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Bone mineral density differences between femurs of scoliotic patients undergoing dual-energy X-ray absorptiometry
Clinical Radiology 68 (2013) e511ee515
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Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Bone mineral density differences between femurs of scoliotic patients undergoing dual-energy X-ray absorptiometry M. Bandirali a, *, C. Messina a, G. Di Leo b, L.M. Sconfienza b, c, A. Aliprandi b, F.M. Ulivieri d, F. Sardanelli b, c degli Studi di Milano, Milano, Italy Scuola di Specializzazione in Radiodiagnostica, Universita Servizio di Radiologia, IRCCS Policlinico San Donato, San Donato Milanese, Milano, Italy c degli Studi di Milano, Milano, Italy Dipartimento di Scienze Biomediche per la Salute, Universita d Mineralometria Ossea Computerizzata e Ambulatorio Malattie Metabolismo Minerale e Osseo, Servizio di Medicina Nucleare, Ospedale Maggiore, Milano, Italy a
b
art icl e i nformat ion Article history: Received 7 December 2012 Received in revised form 15 March 2013 Accepted 29 March 2013
AIM: To investigate whether a difference exists in the bone mineral density (BMD) between femurs in scoliotic patients undergoing dual-energy X-ray absorptiometry (DXA) and whether this difference is related to spine convexity. MATERIALS AND METHODS: Of 1080 consecutive patients who underwent DXA, 127 had lumbar scoliosis seen at DXA. Further, after excluding 30 patients with previous osteoporotic fractures, metallic/image artefacts, soft-tissue calcifications, the BMD differences between femurs of 97 scoliotic patients (94 females; mean age 67 11 years) were analysed. Femurs were classified as ipsilateral or contralateral to the spine convexity. Least significant change was used as a threshold of measurement precision. Differences between femoral neck BMD in respect of and regardless of spine convexity were calculated for each patient. Student’s t-test and Wilcoxon’s signed-rank test were used to assess significance. RESULTS: Fifty-nine of 97 patients (61%) had left-sided scoliosis. Osteoporosis was found in 32/97 patients (33%), osteopenia in 54/97 (56%), and 11/97 (11%) had a normal T-score. Of 97 patients, 46 (47%) had ipsilateral BMD < contralateral BMD. Regardless of spine convexity, 66/ 97 patients (68%) had different BMD values between femurs. Among them, variation of densitometric diagnosis was seen in 29/66 patients (44%), and in 29/97 patients overall (30%). CONCLUSION: Differences in the femoral neck BMD exist between femurs of scoliotic patients undergoing DXA. Thus, bilateral femoral DXA acquisition is recommended. Ó 2013 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Osteoporosis is a metabolic systemic disease characterized by bone mass loss and micro-architectural deterioration degli Studi di * Guarantor and correspondent: M. Bandirali, Universita Milano, Scuola di Specializzazione in Radiodiagnostica, Via Festa del Perdono 7, 20122 Milano, Italy. Tel.: þ390252774468; fax: þ390252774925. E-mail address: [email protected] (M. Bandirali).
of bone tissue, resulting in reduction of bone strength and increased likelihood of fragility fractures.1,2 Postmenopausal osteoporosis is the most common type, a primary form affecting about 40% of white women. This prevalence is expected to increase in the future due to population ageing.3 Diagnosis of osteoporosis is commonly based on bone mineral density (BMD) measurement using dual-energy X-ray absorptiometry (DXA).4 DXA is preferably performed
0009-9260/$ e see front matter Ó 2013 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2013.03.028
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in skeletal sites where fracture risk is the highest, i.e. in the lumbar spine, proximal femurs, and distal forearms.3,5 However, although a significant BMD difference between dominant and non-dominant forearms has been demonstrated,6 the existence of BMD differences between femurs is still under debate.8e10 Thus, no consensus has been reached on which femur to perform DXA. As a consequence, the International Society for Clinical Densitometry (ISCD) 2007 guidelines7 suggest measurement of BMD in both femurs for each patient and to consider the lowest value for diagnosis. In fact, this recommendation is often disregarded in clinical practice, and femoral DXA is arbitrarily performed on the non-dominant femur. In addition, important clinical trials11,12 do not clearly state on which femur the DXA examinations were performed. In 1996, Hans et al.13 studied a small group of otherwise healthy female volunteers with untreated adolescent structural lumbar idiopathic scoliosis and without suspicion of osteoporosis. They showed significant differences in the BMD of the femoral neck between the two femurs.13 In particular, they showed a significantly lower BMD in the femur ipsilateral to the spine convexity compared with the contralateral femur.13 These results suggest that in premenopausal scoliotic women, BMD should be measured on the femur ipsilateral to the spine convexity. Of note, the prevalence of scoliosis among patients undergoing DXA for a suspected or known osteoporosis is reported to be 9e13%14,15; thus, this is a significant issue. To the authors’ knowledge, the potential BMD difference between the two femurs in scoliotic patients routinely undergoing DXA has never been studied. The hypothesis of the present study was that a significant difference in BMD exists between femurs in patients with scoliosis. Thus, the aim of the present study was to test this in scoliotic patients routinely undergoing DXA, and to also evaluate whether the difference is related to spine convexity.
