients were treated supportively with analgesics and discharged, or admitted for reasons unrelated to lumbar spine trauma. Of note, all of these 33 “positive-trauma” cases had documented acute back pain corresponding to the time since trauma. Of the 33 positive-trauma cases, 26 were initially consensus positivetrauma by two independent readers. A third reader adjudicated seven cases. Compared to the original radiology report, 3 of the 33 positivetrauma findings were not described as traumatic by the original radiologist. Notably, the three discrepant cases were part of the seven that went to tiebreak reads in our review. All three were age-indeterminate wedging compression fractures, which were not originally mentioned. Two patients had routine supportive care with analgesics, and follow-up to 15 months documented no advanced imaging or issues related to these fractures. One patient was a metastatic cancer patient and had multiple follow-ups and multiple progressive pathologic compressions. Of the three discrepant trauma cases, two had both AAC and low BMD, while one had only AAC. Of the three original reports, one did not describe AAC, while the others were accurate in this regard. Only 46% of the patients categorized as having AAC during our review had this finding mentioned in their original report (Table 5). Table 3 Estimate of the association of aortic calcification with osteopenia, adjusted for patient age and velocity of trauma (n=303)
Age ≤50 years 51–65 years 66–80 years N80 years Velocity of impact High impact Low impact Osteopenia/low BMD Absent Present
Odds ratio for the presence of aortic calcification (95% CI)
P value
1 17.06 (5.70–51.08) 63.15 (16.85–236.74) 135.91 (32.54–567.61)
Reference b.001 b.001 b.001
1 2.43 (1.02–5.82)
Reference .046
1 1.71 (0.732–4.02)
Reference .214
3
Age ≤50 years 51–65 years 66–80 years N80 years Gender Male Female Velocity of impact High impact Low impact Osteopenia/low BMD Absent Present Aortic calcification Absent Present
Present
Absent
P value
4 (2) 7 (13) 3 (9) 19 (35)
158 (98) 48 (87) 29 (91) 35 (65)
b.001
8 (8) 25 (12)
91 (92) 178 (88)
.328
5 (4) 28 (16)
121 (96) 148 (84)
.001
8 (4) 25 (26)
200 (96) 70 (74)
b.001
12 (6) 21 (20)
188 (94) 82 (80)
b.001
Similarly, only 36% of patients with low BMD had this finding stated in the original radiology report (Table 6). The initial reports were generated in an emergency radiology division with a 24/7/365 coverage. A review of the 12 excluded cases demonstrated that 4 patients could not complete the examination due to pain, inability to position, or refusal to continue with imaging. The remaining eight cases did not have any documentation to explain missing images or incomplete examination. Importantly, two of the cases without documentation showed traumatic findings by lateral lumbar spine radiographs (the only view obtained): an L4 burst fracture and an L1 compression fracture, respectively. Both these patients proceeded immediately to CT and MR, respectively, which confirmed acute fractures.
