- Email: [email protected]
Cortical stability of the femoral neck and hip fracture risk – Authors' reply
Correspondence
difficult to accept a singular focus on the superolateral cortex in causing femoral neck fragility fractures. Second, whereas Mayhew and colleagues are correct in stating that non-human apes have symmetrically thick femoral neck cortices, this is the exception to the rule within primates.5 Quadrupedal primates generally have asymmetrical femoral neck cortices, where the superior cortex is much thinner than the inferior cortex. Thus, the overall structure of femoral neck cortices is similar in many animals and human beings despite postural and locomotor differences, yet femoral neck fragility fractures are rare in animals. A prominent distinction between these species and human beings is their greater femoral neck trabecular bone volume throughout life. Finally, Mayhew and colleagues’ own results belie the primary importance of the age-related thinning of the superolateral cortex in femoral neck fragility fractures. Their measurements of superolateral cortex thickness did not differ between patients with and without hip fractures. This finding implies that other structural features or bone material properties might be altered in individuals with hip fracture. In conclusion, Mayhew and colleagues have reported new observations about age-related changes in cortical geometry in the proximal femur. However, their own data as well as observations from other studies do not support their tenet that thinning of the superolateral cortex is the predominant mechanism underlying increased femoral fragility with ageing. Interventions to reduce hip fracture risk should target all the potential contributors to femoral fragility, including trabecular bone. We declare that we have no conflict of interest.
*Mary L Bouxsein, Roberto J Fajardo [email protected] Orthopedic Biomechanics Laboratory, Beth Israel Deaconess Medical Center, Boston, MA 02215, USA
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Mayhew PM, Thomas CD, Clement JG, et al. Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet 2005; 366: 129–35. Rogers RR, La Barbara M. Contribution of internal bony trabecular to the mechanical properties of the humerus of the pigeon (Columba livia). J Zoology London 1993; 230: 433–31. Riggs BL, Melton LJ, Robb RA, et al. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res 2004; 19: 1945–54. Lotz JC, Cheal EJ, Hayes WC. Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int 1995; 5: 252–61. Rafferty KL. Structural design of the femoral neck in primates. J Hum Evol 1998; 34: 361–83.
Authors’ reply R M D Zebaze and E Seeman raise important issues. Femoral neck trabecular bone density in our female patients declined by 10·3% of the mean per decade; these findings were similar to the population-based results of Riggs and colleagues.1 So half of all trabeculae are probably lost by age 80 years, and from our equations for critical stress (), at thicknesses typically of 0·12–0·30 mm, the remainder will be prone to buckle at loads 50–95% lower than would buckle the thinnest cortical segment. Trabeculae can only therefore function usefully by shortening the unsupported length (L) of elements of the cortex, or as in aircraft wings as shock absorbers. Moreover, trabecular protection against Euler buckling could be four-fold compromised by ageing according to the second formula, since mean L doubles. We did not downwardly adjust for trabecular bone loss, so our estimates of the loss
Subperiosteal Women Men Endocortical Women Men
of cortical with ageing might be insufficient. We accept Mary Bouxsein and Roberto Fajardo’s point that cortical and trabecular bone act in synergy. However, trabeculae are positioned more centrally than the cortex, which reduces their relative resistance to bending. Hirsch and Brodetti removed the trabeculae from the upper femur, reducing its elasticity by 30% in stance.2 But this might be irrelevant to hip fracture when femoral trabeculae are oriented to resist stresses from stance, not from falling sideways. Trabeculae providing radial support to resist buckling are lost preferentially. The data requested by Zebaze and Seeman on femoral neck width are shown in the table. Reid and colleagues3 found no secular decrease in femoral neck width, so the age effect on inferior cortical thickness in a single 1/16 sector is unlikely to be due to this, nor do we accept that our data are implausible. First, figure 2, B in our paper shows that that the lower bound of the 95% CI for this rate of increase is only a third of the estimate. Second, bone formation rates quoted by Zebaze and Seeman for the iliac periosteum are inappropriate; Power and colleagues’ data indicate a fourfold higher rate at the femoral neck4 than ilium, allowing for methodological differences. Lastly, longitudinal in-vivo studies suggest that subperiosteal and endosteal femoral neck widths increase, especially in older women;1 this can only occur through subperiosteal bone formation. In the Study of Osteoporotic Fractures, Beck
Mean width at age 60 (mm)
Change/decade of age (mm)
p for age effect
RMS error (mm)
35·7 41·1
0·3 0·1
0·1 0·7
2·4 3·1
30·9 36·0
0·2 0·1
0·4 0·6
2·4 3·3
RMS=root mean square.