Materials and methods
[mean SD; three males (age 63 13 years) and 94 postmenopausal women (age 67 11 years)], who underwent a DXA examination of the lumbar spine and both femurs. All DXA examinations were performed using a Hologic QDR Delphi W unit (Apex Software v. 3.0.1, Hologic Inc., Bedford, MA, USA). The least significant change (LSC), calculated as previously reported by Hamdy et al.,9 was used as a threshold of measurement precision. Femoral neck LSC for our DXA system was 0.029 g/cm2. All examinations were acquired and processed according to ISCD guidelines.7 In particular, the patient was repositioned for each of the three acquisition sites. The present study was concerned with the evaluation of femoral neck BMD values; results of spine BMD are not considered in this report, as scoliosis affects these values.14,18,19
Analysis in respect of spine convexity BMDIpsilateral was the BMD value measured on the femur ipsilateral to spine convexity and BMDcontralateral was that of the contralateral femur in each patient. The difference in ipsilateral versus contralateral (DBMDIC) femoral neck BMD was calculated as
DBMDIC ¼ BMDipsilateral BMDcontralateral As neither BMDipsilateral or BMDcontralateral may be considered as a reference, DBMDIC was normalized to their mean as BMDipsilateral BMDcontralateral 100 DBMD%IC ¼ Mean BMDipsilateral BMDcontralateral Regarding the T-score, the absolute difference (DTIC) and the percent difference (DT%IC) were calculated in the same way as for the BMD.
Analysis regardless of spine convexity Local ethics committee approval was obtained for this retrospective study and informed consent was waived. All patients had given written informed consent for the potential use of results of their examination for scientific purposes. Using the digital archive system, DXA examinations of 1080 patients performed at our tertiary university hospital from February to June 2011 were reviewed. DXA images of the lumbar spine were used for scoliosis detection (left or right convexity) and grading (Cobb’s angle), as reported by Urrutia et al.15 This method of patient selection was based on the demonstration of a close correlation between Cobb’s angle measured on DXA and that measured on anteroposterior lumbar radiographs,14 and on the definition of scoliosis as a deviation of the spine in the coronal plane of 10 .16,17 Lumbar scoliosis was detected in 127 (12%) patients. Thirty patients with previous osteoporotic fractures, metallic implants, or other metallic devices, extensive soft-tissue calcifications, or imaging artefacts were excluded. Thus, the cohort included 97 scoliotic patients aged 67 11 years
BMDhigher was the higher BMD between the femurs, and BMDlower was the lower BMD for each patient. Their difference (DBMDHL) was calculated as
DBMDHL ¼ BMDhigher BMDlower As neither BMDhigher or BMDlower may be considered as a reference, DBMDHL was normalized to their mean as BMDhigher BMDlower 100 DBMD%HL ¼ Mean BMDhigher BMDlower Regarding the T-score, the absolute difference (DTHL) and the percent difference (DT%HL) were calculated in the same way as for BMD. Diagnosis was defined based on the lower femoral Tscore. According to the World Health Organization (WHO), patients were considered normal when T 1, osteopenic when 2.5 < T < 1, or osteoporotic when T 2.5.7
M. Bandirali et al. / Clinical Radiology 68 (2013) e511ee515
The median BMD ipsilateral to the spinal convexity or of the femur with the higher BMD value were compared to BMD contralateral to the spine convexity or of the femur with the lower BMD value, using the Student’s t-test. The median T-scores ipsilateral to spine convexity or of the femur with the higher BMD value were compared to T-scores contralateral to the spine convexity or of the femur with the lower BMD value using the Wilcoxon’s signed-rank test. Continuous data were presented as mean standard deviations and p < 0.05 was considered significant. SPSS software (v. 19, IBM, Armonk, NY, USA) was used.
Results In the present series, 59/97 patients (61%) were affected by left-sided scoliosis, whereas 38/97 patients (39%) were affected by right-sided scoliosis. Considering the lowest femoral neck T-score value between both femurs, 32/97 patients (33%) were diagnosed with osteoporosis and 54/97 patients (56%) were diagnosed with osteopenia, whereas 11/97 patients (11%) had a normal T-score value.