4. Discussion Our study supports that ED trauma patients with AAC and low BMD are more likely to have vertebral fractures on lumbar spine radiographs. Although severity of AAC has been shown to be an independent predictor of hip fractures [4,16,17], the literature on association between AAC and vertebral fractures is complex and occasionally conflicting [1–7,17,18]. This is explained by the wide variety of patient populations and various techniques used in identification of AAC and low BMD [1–7,16–19]. Important population attributes that influence this association appear to be gender [3,7,8,14,18], population age [3], postmenopausal women [7,18], study size [3], overall burden of cardiovascular pathology in the population examined [3,19], and ethnicity [1,8,9]. In addition to these population differences, study design and techniques employed in prior studies vary widely, with AAC being assessed quantitatively versus subjectively [5,7,18] and low BMD being measured by dual X-ray absorptiometry (DXA), radiographic criteria, or metacarpal cortical area [14,18]. Here we chose to focus on factors that can be readily assessed by the clinical radiologist during routine reading of lumbar spine radiographs, without allocation of additional resources or extra time commitment. Table 5 If present, was aortic calcification mentioned in the original radiology report? (n=303) Mentioned in the original report Aortic calcification
Yes
No
Present Absent
47 1 48
56 199 255
103 200
Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021
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Table 6 If present, was subjective low BMD mentioned in the original radiology report? (n=303) Mentioned in the original report Low BMD
Yes
No
Present Absent
35 4 38
61 203 264
96 207
As expected, age was directly correlated to the incidence of aortic calcifications, and the odds ratio for patients greater than 80 years of age was 135 times greater than for patients less than or equal to 50 years of age. There was an association between AAC and low BMD, but this was not significant after adjusting for age. This may be secondary to the age of our population (53±22 years) and the relative paucity of aortic calcifications in younger patients. In the longitudinal study by Kiel et al., an initial cross-sectional analysis done with an average age of approximately 54 years was unable to show a significant independent relationship between aortic calcification and metacarpal cortical bone volume [14]. However, at the termination of that 25-year followup study, there was a significant association between these variables in women independent of age, supporting the fact that an older population is necessary to achieve significance in this assessment [14]. Zhou et al. recently demonstrated that severe AAC was associated with a threefold greater risk of vertebral fractures in Asian postmenopausal women using lateral lumbar spine radiographs [7]. El Maghraoui et al. showed that severe AAC was associated with increased fracture prevalence in postmenopausal Caucasian women independent of age and BMD in a study utilizing DXA [18]. Both of these studies used a semiquantitative method of classifying AAC, which was described by Kauppila et al. [20]. Our ED population was not as homogenous or as old as most prior study populations, and our assessment of AAC was binary. The clinical radiologist can easily classify patients into four groups based on lumbar spine radiographs via our binary methods: negative AAC and normal BMD (58%, n= 177), positive AAC and normal BMD (10%, n= 31), negative AAC and low BMD (8%, n= 23), and positive AAC and low BMD (24%, n= 72). This last group (positive AAC, low BMD) made up approximately one quarter of ED patients who received lumbar spine radiographs in our study and is at greater risk for lumbar spine traumatic injury. There is a well-known relationship between low BMD and fractures, and data independently connect AAC to increased fracture incidence [1–7,17,18]. In our study, the preponderance of trauma patients was in this quartile. Interestingly, the odds ratio for the presence of AAC in those with low-impact trauma was 2.4 times greater than in those patients with high-impact trauma independent of age (multivariate logistic model, adjusted for age and gender). To our knowledge, this association has never been previously reported. We theorize that this is related to a combination of ED physician imaging practices and self-selection for ED visits following low-impact trauma. Specifically, healthy patients with no preexisting conditions who suffer low-impact trauma may be less likely to visit the ED and, even if they do visit the ED, less likely to undergo imaging. Those with chronic disease may be more likely to undergo imaging following low-impact trauma and also more likely to have AAC. This is an important observation because low-impact trauma can cause nondisplaced fractures, particularly in the hip and spine, which may be harder to detect by plain radiographs. In this series of trauma patients, the radiologist did not routinely document the presence of AAC or low BMD in their final report. We presume this is because emergency radiologists in the setting of trauma dismiss these findings as incidental, and may not be aware of the importance of AAC and its independent association with osteoporosis and fractures. In an ED patient who may not have prior workup or known risk factors, documenting AAC is important since it predicts an increased incidence of cardiovascular events [21]. Additionally, the subjective
reporting of low BMD by the radiologist may be the first knowledge of possible osteoporosis and may prompt additional workup. This association can also be used as a teaching tool for residents, encouraging them to raise their level of suspicion for fractures in patients with AAC and low BMD. Overall, we suggest that radiologists be more alert to trauma in subgroups of patients with AAC and low BMD. Our study had limitations. Initially, 315 consecutive lumbar spine examinations were identified, but 12 were excluded due to missing images and incomplete examinations. We specifically note the exclusion of these cases because two of these patients had vertebral fractures. In evaluating AAC, we used a binary approach (present or absent) rather than characterizing magnitude or severity of calcification. We did this to create an analysis that could be easily utilized by radiologists in the clinical setting. The acuity of radiographic findings was not routinely confirmed by advanced imaging, but lumbar radiographs often describe age-indeterminate findings that require clinical correlation for point tenderness. We note that two of the three originally missed fractures were cases with both AAC and low BMD, while the third had AAC only. This suggests that greater attention to cases with AAC and low BMD could improve fracture detection. However, this study did not have the data to conclude that radiologists who report AAC and low BMD have better accuracy in fracture diagnosis. Given that AAC and BMD are not independent variables, to truly test the independent effect of these on fractures, we would have had to interpret the images while covering the aorta, so AAC was not visible. Finally, we did have an objective test to confirm low BMD. However, we note that previous studies have concluded that subjective radiological report of low BMD is a strong predictor of osteopenia or osteoporosis; we are not attempting to duplicate this work. 5. Conclusion A higher index of suspicion for lumbar fractures is warranted in the subgroup of patients with AAC and low BMD. Additionally, AAC and low BMD may reveal clinically relevant information about overall patient health. Our study shows that radiologists do not routinely document these findings in the acute setting.