Table: Superolateral-inferomedial femoral neck widths normal to its axis
www.thelancet.com Vol 366 October 29, 2005
Correspondence
and colleagues5 found that rates of increase in femoral neck width averaged 0·28% per year. The evidence is that hip bending resistance is maintained by cortical adaptation in the face of trabecular losses. The other points of Zebaze and Seeman were discussed in our paper, with some answers awaiting future research, including longitudinal invivo studies of cortical thickness for which CT methods remain limiting in their anatomical resolution. We tackled the analysis of the elastic stability of geometrically complex structures using a segmental approach because, in a shell-like structure, once any segment buckles the others undergo increased strain, accelerating the propagation of cracks started by the initial destabilisation, and commonly resulting in a domino-like collapse. We measured surface curvature directly and presented our results: unexpectedly the less curved it was, the thinner was the cortex and so with loss of curvature it became doubly vulnerable. Agreed, this emphasises the need for future studies of trabecular buttressing. Higher resolution CT will make this possible ex vivo. The purpose of our study was descriptive and quantitative. Its results were qualitatively predicted by previous work. We drew attention to a major difference in structure between young and old femoral necks that has profound implications for resistance to fracture. We hope our work will accelerate a growing understanding of the fracture mechanics of the elderly hip. It can now be envisaged how ageing and lifestyle might substantially modify the effects of postmenopausal osteoporosis on hip fragility. Further references available from the authors. We thank John C Clement, Thomas J Beck, and William Bonfield for contributing to discussions on this response. We declare that we have no conflicts of interest other than those stated in the original paper.
*Jonathan Reeve, Paul M Mayhew, C David Thomas, Nigel Loveridge, Chris J Burgoyne [email protected] www.thelancet.com Vol 366 October 29, 2005
Department of Medicine (JR, PMM, NL) and Engineering (CJB), University of Cambridge, Cambridge CB2 2QQ, UK; and School of Dental Science, University of Melbourne, Victoria, Australia (CDT) 1
2
3
4
5
Riggs BL, Melton 3 LJ, Robb RA, et al. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res 2004; 19: 1945–54. Hirsch C, Brodetti A. The weight-bearing capacity of structural elements in femoral necks. Acta Orthop Scand 1956; 26: 15–24. Reid IR, Chin K, Evans MC, Jones JG. Relation between increase in length of hip axis in older women between 1950s and 1990s and increase in age-specific rates of hip fracture. BMJ 1994; 309: 508–09. Power J, Loveridge N, Lyon A, Rushton N, Parker M, Reeve J. Osteoclastic cortical erosion as a determinant of sub-periosteal osteoblastic bone formation in the femoral neck’s response to BMU imbalance: effects of stance-related loading and hip fracture. Osteoporos Int 2005; 16: 1049–56. Beck TJ, Oreskovic TL, Stone KL, et al. Structural adaptation to changing skeletal load in the progression towards hip fragility: the Study of Osteoporotic Fractures. J Bone Miner Res 2001; 16: 1108–19.