Analysis in respect of spine convexity Mean BMDipsilateral was significantly lower (0.629 0.108 g/cm2) than BMDcontralateral (0.653 0.118 g/cm2; p < 0.001). However, the mean DBMDIC was 0.024 g/cm2 (mean DBMD%IC ¼ 4%), lower than the LSC threshold. The mean T-scoreipsilateral was significantly lower (2.0 0.9) than the T-scorecontralateral (1.8 1.0; p < 0.001). The mean DTOC was 0.2 (mean DT% IC¼ 12%). Out of 97 patients, 72 (74%) had BMDIpsilateral values lower than their BMDcontralateral. Using the LSC threshold, this value decreased to 46/97 patients (47%). Full data are reported in Table 1. Fig 1 shows a DXA examination of a patient affected by left-sided scoliosis.
Analysis regardless of spine convexity The difference between BMDhigher (0.664 0.116 g/cm2) and BMDlower (0.617 0.106 g/cm2) was statistically significant (p < 0.001). The mean DBMDHLwas 0.047 g/cm2 (mean DBMD%HL ¼ 7.3%), higher than the LSC threshold. The difference between the mean T-scorehigher (1.7 1.0) and the mean T-scorelower (2.1 0.9; p < 0.001) was statistically significant (p < 0.001). The mean DTHL was 0.4 (mean DT%HL ¼ 32%). Out of 97 patients, 95 (98%) had different BMD values between femurs. Using the LSC threshold, this value decreased to 66/97 patients (68%). Full data are reported in Table 2. Among these 66 patients, considering two different
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scenarios in which DXA is performed on the femoral neck with the higher or lower BMD, respectively, a variation of densitometric diagnosis based on WHO recommendation was seen in 29/66 patients (44%), and in 29/97 patients overall (30%). Full data are reported in Table 3.
Discussion The present study confirmed the hypothesis that, in patients affected by lumbar spine scoliosis detected at DXA, BMD values measured on both femoral necks are significantly different. Also, differences were not related to spine convexity. Differences between the BMD values of the two femoral necks of the same patient are still a debated topic. Some authors19,20 have demonstrated that there is no difference in BMD between the femurs of the same patient, whereas others report significant differences.9,10 This latter issue is taken into account in the ISCD 2007 guidelines7 that suggest performing DXA on both femurs of the same patient and to choose the lower value to establish a diagnosis of osteoporosis. It is known that a correlation exists between osteoporosis and scoliosis18,21 and vice versa.22,23 Also, some reports describe the presence of loading imbalance on lower limbs due to scoliosis. Although some authors show no difference in terms of static strength between the two sides,24 it is well known that bone architecture and its mineral density are widely influenced by dynamic forces.10,25 Thus, regardless of the reasons, the evidence of a difference between two femurs in a scoliotic patient is largely expected. The only paper reporting such a topic was published in 1996 by Hans et al.,13 who reported that the BMDipsilateral was lower than the BMDcontralateral in a small sample of 15 women. These data are not consistent with what we have found, as in the present series less than half the patients had BMDipsilateral < BMDcontralateral. Conversely, about one out of five patients in the present series had an unexpected value of BMDipsilateral > BMDcontralateral. These data may have different explanations. First, the sample size is six-times larger than that reported by Hans et al.13 Thus, their data may not be reproduced on a larger scale. Also, the present population mainly included post-menopausal women routinely undergoing DXA for osteoporosis detection. This is different to that reported by Hans et al.,13 whose series included 11 pre-menopausal and four postmenopausal women, with a mean age of 45 years. Furthermore those patients were affected by untreated adolescent structural lumbar idiopathic scoliosis, whereas no data regarding scoliosis type are available in the present series. However, primary degenerative scoliosis is the most frequent type in the elderly population.16,17
Table 1 Comparison of femoral neck bone mineral density (BMD) according to spine convexity. BMD
Regardless least significant change threshold Using least significant change threshold
Ipsilateral < contralateral
Ipsilateral ¼ contralateral
Ipsilateral > contralateral
72/97 (74%) 46/97 (47%)
2/97 (2%) 31/97 (32%)
23/97 (24%) 20/97 (21%)
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Figure 1 DXA images of a patient affected by left-sided scoliosis. (a) Lumbar spine scan. Cobb’s angle was 16 . Femoral scan performed on the femoral neck (b) contralateral and (c) ipsilateral to the spine convexity. Note that the T-score decreases from e2.1 to e2.7, implying a diagnosis variation from osteopenia to osteoporosis.