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Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021
T.N. Hanna et al. / Clinical Imaging xxx (2014) xxx–xxx [12] Michel BA, Lane NE, Jones HH, Fries JF, Bloch DA. Plain radiographs can be useful in estimating lumbar bone density. J Rheumatol 1990;17:528–31. [13] Garton MJ, Robertson EM, Gilbert FJ, Gomersall L, Reid DM. Can radiologists detect osteopenia on plain radiographs? Clin Radiol 1994;49:118–22. [14] Kiel DP, Kauppila LI, Cupples LA, Hannan MT, O’Donnell CJ, Wilson PWF. Bone loss and the progression of abdominal aortic calcification over a 25 year period: the Framingham Heart Study. Calcif Tissue Int 2001;68:271–6. [15] Pennisi P, Signorelli SS, Riccobene S, Celotta G, Di Pino L, La Malfa T, et al. Low bone density and abnormal bone turnover in patients with atherosclerosis of peripheral vessels. Osteoporos Int 2004;15:389–95. [16] Collins TC, Ewing SK, Diem SJ, Taylor BC, Orwoll ES, Cummings SR, et al. Peripheral arterial disease is associated with higher rates of hip bone loss and increased fracture risk in older men. Circulation 2009;119:2305–12.
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[17] Wang TK, Bolland MJ, Pelt NC, Horne AM, Mason BH, Ames RW, et al. Relationships between calcium metabolism, bone density, and fractures. J Bone Miner Res 2010; 25:2501–9. [18] El Maghraoui A, Rezqui A, Mounach A, Achemlal L, Bezza A, Dehhaoui M, et al. Vertebral fractures and abdominal aortic calcification in postmenopausal women. A cohort study. Bone 2013;56:213–9. [19] Sennerby U, Farahmand B, Ahlbom A, Ljunghall S, Michaëlsson K. Cardiovascular diseases and future risk of hip fracture in women. Osteoporos Int 2007;18:1355–62. [20] Kauppila LI, Polak JF, Cupples LA, Hannan MT, Kiel DP, Wilson PWF. New indices to classify location, severity, and progression of calcific lesions in the abdominal aorta: a 25-year follow-up study. Atherosclerosis 1997;132:245–50. [21] Jayalath RW, Mangan SH, Golledge J. Aortic calcification. Eur J Vasc Endovasc Surg 2005;30:476–88.
Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021
Contents lists available at ScienceDirect
Clinical Imaging journal homepage: http://www.clinicalimaging.org
Original Article
Association of lumbar fractures, abdominal aortic calcification, and osteopenia☆ Tarek N. Hanna a,⁎, Matthew E. Zygmont a, Elie Harmouche b, Ninad Salastekar c, Jamlik-Omari Johnson a, Faisal Khosa a,1 a b c
Division of Emergency Radiology, Department of Radiology and Imaging Sciences, Emory University School of Medicine, Atlanta, GA Division of Musculoskeletal Radiology, Department of Radiology and Imaging Sciences, Emory University School of Medicine, Atlanta, GA Rollins School of Public Health, Emory University, Atlanta, GA
a r t i c l e
i n f o
Article history: Received 24 September 2014 Received in revised form 11 November 2014 Accepted 30 November 2014 Available online xxxx Keywords: Osteoporosis Emergency department Aortic calcifications Lumbar spine Vertebral fracture
a b s t r a c t Purpose: The purpose was to assess if abdominal aortic calcification (AAC) and low bone mineral density (BMD) are associated with fractures on lumbar spine radiographs in trauma patients. Methods: Retrospectively, 303 consecutive lumbar radiographs were independently reviewed by two radiologists for AAC, low BMD, and traumatic findings. Results: Thirty-one percent of patients had low BMD, 34% had AAC, and 24% had both. Eleven percent of radiographs showed traumatic findings. Seventy-six percent of positive cases had low BMD (Pb .001), and 64% had AAC (Pb.001). Conclusion: A higher index of suspicion for fractures is warranted when AAC and low BMD are present.