We agree with Paul Mayhew and colleagues1 that hip fragility increases with normal ageing because the upper femoral neck cortex becomes thinner. Hip fractures comprise two types— femoral neck (cervical or intracapsular) and trochanteric (extracapsular)—and atrophic thinning in the superolateral region would be associated with the former type of hip fracture. This suggestion is consistent with a previous finding in the EPIDOS study2 that prediction of femoral neck fracture was enhanced by the upper part, but not lower part, of femoral neck areal bone mineral density. Mayhew and colleagues show that there is considerable variation (0·6–1·2 mm) in femoral neck cortical thickness in the superoposterior sector in elderly women. Therefore, it is important to understand the factors that affect cortical thinning of the superoposterior femoral neck. From a biomechanical point of view, not only physical activity but also femoral neck geometry such as femoral neck-shaft and anteversion angles and hip axis length could be related to femoral neck cortical thickness because bone strain
generated by mechanical loading is one of the most pivotal factors in controlling bone mass.3 Femoral neck-shaft and anteversion angles show wide ranges in normal individuals, and averages of these angles decrease with growth from 150º and 40º, respectively, at birth to 130º and 15º, respectively, in adults. Larger angles of femoral neck-shaft and anteversion could cause thinner superior and posterior cortices of the femoral neck, respectively, resulting from a decrease in bone strain from loading. Similarly, shorter hip axis length could also induce the thinner upper cortex because of a smaller bone strain. However, in a sideways fall, the risk of femoral neck fracture could become higher when femoral neckshaft angle is larger or hip axis length is longer. These could explain previous findings that the femoral neck-shaft angle seems to be an indicator of femoral neck fracture risk, whereas the relation between hip axis length and femoral neck fracture risk remains controversial.4 High physical activity including targeted exercise in children might be useful for the improvement of agerelated hip fragility in adults, because there is a general inverse relation between mechanical loading levels in the proximal femur and femoral neckshaft angle. However, sitting with legs in the W position during childhood is not recommended because such a habit impairs physiological reduction of femoral anteversion. Little is known about the relation between femoral anteversion angle and femoral neck fracture risk, but reduction of posterior cortical thickness in the femoral neck could be linked to femoral anteversion. Therefore, not only femoral neckshaft angle but also anteversion angle might be useful parameters for predicting femoral neck fracture risk. Finally, hip fracture risk should be assessed separately as the risk of femoral neck and trochanteric hip fractures, because there is a different patho1525
difficult to accept a singular focus on the superolateral cortex in causing femoral neck fragility fractures. Second, whereas Mayhew and colleagues are correct in stating that non-human apes have symmetrically thick femoral neck cortices, this is the exception to the rule within primates.5 Quadrupedal primates generally have asymmetrical femoral neck cortices, where the superior cortex is much thinner than the inferior cortex. Thus, the overall structure of femoral neck cortices is similar in many animals and human beings despite postural and locomotor differences, yet femoral neck fragility fractures are rare in animals. A prominent distinction between these species and human beings is their greater femoral neck trabecular bone volume throughout life. Finally, Mayhew and colleagues’ own results belie the primary importance of the age-related thinning of the superolateral cortex in femoral neck fragility fractures. Their measurements of superolateral cortex thickness did not differ between patients with and without hip fractures. This finding implies that other structural features or bone material properties might be altered in individuals with hip fracture. In conclusion, Mayhew and colleagues have reported new observations about age-related changes in cortical geometry in the proximal femur. However, their own data as well as observations from other studies do not support their tenet that thinning of the superolateral cortex is the predominant mechanism underlying increased femoral fragility with ageing. Interventions to reduce hip fracture risk should target all the potential contributors to femoral fragility, including trabecular bone. We declare that we have no conflict of interest.
*Mary L Bouxsein, Roberto J Fajardo [email protected] Orthopedic Biomechanics Laboratory, Beth Israel Deaconess Medical Center, Boston, MA 02215, USA
1524
1
2
3
4
5
Mayhew PM, Thomas CD, Clement JG, et al. Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet 2005; 366: 129–35. Rogers RR, La Barbara M. Contribution of internal bony trabecular to the mechanical properties of the humerus of the pigeon (Columba livia). J Zoology London 1993; 230: 433–31. Riggs BL, Melton LJ, Robb RA, et al. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res 2004; 19: 1945–54. Lotz JC, Cheal EJ, Hayes WC. Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int 1995; 5: 252–61. Rafferty KL. Structural design of the femoral neck in primates. J Hum Evol 1998; 34: 361–83.