Regardless of spine convexity, over two-thirds of patients have different femoral neck BMD values between femurs. These data imply that in about one-third of patients included in the present series there is a variation of diagnosis from normal to osteopenia and from osteopenia to osteoporosis (see Table 3). However, if small differences around the diagnostic threshold cause a variation in diagnosis, larger differences close to the mean of the diagnostic interval do not produce any effect. Thus, these data may be underestimated. Table 2 Comparison of femoral neck bone mineral density (BMD) regardless to spine convexity. BMD Different between femurs Regardless least significant change threshold Using least significant change threshold
Non different between femurs
95/97 (98%)
2/97 (2%)
66/97 (68%)
31/97 (32%)
The present report focused on the evaluation of femoral neck BMD values only for two main reasons. First, the WHO international reference standard for osteoporosis diagnosis is a T-score of 2.5 or less measured at the femoral neck.7 Also femoral neck BMD is recommended for use in FRAXÒ, a diagnostic tool developed by WHO used to evaluate the 10-year probability of bone fracture risk.26 The clinical implications of the present results may be appreciated considering that more than two-thirds of the present patients showed a BMD difference between the two femurs regardless of spine convexity. As it is unknown a priori which femur has the lowest BMD, it is recommended that all scoliotic patients detected at spine DXA should undergo bilateral femoral DXA. In other words, the ISCD guideline suggesting the study of both femurs for all patients7 should be considered mandatory for scoliotic patients. Apart from the retrospective nature of the study, the main limitation of this work is that lumbar DXA was used for identification of scoliosis. Thus, the evaluation was limited to the lumbar spine and scoliotic curvature of the
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Table 3 Variation of densitometric diagnosis according to higher or lower femoral neck bone mineral density (BMD) based on World Health Organization recommendation in 66 patients with BMD difference between femurs higher than least significant change. Higher BMD femoral neck
Lower BMD femoral neck
Number of patients
Totala
Overallb
From
Normal Osteopenia Osteoporosis
To
Normal Osteopenia Osteoporosis
8/66 (12%) 22/66 (33%) 7/66 (11%)
37/66 (56%)
37/97 (38%)
From
Normal Osteopenia
To
Osteopenia Osteoporosis
10/66 (15%) 19/66 (29%)
29/66 (44%)
29/97 (30%)
a b
Values reported are related to 66 patients. Values reported represent comparison to whole study population.
whole spine could not be evaluated. Regarding the reliability of detecting scoliosis at DXA, it has been demonstrated that Cobb’s angle measured by DXA is comparable to that obtained with conventional radiographs allowing a reliable definition of scoliosis.14,15 However, knowledge of only the lumbar spine deserves some consideration. The presence of a second curvature in the dorsal spine opposite to that in the lumbar spine makes the distinction between ipsilateral and contralateral convexity somewhat arbitrary and may explain paradoxical cases. However, regardless of the side of convexity, a significant BMD difference does exist between the two femurs. Future studies are warranted in order to investigate how whole-spine scoliotic curvature impacts on the BMD of the two femurs. In conclusion, the present study demonstrated that a difference in femoral neck BMD exists between the two femurs of scoliotic patients undergoing DXA. For these patients, bilateral femoral DXA acquisition should be recommended.
References 1. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA 2001;285:785e95. 2. Consensus development conference: prophylaxis and treatment. Am J Med 1991;90:107e10. 3. S anchez-Riera L, Wilson N, Kamalaraj N, et al. Osteoporosis and fragility fractures. Best Pract Res Clin Rheumatol 2010;24:793e810. 4. Rachner TD, Khosla S, Hofbauer LC. Osteoporosis: now and the future. Lancet 2011;377:1276e87. 5. Delnevo A, Bandirali M, Di Leo G, et al. Differences among array, fast array, and high-definition scan modes in bone mineral density measurement at dual-energy x-ray absorptiometry on a phantom. Clin Radiol 2013;68:616e9. 6. Faulkner KG, Cummings SR, Nevitt MC, et al. Hip axis length and osteoporotic fractures. Study of Osteoporotic Fractures Research Group. J Bone Miner Res 1995;10:506e8. 7. Lewiecki EM, Gordon CM, Baim S, et al. International Society for Clinical Densitometry 2007 Adult and Pediatric Official Positions. Bone 2008;43:1115e21. 8. Benoist M. Natural history of the aging spine. Eur Spine J 2003;12(Suppl. 2):S86e89.