© 2014 Elsevier Inc. All rights reserved.
1. Introduction There is a long-established association between low bone mineral density (BMD) and fragility fractures. More recently, studies have shown that abdominal aortic calcification (AAC) has an association with vertebral fractures [1–7]. In a prior study by Szulc et al., the severity of aortic calcification was associated with a higher prevalence and number of vertebral fractures even after adjusting for BMD and other confounding variables [3]. AAC is an important marker of overall atherosclerotic burden [1,8,9] and readily identifiable on radiographs. Similarly, radiologists are able to subjectively identify low BMD on lumbar spine radiographs, which is a strong predictor of osteopenia or osteoporosis [10–13]. The association of AAC with low BMD has been documented in a variety of populations [1,2,8,14,15], and there is evidence that women with the most severe AAC demonstrate the greatest magnitude of bone loss after controlling for age and other confounding variables [14]. Although AAC and low BMD are radiologic ☆ Disclosure: Dr. Khosa is the American Roentgen Ray Society Scholar (2013–2015). No financial disclosures or conflict of interest on behalf of the authors. There was no commercial funding for this study. The authors have full control over all the data. The study will not be published elsewhere in any language without the consent of the copyright owners. ⁎ Corresponding author. Division of Emergency Radiology, Department of Radiology and Imaging Sciences, Emory University Midtown Hospital, 550 Peachtree Road, Atlanta GA 30308. Fax: +1 404 686 5709. E-mail address: [email protected] (T.N. Hanna). 1 Dr. Khosa is at the American Roentgen Ray Society Scholar (2013–2015).
diagnoses, a preponderance of the literature on the significance of these findings in the trauma setting is nonradiological. It is unclear how often radiologists document these findings, which may be dismissed as incidental. To our knowledge, the association between AAC, low BMD, and vertebral fractures as assessed by lumbar spine radiographs has not been explored in the acute setting. In addition to exploring the association of these three variables in emergency department (ED) trauma patients, we analyzed the original radiology reports to see how frequently these findings are being documented for clinicians. Could the identification and understanding of AAC and low BMD make radiologists more accurate at detecting lumbar fractures? 2. Materials and methods This retrospective investigation was conducted with institutional review board approval and was compliant with the Health Insurance Portability and Accountability Act. The requirement for written informed consent was waived because of the retrospective nature of the investigation. 2.1. Study population Our investigation was conducted at two university-affiliated teaching hospitals, which are both level 2 trauma centers. Our initial cohort included 844 consecutive ED patients receiving a standard three-view lumbosacral spine radiographic series from February 2011 to February
http://dx.doi.org/10.1016/j.clinimag.2014.11.021 0899-7071/© 2014 Elsevier Inc. All rights reserved.
Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021
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T.N. Hanna et al. / Clinical Imaging xxx (2014) xxx–xxx
2014. An initial power analysis suggested the necessary sample size for statistical significance, which determined the length of this time period. We defined the standard views as anteroposterior, lateral, and conedlateral views. Patients were included if there was a history of trauma within 48 h prior to presentation. Patients were excluded if they had less than three views, history of trauma or back pain for more than 48 h, history of known prior lumbar spinal surgery, or incomplete documentation related to current visit. These criteria yielded 315 patients. Age, gender, mechanism of injury, impact velocity, and follow-up imaging results done within 1 month were recorded through chart review. High-impact injury was defined as any motorized vehicle collision, falls from a height above 1 m or more than five stairs, crush injuries, or pedestrian versus automobile accidents. Low-impact injury was defined as ground-level fall, assault, or if the patient was found on the ground. Of the 315 cases, 12 were excluded during radiographic review, as three-view lumbar spine images were not available in the picture archiving and communication system for these patients, yielding a final cohort of 303 examinations. 2.2. Lumbar spine radiograph review Examinations that met study inclusion criteria were reviewed by two board-certified fellowship-trained radiologists (musculoskeletal radiology and neuroradiology). During radiographic review, no patient demographic information was displayed on the images. The reviewers were blinded to the original radiology report. Data were collected via a standard electronic data entry form. Bone mineralization was subjectively characterized by the radiologist as normal or decreased. This BMD assessment was not standardized or objective; rather, it was an observational data point of clinical practice based on previously published literature that a radiological report of low BMD is a strong predictor of osteopenia or osteoporosis [10–13]. The presence or absence of AAC was recorded. The examinations were interpreted for the presence and location of fractures. All discrepancies between the two primary reviewers were adjudicated by a third board-certified fellowship-trained radiologist (neuroradiology and emergency radiology). With regard to fractures, findings were also compared with follow-up imaging including computed tomography (CT) or magnetic resonance (MR) when available. 2.2.1. Report review Original radiology reports were screened for documentation of AAC and low BMD. In this assessment for AAC, any mention of aortic calcification, aortic atherosclerosis, or prevertebral vascular calcifications was included. Similarly, in assessing the radiology reports for low BMD, any mention of osteopenia, osteoporosis, low BMD, bone demineralization, or other synonymous descriptors was included. Following the radiograph review, the reports for those cases, which were documented as traumatic, were reviewed to see if the original radiology report documented the traumatic findings. 2.3. Statistical analysis Continuous variables were expressed as mean±standard deviation, and categorical variables were expressed as frequency n (%). Age was categorized into four categories—less than or equal to 50 years, 51–65 years, 66–80 years, and greater than 80 years—for the purpose of this analysis. Comparison between levels of categorical variables was carried out using Fisher’s Exact Test. Odds ratios with 95% confidence interval (CI) were reported using multivariate logistic analyses to estimate the association of the presence of aortic calcification with the presence of low BMD, adjusting for patient age, gender, and velocity of impact. Collinearity and interaction were assessed. Also, confounding was said to be present if the estimate for the effect of osteopenia changed by more than 10% after dropping the confounder (age, gender). Cohen’s kappa (unweighted) was used to assess interobserver agreement
among the reviewing radiologists for low BMD and AAC. Significance was assessed at two-sided α error of 0.05. All analyses were carried out using SAS 9.3 (SAS Institute Inc., Cary, NC, USA). 