Authors’ reply R M D Zebaze and E Seeman raise important issues. Femoral neck trabecular bone density in our female patients declined by 10·3% of the mean per decade; these findings were similar to the population-based results of Riggs and colleagues.1 So half of all trabeculae are probably lost by age 80 years, and from our equations for critical stress (), at thicknesses typically of 0·12–0·30 mm, the remainder will be prone to buckle at loads 50–95% lower than would buckle the thinnest cortical segment. Trabeculae can only therefore function usefully by shortening the unsupported length (L) of elements of the cortex, or as in aircraft wings as shock absorbers. Moreover, trabecular protection against Euler buckling could be four-fold compromised by ageing according to the second formula, since mean L doubles. We did not downwardly adjust for trabecular bone loss, so our estimates of the loss
Subperiosteal Women Men Endocortical Women Men
of cortical with ageing might be insufficient. We accept Mary Bouxsein and Roberto Fajardo’s point that cortical and trabecular bone act in synergy. However, trabeculae are positioned more centrally than the cortex, which reduces their relative resistance to bending. Hirsch and Brodetti removed the trabeculae from the upper femur, reducing its elasticity by 30% in stance.2 But this might be irrelevant to hip fracture when femoral trabeculae are oriented to resist stresses from stance, not from falling sideways. Trabeculae providing radial support to resist buckling are lost preferentially. The data requested by Zebaze and Seeman on femoral neck width are shown in the table. Reid and colleagues3 found no secular decrease in femoral neck width, so the age effect on inferior cortical thickness in a single 1/16 sector is unlikely to be due to this, nor do we accept that our data are implausible. First, figure 2, B in our paper shows that that the lower bound of the 95% CI for this rate of increase is only a third of the estimate. Second, bone formation rates quoted by Zebaze and Seeman for the iliac periosteum are inappropriate; Power and colleagues’ data indicate a fourfold higher rate at the femoral neck4 than ilium, allowing for methodological differences. Lastly, longitudinal in-vivo studies suggest that subperiosteal and endosteal femoral neck widths increase, especially in older women;1 this can only occur through subperiosteal bone formation. In the Study of Osteoporotic Fractures, Beck
Mean width at age 60 (mm)
Change/decade of age (mm)
p for age effect
RMS error (mm)
35·7 41·1
0·3 0·1
0·1 0·7
2·4 3·1
30·9 36·0
0·2 0·1
0·4 0·6
2·4 3·3
RMS=root mean square.
Table: Superolateral-inferomedial femoral neck widths normal to its axis
www.thelancet.com Vol 366 October 29, 2005
Correspondence
and colleagues5 found that rates of increase in femoral neck width averaged 0·28% per year. The evidence is that hip bending resistance is maintained by cortical adaptation in the face of trabecular losses. The other points of Zebaze and Seeman were discussed in our paper, with some answers awaiting future research, including longitudinal invivo studies of cortical thickness for which CT methods remain limiting in their anatomical resolution. We tackled the analysis of the elastic stability of geometrically complex structures using a segmental approach because, in a shell-like structure, once any segment buckles the others undergo increased strain, accelerating the propagation of cracks started by the initial destabilisation, and commonly resulting in a domino-like collapse. We measured surface curvature directly and presented our results: unexpectedly the less curved it was, the thinner was the cortex and so with loss of curvature it became doubly vulnerable. Agreed, this emphasises the need for future studies of trabecular buttressing. Higher resolution CT will make this possible ex vivo. The purpose of our study was descriptive and quantitative. Its results were qualitatively predicted by previous work. We drew attention to a major difference in structure between young and old femoral necks that has profound implications for resistance to fracture. We hope our work will accelerate a growing understanding of the fracture mechanics of the elderly hip. It can now be envisaged how ageing and lifestyle might substantially modify the effects of postmenopausal osteoporosis on hip fragility. Further references available from the authors. We thank John C Clement, Thomas J Beck, and William Bonfield for contributing to discussions on this response. We declare that we have no conflicts of interest other than those stated in the original paper.