9. Hamdy R, Kiebzak GM, Seier E, et al. The prevalence of significant leftright differences in hip bone mineral density. Osteoporos Int 2006;17:1772e80. 10. Downey PA, Siegel MI. Bone biology and the clinical implications for osteoporosis. Phys Ther 2006;86:77e91. 11. Neer RM, Arnaud CD, Zanchetta JR, et al. Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 2001;344:1434e41. 12. Chesnut III CH, Skag A, Christiansen C, et al, Oral Ibandronate Osteoporosis Vertebral Fracture Trial in North America and Europe (BONE). Effects of oral ibandronate administered daily or intermittently on fracture risk in postmenopausal osteoporosis. J Bone Miner Res 2004;19:1241e9. 13. Hans D, Biot B, Schott AM, et al. No diffuse osteoporosis in lumbar scoliosis but lower femoral bone density on the convexity. Bone 1996;18:15e7. 14. Pappou IP, Girardi FP, Sandhu HS, et al. Discordantly high spinal bone mineral density values in patients with adult lumbar scoliosis. Spine 2006;31:1614e20. 15. Urrutia J, Diaz-Ledezma C, Espinosa J, et al. Lumbar scoliosis in postmenopausal women: prevalence and relationship with bone density, age, and body mass index. Spine 2011;36:737e40. 16. Aebi M. The adult scoliosis. Eur Spine J 2005;14:925e48. 17. Schwab FJ, Smith VA, Biserni M, et al. Adult scoliosis: a quantitative radiographic and clinical analysis. Spine 2002;27:387e92. 18. Daffner SD, Vaccaro AR. Adult degenerative lumbar scoliosis. Am J Orthop (Belle Mead NJ) 2003;32:77e82. 19. Bonnick SL, Nichols DL, Sanborn CF, et al. Right and left proximal femur analyses: is there a need to do both? Calcif Tissue Int 1996;58:307e10. 20. Lilley J, Walters BG, Heath DA, et al. Comparison and investigation of bone mineral density in opposing femora by dual-energy X-ray absorptiometry. Osteoporos Int 1992;2:274e8. 21. Thevenon A, Pollez B, Cantegrit F, et al. Relationship between kyphosis, scoliosis, and osteoporosis in the elderly population. Spine (Phila Pa 1976) 1987;12:744e55. 22. Velis KP, Healey JH, Schneider R. Osteoporosis in unstable adult scoliosis. Clin Orthop Relat Res 1988;273:132e41. 23. Carter OD, Haynes SG. Prevalence rates for scoliosis in US adults: results from the first National Health and Nutrition Examination Survey. Int J Epidemiol 1987;16:537e44. 24. Faulkner KG, Genant HK, McClung M. Bilateral comparison of femoral bone density and hip axis length from single and fan beam DXA scans. Calcif Tissue Int 1995;56:26e31. 25. Goldstein SA. The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech 1987;20:1055e61. 26. WHO fracture risk assessment tool. World Health Organization collaborating centre for metabolic bone diseases. UK: University of Sheffield. Available at: http://www.shef.ac.uk/FRAX/index.jsp [accessed 24.10.12].
Contents lists available at SciVerse ScienceDirect
Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Bone mineral density differences between femurs of scoliotic patients undergoing dual-energy X-ray absorptiometry M. Bandirali a, *, C. Messina a, G. Di Leo b, L.M. Sconfienza b, c, A. Aliprandi b, F.M. Ulivieri d, F. Sardanelli b, c degli Studi di Milano, Milano, Italy Scuola di Specializzazione in Radiodiagnostica, Universita Servizio di Radiologia, IRCCS Policlinico San Donato, San Donato Milanese, Milano, Italy c degli Studi di Milano, Milano, Italy Dipartimento di Scienze Biomediche per la Salute, Universita d Mineralometria Ossea Computerizzata e Ambulatorio Malattie Metabolismo Minerale e Osseo, Servizio di Medicina Nucleare, Ospedale Maggiore, Milano, Italy a
b
art icl e i nformat ion Article history: Received 7 December 2012 Received in revised form 15 March 2013 Accepted 29 March 2013
AIM: To investigate whether a difference exists in the bone mineral density (BMD) between femurs in scoliotic patients undergoing dual-energy X-ray absorptiometry (DXA) and whether this difference is related to spine convexity. MATERIALS AND METHODS: Of 1080 consecutive patients who underwent DXA, 127 had lumbar scoliosis seen at DXA. Further, after excluding 30 patients with previous osteoporotic fractures, metallic/image artefacts, soft-tissue calcifications, the BMD differences between femurs of 97 scoliotic patients (94 females; mean age 67 11 years) were analysed. Femurs were classified as ipsilateral or contralateral to the spine convexity. Least significant change was used as a threshold of measurement precision. Differences between femoral neck BMD in respect of and regardless of spine convexity were calculated for each patient. Student’s t-test and Wilcoxon’s signed-rank test were used to assess significance. RESULTS: Fifty-nine of 97 patients (61%) had left-sided scoliosis. Osteoporosis was found in 32/97 patients (33%), osteopenia in 54/97 (56%), and 11/97 (11%) had a normal T-score. Of 97 patients, 46 (47%) had ipsilateral BMD < contralateral BMD. Regardless of spine convexity, 66/ 97 patients (68%) had different BMD values between femurs. Among them, variation of densitometric diagnosis was seen in 29/66 patients (44%), and in 29/97 patients overall (30%). CONCLUSION: Differences in the femoral neck BMD exist between femurs of scoliotic patients undergoing DXA. Thus, bilateral femoral DXA acquisition is recommended. Ó 2013 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Osteoporosis is a metabolic systemic disease characterized by bone mass loss and micro-architectural deterioration degli Studi di * Guarantor and correspondent: M. Bandirali, Universita Milano, Scuola di Specializzazione in Radiodiagnostica, Via Festa del Perdono 7, 20122 Milano, Italy. Tel.: þ390252774468; fax: þ390252774925. E-mail address: [email protected] (M. Bandirali).