3. Results Table 1 summarizes the distribution of demographic and clinical variables in the 303 patients comprising the study population. The mean age of study participants was 53±22 years. Fifty-three percent of the patients were less than 50 years of age, and 67% were women. Based on the clinical history, 58% patients were categorized as having suffered trauma with a low-velocity of impact. Our population demographics differ from the typical trauma population in that patients are older and more likely to be female, which may represent an inherent modality selection bias, as trauma patients imaged by radiographs are older and more likely to have suffered lower-impact trauma. Based on radiographic review, low BMD was present in 31% (n=95/303) of the patients. AAC was present in 34% (n=103/303) of the study population. There was a high degree of radiologist agreement for both low BMD and AAC, with Cohen’s kappa (unweighted) of 0.75 (0.64–0.86) and 0.86 (0.75–0.97) respectively. AAC was present in 76% of patients with low BMD as compared to just 15% of patients with normal BMD (Pb.001). The percentage of patients with AAC increased with increasing age and was present in 91% of patients above 80 years of age. The difference in the proportion of patients with AAC among men and women was not statistically significant (P= .156). An analysis of the distribution of demographic and clinical variables categorized by the presence or absence of AAC is presented in Table 2. Multivariate logistic analyses revealed that the association between AAC and low BMD was not significant after adjusting for patient age, gender, and velocity of impact (Table 3). Age and velocity of impact were, however, were associated with AAC (Pb .001 and P=.046 respectively). The odds for the presence of AAC in the age groups of 51–65, 66–80, and N 80 years were 17, 63, and 135 times greater than those for patients less than or equal to 50 years of age. The age-adjusted odds for the presence of AAC in patients who suffered low-impact trauma were 2.4 times greater than those in patients with highimpact trauma. Gender neither was significantly associated with the presence of AAC nor was a significant confounder. Hence, gender was excluded from the model before calculating the adjusted estimates. Of the 303 cases, 11% (n= 33) were considered to have traumatic findings based on lumbar spine radiographs (“positive-trauma” cases). Distribution of variables categorized by the presence and absence of radiographic traumatic findings is shown in Table 4. Trauma was correlated with age (Pb.001) and also with low-impact velocity (Pb.001). In 76% (n= 25/33) of positive-trauma cases, low BMD was present Table 1 Distribution of demographic and clinical variables in the study population (n=303) N (%) Age ≤50 years 51–65 years 66–80 years N80 years Gender Male Female No. of traumatic cases Velocity of impact High impact Low impact Osteopenia/low BMD Absent Present Aortic calcification Absent Present
162 (53) 55 (18) 32 (11) 54 (18) 99 (33) 203 (67) 33 (11) 126 (42) 176 (58) 208 (69) 95 (31) 200 (66) 103 (34)
Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021
T.N. Hanna et al. / Clinical Imaging xxx (2014) xxx–xxx Table 2 Distribution of demographic and clinical variables categorized by presence/absence of aortic calcification (n=303)
Table 4 Distribution of variables categorized by the presence and absence of radiographic trauma Trauma n (%)
Aortic calcification n (%)
Age ≤50 years 51–65 years 66–80 years N80 years Gender Male Female Velocity of impact High impact Low impact Osteopenia/low BMD Absent Present
Present
Absent
P value
5 (3) 24 (44) 25 (78) 49 (91)
157 (97) 31 (56) 7 (22) 5 (9)
b.001
28 (28) 75 (37)
71 (72) 128 (63)
.156
13 (10) 90 (51)
113 (90) 86 (49)
b.001
31 (15) 72 (76)
177 (85) 23 (24)
b.001
(Pb.001). In 64% (n=21/33) of positive-trauma cases, AAC was present (Pb.001). The vast majority of positive-trauma cases (88%, n=28) were wedge compression fractures, and the majority (76%, n= 25/33) of positive-trauma examinations had only one traumatic finding. There were five patients with two traumatic findings (2%), two patients with three traumatic findings (1%), and one patient with four traumatic findings (0.3%). The remaining positive-trauma cases consisted of bursttype vertebral body fracture (2%, n= 1), transverse process fractures (2%, n=1), sacral fracture (2%, n=1), and possible acute ligamentous/ disc injury (2%, n=1). Only 5 of these 33 cases proceeded to advanced imaging, which confirmed the radiographic findings; the majority of the remaining patients were treated supportively with analgesics and discharged, or admitted for reasons unrelated to lumbar spine trauma. Of note, all of these 33 “positive-trauma” cases had documented acute back pain corresponding to the time since trauma. Of the 33 positive-trauma cases, 26 were initially consensus positivetrauma by two independent readers. A third reader adjudicated seven cases. Compared to the original radiology report, 3 of the 33 positivetrauma findings were not described as traumatic by the original radiologist. Notably, the three discrepant cases were part of the seven that went to tiebreak reads in our review. All three were age-indeterminate wedging compression fractures, which were not originally mentioned. Two patients had routine supportive care with analgesics, and follow-up to 15 months documented no advanced imaging or issues related to these fractures. One patient was a metastatic cancer patient and had multiple follow-ups and multiple progressive pathologic compressions. Of the three discrepant trauma cases, two had both AAC and low BMD, while one had only AAC. Of the three original reports, one did not describe AAC, while the others were accurate in this regard. Only 46% of the patients categorized as having AAC during our review had this finding mentioned in their original report (Table 5). Table 3 Estimate of the association of aortic calcification with osteopenia, adjusted for patient age and velocity of trauma (n=303)