*Jonathan Reeve, Paul M Mayhew, C David Thomas, Nigel Loveridge, Chris J Burgoyne [email protected] www.thelancet.com Vol 366 October 29, 2005
Department of Medicine (JR, PMM, NL) and Engineering (CJB), University of Cambridge, Cambridge CB2 2QQ, UK; and School of Dental Science, University of Melbourne, Victoria, Australia (CDT) 1
2
3
4
5
Riggs BL, Melton 3 LJ, Robb RA, et al. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res 2004; 19: 1945–54. Hirsch C, Brodetti A. The weight-bearing capacity of structural elements in femoral necks. Acta Orthop Scand 1956; 26: 15–24. Reid IR, Chin K, Evans MC, Jones JG. Relation between increase in length of hip axis in older women between 1950s and 1990s and increase in age-specific rates of hip fracture. BMJ 1994; 309: 508–09. Power J, Loveridge N, Lyon A, Rushton N, Parker M, Reeve J. Osteoclastic cortical erosion as a determinant of sub-periosteal osteoblastic bone formation in the femoral neck’s response to BMU imbalance: effects of stance-related loading and hip fracture. Osteoporos Int 2005; 16: 1049–56. Beck TJ, Oreskovic TL, Stone KL, et al. Structural adaptation to changing skeletal load in the progression towards hip fragility: the Study of Osteoporotic Fractures. J Bone Miner Res 2001; 16: 1108–19.
We agree with Paul Mayhew and colleagues1 that hip fragility increases with normal ageing because the upper femoral neck cortex becomes thinner. Hip fractures comprise two types— femoral neck (cervical or intracapsular) and trochanteric (extracapsular)—and atrophic thinning in the superolateral region would be associated with the former type of hip fracture. This suggestion is consistent with a previous finding in the EPIDOS study2 that prediction of femoral neck fracture was enhanced by the upper part, but not lower part, of femoral neck areal bone mineral density. Mayhew and colleagues show that there is considerable variation (0·6–1·2 mm) in femoral neck cortical thickness in the superoposterior sector in elderly women. Therefore, it is important to understand the factors that affect cortical thinning of the superoposterior femoral neck. From a biomechanical point of view, not only physical activity but also femoral neck geometry such as femoral neck-shaft and anteversion angles and hip axis length could be related to femoral neck cortical thickness because bone strain
generated by mechanical loading is one of the most pivotal factors in controlling bone mass.3 Femoral neck-shaft and anteversion angles show wide ranges in normal individuals, and averages of these angles decrease with growth from 150º and 40º, respectively, at birth to 130º and 15º, respectively, in adults. Larger angles of femoral neck-shaft and anteversion could cause thinner superior and posterior cortices of the femoral neck, respectively, resulting from a decrease in bone strain from loading. Similarly, shorter hip axis length could also induce the thinner upper cortex because of a smaller bone strain. However, in a sideways fall, the risk of femoral neck fracture could become higher when femoral neckshaft angle is larger or hip axis length is longer. These could explain previous findings that the femoral neck-shaft angle seems to be an indicator of femoral neck fracture risk, whereas the relation between hip axis length and femoral neck fracture risk remains controversial.4 High physical activity including targeted exercise in children might be useful for the improvement of agerelated hip fragility in adults, because there is a general inverse relation between mechanical loading levels in the proximal femur and femoral neckshaft angle. However, sitting with legs in the W position during childhood is not recommended because such a habit impairs physiological reduction of femoral anteversion. Little is known about the relation between femoral anteversion angle and femoral neck fracture risk, but reduction of posterior cortical thickness in the femoral neck could be linked to femoral anteversion. Therefore, not only femoral neckshaft angle but also anteversion angle might be useful parameters for predicting femoral neck fracture risk. Finally, hip fracture risk should be assessed separately as the risk of femoral neck and trochanteric hip fractures, because there is a different patho1525