of bone tissue, resulting in reduction of bone strength and increased likelihood of fragility fractures.1,2 Postmenopausal osteoporosis is the most common type, a primary form affecting about 40% of white women. This prevalence is expected to increase in the future due to population ageing.3 Diagnosis of osteoporosis is commonly based on bone mineral density (BMD) measurement using dual-energy X-ray absorptiometry (DXA).4 DXA is preferably performed
0009-9260/$ e see front matter Ó 2013 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2013.03.028
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in skeletal sites where fracture risk is the highest, i.e. in the lumbar spine, proximal femurs, and distal forearms.3,5 However, although a significant BMD difference between dominant and non-dominant forearms has been demonstrated,6 the existence of BMD differences between femurs is still under debate.8e10 Thus, no consensus has been reached on which femur to perform DXA. As a consequence, the International Society for Clinical Densitometry (ISCD) 2007 guidelines7 suggest measurement of BMD in both femurs for each patient and to consider the lowest value for diagnosis. In fact, this recommendation is often disregarded in clinical practice, and femoral DXA is arbitrarily performed on the non-dominant femur. In addition, important clinical trials11,12 do not clearly state on which femur the DXA examinations were performed. In 1996, Hans et al.13 studied a small group of otherwise healthy female volunteers with untreated adolescent structural lumbar idiopathic scoliosis and without suspicion of osteoporosis. They showed significant differences in the BMD of the femoral neck between the two femurs.13 In particular, they showed a significantly lower BMD in the femur ipsilateral to the spine convexity compared with the contralateral femur.13 These results suggest that in premenopausal scoliotic women, BMD should be measured on the femur ipsilateral to the spine convexity. Of note, the prevalence of scoliosis among patients undergoing DXA for a suspected or known osteoporosis is reported to be 9e13%14,15; thus, this is a significant issue. To the authors’ knowledge, the potential BMD difference between the two femurs in scoliotic patients routinely undergoing DXA has never been studied. The hypothesis of the present study was that a significant difference in BMD exists between femurs in patients with scoliosis. Thus, the aim of the present study was to test this in scoliotic patients routinely undergoing DXA, and to also evaluate whether the difference is related to spine convexity.
Materials and methods
[mean SD; three males (age 63 13 years) and 94 postmenopausal women (age 67 11 years)], who underwent a DXA examination of the lumbar spine and both femurs. All DXA examinations were performed using a Hologic QDR Delphi W unit (Apex Software v. 3.0.1, Hologic Inc., Bedford, MA, USA). The least significant change (LSC), calculated as previously reported by Hamdy et al.,9 was used as a threshold of measurement precision. Femoral neck LSC for our DXA system was 0.029 g/cm2. All examinations were acquired and processed according to ISCD guidelines.7 In particular, the patient was repositioned for each of the three acquisition sites. The present study was concerned with the evaluation of femoral neck BMD values; results of spine BMD are not considered in this report, as scoliosis affects these values.14,18,19
Analysis in respect of spine convexity BMDIpsilateral was the BMD value measured on the femur ipsilateral to spine convexity and BMDcontralateral was that of the contralateral femur in each patient. The difference in ipsilateral versus contralateral (DBMDIC) femoral neck BMD was calculated as
DBMDIC ¼ BMDipsilateral BMDcontralateral As neither BMDipsilateral or BMDcontralateral may be considered as a reference, DBMDIC was normalized to their mean as BMDipsilateral BMDcontralateral 100 DBMD%IC ¼ Mean BMDipsilateral BMDcontralateral Regarding the T-score, the absolute difference (DTIC) and the percent difference (DT%IC) were calculated in the same way as for the BMD.