Age ≤50 years 51–65 years 66–80 years N80 years Velocity of impact High impact Low impact Osteopenia/low BMD Absent Present
Odds ratio for the presence of aortic calcification (95% CI)
P value
1 17.06 (5.70–51.08) 63.15 (16.85–236.74) 135.91 (32.54–567.61)
Reference b.001 b.001 b.001
1 2.43 (1.02–5.82)
Reference .046
1 1.71 (0.732–4.02)
Reference .214
3
Age ≤50 years 51–65 years 66–80 years N80 years Gender Male Female Velocity of impact High impact Low impact Osteopenia/low BMD Absent Present Aortic calcification Absent Present
Present
Absent
P value
4 (2) 7 (13) 3 (9) 19 (35)
158 (98) 48 (87) 29 (91) 35 (65)
b.001
8 (8) 25 (12)
91 (92) 178 (88)
.328
5 (4) 28 (16)
121 (96) 148 (84)
.001
8 (4) 25 (26)
200 (96) 70 (74)
b.001
12 (6) 21 (20)
188 (94) 82 (80)
b.001
Similarly, only 36% of patients with low BMD had this finding stated in the original radiology report (Table 6). The initial reports were generated in an emergency radiology division with a 24/7/365 coverage. A review of the 12 excluded cases demonstrated that 4 patients could not complete the examination due to pain, inability to position, or refusal to continue with imaging. The remaining eight cases did not have any documentation to explain missing images or incomplete examination. Importantly, two of the cases without documentation showed traumatic findings by lateral lumbar spine radiographs (the only view obtained): an L4 burst fracture and an L1 compression fracture, respectively. Both these patients proceeded immediately to CT and MR, respectively, which confirmed acute fractures.
4. Discussion Our study supports that ED trauma patients with AAC and low BMD are more likely to have vertebral fractures on lumbar spine radiographs. Although severity of AAC has been shown to be an independent predictor of hip fractures [4,16,17], the literature on association between AAC and vertebral fractures is complex and occasionally conflicting [1–7,17,18]. This is explained by the wide variety of patient populations and various techniques used in identification of AAC and low BMD [1–7,16–19]. Important population attributes that influence this association appear to be gender [3,7,8,14,18], population age [3], postmenopausal women [7,18], study size [3], overall burden of cardiovascular pathology in the population examined [3,19], and ethnicity [1,8,9]. In addition to these population differences, study design and techniques employed in prior studies vary widely, with AAC being assessed quantitatively versus subjectively [5,7,18] and low BMD being measured by dual X-ray absorptiometry (DXA), radiographic criteria, or metacarpal cortical area [14,18]. Here we chose to focus on factors that can be readily assessed by the clinical radiologist during routine reading of lumbar spine radiographs, without allocation of additional resources or extra time commitment. Table 5 If present, was aortic calcification mentioned in the original radiology report? (n=303) Mentioned in the original report Aortic calcification
Yes
No
Present Absent
47 1 48
56 199 255
103 200
Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021
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T.N. Hanna et al. / Clinical Imaging xxx (2014) xxx–xxx
Table 6 If present, was subjective low BMD mentioned in the original radiology report? (n=303) Mentioned in the original report Low BMD
Yes
No
Present Absent
35 4 38
61 203 264
96 207
As expected, age was directly correlated to the incidence of aortic calcifications, and the odds ratio for patients greater than 80 years of age was 135 times greater than for patients less than or equal to 50 years of age. There was an association between AAC and low BMD, but this was not significant after adjusting for age. This may be secondary to the age of our population (53±22 years) and the relative paucity of aortic calcifications in younger patients. In the longitudinal study by Kiel et al., an initial cross-sectional analysis done with an average age of approximately 54 years was unable to show a significant independent relationship between aortic calcification and metacarpal cortical bone volume [14]. However, at the termination of that 25-year followup study, there was a significant association between these variables in women independent of age, supporting the fact that an older population is necessary to achieve significance in this assessment [14]. Zhou et al. recently demonstrated that severe AAC was associated with a threefold greater risk of vertebral fractures in Asian postmenopausal women using lateral lumbar spine radiographs [7]. El Maghraoui et al. showed that severe AAC was associated with increased fracture prevalence in postmenopausal Caucasian women independent