Analysis regardless of spine convexity Local ethics committee approval was obtained for this retrospective study and informed consent was waived. All patients had given written informed consent for the potential use of results of their examination for scientific purposes. Using the digital archive system, DXA examinations of 1080 patients performed at our tertiary university hospital from February to June 2011 were reviewed. DXA images of the lumbar spine were used for scoliosis detection (left or right convexity) and grading (Cobb’s angle), as reported by Urrutia et al.15 This method of patient selection was based on the demonstration of a close correlation between Cobb’s angle measured on DXA and that measured on anteroposterior lumbar radiographs,14 and on the definition of scoliosis as a deviation of the spine in the coronal plane of 10 .16,17 Lumbar scoliosis was detected in 127 (12%) patients. Thirty patients with previous osteoporotic fractures, metallic implants, or other metallic devices, extensive soft-tissue calcifications, or imaging artefacts were excluded. Thus, the cohort included 97 scoliotic patients aged 67 11 years
BMDhigher was the higher BMD between the femurs, and BMDlower was the lower BMD for each patient. Their difference (DBMDHL) was calculated as
DBMDHL ¼ BMDhigher BMDlower As neither BMDhigher or BMDlower may be considered as a reference, DBMDHL was normalized to their mean as BMDhigher BMDlower 100 DBMD%HL ¼ Mean BMDhigher BMDlower Regarding the T-score, the absolute difference (DTHL) and the percent difference (DT%HL) were calculated in the same way as for BMD. Diagnosis was defined based on the lower femoral Tscore. According to the World Health Organization (WHO), patients were considered normal when T 1, osteopenic when 2.5 < T < 1, or osteoporotic when T 2.5.7
M. Bandirali et al. / Clinical Radiology 68 (2013) e511ee515
The median BMD ipsilateral to the spinal convexity or of the femur with the higher BMD value were compared to BMD contralateral to the spine convexity or of the femur with the lower BMD value, using the Student’s t-test. The median T-scores ipsilateral to spine convexity or of the femur with the higher BMD value were compared to T-scores contralateral to the spine convexity or of the femur with the lower BMD value using the Wilcoxon’s signed-rank test. Continuous data were presented as mean standard deviations and p < 0.05 was considered significant. SPSS software (v. 19, IBM, Armonk, NY, USA) was used.
Results In the present series, 59/97 patients (61%) were affected by left-sided scoliosis, whereas 38/97 patients (39%) were affected by right-sided scoliosis. Considering the lowest femoral neck T-score value between both femurs, 32/97 patients (33%) were diagnosed with osteoporosis and 54/97 patients (56%) were diagnosed with osteopenia, whereas 11/97 patients (11%) had a normal T-score value.
Analysis in respect of spine convexity Mean BMDipsilateral was significantly lower (0.629 0.108 g/cm2) than BMDcontralateral (0.653 0.118 g/cm2; p < 0.001). However, the mean DBMDIC was 0.024 g/cm2 (mean DBMD%IC ¼ 4%), lower than the LSC threshold. The mean T-scoreipsilateral was significantly lower (2.0 0.9) than the T-scorecontralateral (1.8 1.0; p < 0.001). The mean DTOC was 0.2 (mean DT% IC¼ 12%). Out of 97 patients, 72 (74%) had BMDIpsilateral values lower than their BMDcontralateral. Using the LSC threshold, this value decreased to 46/97 patients (47%). Full data are reported in Table 1. Fig 1 shows a DXA examination of a patient affected by left-sided scoliosis.
Analysis regardless of spine convexity The difference between BMDhigher (0.664 0.116 g/cm2) and BMDlower (0.617 0.106 g/cm2) was statistically significant (p < 0.001). The mean DBMDHLwas 0.047 g/cm2 (mean DBMD%HL ¼ 7.3%), higher than the LSC threshold. The difference between the mean T-scorehigher (1.7 1.0) and the mean T-scorelower (2.1 0.9; p < 0.001) was statistically significant (p < 0.001). The mean DTHL was 0.4 (mean DT%HL ¼ 32%). Out of 97 patients, 95 (98%) had different BMD values between femurs. Using the LSC threshold, this value decreased to 66/97 patients (68%). Full data are reported in Table 2. Among these 66 patients, considering two different
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scenarios in which DXA is performed on the femoral neck with the higher or lower BMD, respectively, a variation of densitometric diagnosis based on WHO recommendation was seen in 29/66 patients (44%), and in 29/97 patients overall (30%). Full data are reported in Table 3.