of age and BMD in a study utilizing DXA [18]. Both of these studies used a semiquantitative method of classifying AAC, which was described by Kauppila et al. [20]. Our ED population was not as homogenous or as old as most prior study populations, and our assessment of AAC was binary. The clinical radiologist can easily classify patients into four groups based on lumbar spine radiographs via our binary methods: negative AAC and normal BMD (58%, n= 177), positive AAC and normal BMD (10%, n= 31), negative AAC and low BMD (8%, n= 23), and positive AAC and low BMD (24%, n= 72). This last group (positive AAC, low BMD) made up approximately one quarter of ED patients who received lumbar spine radiographs in our study and is at greater risk for lumbar spine traumatic injury. There is a well-known relationship between low BMD and fractures, and data independently connect AAC to increased fracture incidence [1–7,17,18]. In our study, the preponderance of trauma patients was in this quartile. Interestingly, the odds ratio for the presence of AAC in those with low-impact trauma was 2.4 times greater than in those patients with high-impact trauma independent of age (multivariate logistic model, adjusted for age and gender). To our knowledge, this association has never been previously reported. We theorize that this is related to a combination of ED physician imaging practices and self-selection for ED visits following low-impact trauma. Specifically, healthy patients with no preexisting conditions who suffer low-impact trauma may be less likely to visit the ED and, even if they do visit the ED, less likely to undergo imaging. Those with chronic disease may be more likely to undergo imaging following low-impact trauma and also more likely to have AAC. This is an important observation because low-impact trauma can cause nondisplaced fractures, particularly in the hip and spine, which may be harder to detect by plain radiographs. In this series of trauma patients, the radiologist did not routinely document the presence of AAC or low BMD in their final report. We presume this is because emergency radiologists in the setting of trauma dismiss these findings as incidental, and may not be aware of the importance of AAC and its independent association with osteoporosis and fractures. In an ED patient who may not have prior workup or known risk factors, documenting AAC is important since it predicts an increased incidence of cardiovascular events [21]. Additionally, the subjective
reporting of low BMD by the radiologist may be the first knowledge of possible osteoporosis and may prompt additional workup. This association can also be used as a teaching tool for residents, encouraging them to raise their level of suspicion for fractures in patients with AAC and low BMD. Overall, we suggest that radiologists be more alert to trauma in subgroups of patients with AAC and low BMD. Our study had limitations. Initially, 315 consecutive lumbar spine examinations were identified, but 12 were excluded due to missing images and incomplete examinations. We specifically note the exclusion of these cases because two of these patients had vertebral fractures. In evaluating AAC, we used a binary approach (present or absent) rather than characterizing magnitude or severity of calcification. We did this to create an analysis that could be easily utilized by radiologists in the clinical setting. The acuity of radiographic findings was not routinely confirmed by advanced imaging, but lumbar radiographs often describe age-indeterminate findings that require clinical correlation for point tenderness. We note that two of the three originally missed fractures were cases with both AAC and low BMD, while the third had AAC only. This suggests that greater attention to cases with AAC and low BMD could improve fracture detection. However, this study did not have the data to conclude that radiologists who report AAC and low BMD have better accuracy in fracture diagnosis. Given that AAC and BMD are not independent variables, to truly test the independent effect of these on fractures, we would have had to interpret the images while covering the aorta, so AAC was not visible. Finally, we did have an objective test to confirm low BMD. However, we note that previous studies have concluded that subjective radiological report of low BMD is a strong predictor of osteopenia or osteoporosis; we are not attempting to duplicate this work. 5. Conclusion A higher index of suspicion for lumbar fractures is warranted in the subgroup of patients with AAC and low BMD. Additionally, AAC and low BMD may reveal clinically relevant information about overall patient health. Our study shows that radiologists do not routinely document these findings in the acute setting.
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Please cite this article as: Hanna TN, et al, Association of lumbar fractures, abdominal aortic calcification, and osteopenia, Clin Imaging (2014), http://dx.doi.org/10.1016/j.clinimag.2014.11.021