Discussion The present study confirmed the hypothesis that, in patients affected by lumbar spine scoliosis detected at DXA, BMD values measured on both femoral necks are significantly different. Also, differences were not related to spine convexity. Differences between the BMD values of the two femoral necks of the same patient are still a debated topic. Some authors19,20 have demonstrated that there is no difference in BMD between the femurs of the same patient, whereas others report significant differences.9,10 This latter issue is taken into account in the ISCD 2007 guidelines7 that suggest performing DXA on both femurs of the same patient and to choose the lower value to establish a diagnosis of osteoporosis. It is known that a correlation exists between osteoporosis and scoliosis18,21 and vice versa.22,23 Also, some reports describe the presence of loading imbalance on lower limbs due to scoliosis. Although some authors show no difference in terms of static strength between the two sides,24 it is well known that bone architecture and its mineral density are widely influenced by dynamic forces.10,25 Thus, regardless of the reasons, the evidence of a difference between two femurs in a scoliotic patient is largely expected. The only paper reporting such a topic was published in 1996 by Hans et al.,13 who reported that the BMDipsilateral was lower than the BMDcontralateral in a small sample of 15 women. These data are not consistent with what we have found, as in the present series less than half the patients had BMDipsilateral < BMDcontralateral. Conversely, about one out of five patients in the present series had an unexpected value of BMDipsilateral > BMDcontralateral. These data may have different explanations. First, the sample size is six-times larger than that reported by Hans et al.13 Thus, their data may not be reproduced on a larger scale. Also, the present population mainly included post-menopausal women routinely undergoing DXA for osteoporosis detection. This is different to that reported by Hans et al.,13 whose series included 11 pre-menopausal and four postmenopausal women, with a mean age of 45 years. Furthermore those patients were affected by untreated adolescent structural lumbar idiopathic scoliosis, whereas no data regarding scoliosis type are available in the present series. However, primary degenerative scoliosis is the most frequent type in the elderly population.16,17
Table 1 Comparison of femoral neck bone mineral density (BMD) according to spine convexity. BMD
Regardless least significant change threshold Using least significant change threshold
Ipsilateral < contralateral
Ipsilateral ¼ contralateral
Ipsilateral > contralateral
72/97 (74%) 46/97 (47%)
2/97 (2%) 31/97 (32%)
23/97 (24%) 20/97 (21%)
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Figure 1 DXA images of a patient affected by left-sided scoliosis. (a) Lumbar spine scan. Cobb’s angle was 16 . Femoral scan performed on the femoral neck (b) contralateral and (c) ipsilateral to the spine convexity. Note that the T-score decreases from e2.1 to e2.7, implying a diagnosis variation from osteopenia to osteoporosis.
Regardless of spine convexity, over two-thirds of patients have different femoral neck BMD values between femurs. These data imply that in about one-third of patients included in the present series there is a variation of diagnosis from normal to osteopenia and from osteopenia to osteoporosis (see Table 3). However, if small differences around the diagnostic threshold cause a variation in diagnosis, larger differences close to the mean of the diagnostic interval do not produce any effect. Thus, these data may be underestimated. Table 2 Comparison of femoral neck bone mineral density (BMD) regardless to spine convexity. BMD Different between femurs Regardless least significant change threshold Using least significant change threshold
Non different between femurs
95/97 (98%)
2/97 (2%)
66/97 (68%)
31/97 (32%)
The present report focused on the evaluation of femoral neck BMD values only for two main reasons. First, the WHO international reference standard for osteoporosis diagnosis is a T-score of 2.5 or less measured at the femoral neck.7 Also femoral neck BMD is recommended for use in FRAXÒ, a diagnostic tool developed by WHO used to evaluate the 10-year probability of bone fracture risk.26 The clinical implications of the present results may be appreciated considering that more than two-thirds of the present patients showed a BMD difference between the two femurs regardless of spine convexity. As it is unknown a priori which femur has the lowest BMD, it is recommended that all scoliotic patients detected at spine DXA should undergo bilateral femoral DXA. In other words, the ISCD guideline suggesting the study of both femurs for all patients7 should be considered mandatory for scoliotic patients. Apart from the retrospective nature of the study, the main limitation of this work is that lumbar DXA was used for identification of scoliosis. Thus, the evaluation was limited to the lumbar spine and scoliotic curvature of the
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Table 3 Variation of densitometric diagnosis according to higher or lower femoral neck bone mineral density (BMD) based on World Health Organization recommendation in 66 patients with BMD difference between femurs higher than least significant change. Higher BMD femoral neck
Lower BMD femoral neck
Number of patients
Totala
Overallb
From
Normal Osteopenia Osteoporosis
To
Normal Osteopenia Osteoporosis
8/66 (12%) 22/66 (33%) 7/66 (11%)
37/66 (56%)
37/97 (38%)
From
Normal Osteopenia
To
Osteopenia Osteoporosis
10/66 (15%) 19/66 (29%)
29/66 (44%)
29/97 (30%)
a b
Values reported are related to 66 patients. Values reported represent comparison to whole study population.
whole spine could not be evaluated. Regarding the reliability of detecting scoliosis at DXA, it has been demonstrated that Cobb’s angle measured by DXA is comparable to that obtained with conventional radiographs allowing a reliable definition of scoliosis.14,15 However, knowledge of only the lumbar spine deserves some consideration. The presence of a second curvature in the dorsal spine opposite to that in the lumbar spine makes the distinction between ipsilateral and contralateral convexity somewhat arbitrary and may explain paradoxical cases. However, regardless of the side of convexity, a significant BMD difference does exist between the two femurs. Future studies are warranted in order to investigate how whole-spine scoliotic curvature impacts on the BMD of the two femurs. In conclusion, the present study demonstrated that a difference in femoral neck BMD exists between the two femurs of scoliotic patients undergoing DXA. For these patients, bilateral femoral DXA acquisition should be recommended.
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