Impaired bone quality in the superolateral femoral neck occurs independent of hip geometry and bone mineral density
Skeletal adaptation is substantially influenced by mechanical loads. Osteocytes and their lacuno-canalicular network have been identified as a key player in load sensation and bone quality regulation. In the femoral neck, one of the most common fracture sites, a complex loading pattern with lower ha...
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          | Published in | Acta biomaterialia Vol. 141; pp. 233 - 243 | 
|---|---|
| Main Authors | , , , , , , , , , | 
| Format | Journal Article | 
| Language | English | 
| Published | 
        England
          Elsevier Ltd
    
        15.03.2022
     Elsevier BV  | 
| Subjects | |
| Online Access | Get full text | 
| ISSN | 1742-7061 1878-7568 1878-7568  | 
| DOI | 10.1016/j.actbio.2022.01.002 | 
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| Abstract | Skeletal adaptation is substantially influenced by mechanical loads. Osteocytes and their lacuno-canalicular network have been identified as a key player in load sensation and bone quality regulation. In the femoral neck, one of the most common fracture sites, a complex loading pattern with lower habitual loading in the superolateral neck and higher compressive stresses in the inferomedial neck is present. Variations in the femoral neck-shaft angle (NSA), i.e., coxa vara or coxa valga, provide the opportunity to examine the influence of loading patterns on bone quality. We obtained femoral neck specimens of 28 osteoarthritic human subjects with coxa vara, coxa norma and coxa valga during total hip arthroplasty. Bone mineral density (BMD) was assessed preoperatively by dual energy X-ray absorptiometry (DXA). Cortical and trabecular microstructure and three-dimensional osteocyte lacunar characteristics were assessed in the superolateral and inferomedial neck using ex vivo high resolution micro-computed tomography. Additionally, BMD distribution and osteocyte lacunar characteristics were analyzed by quantitative backscattered electron imaging (qBEI). All groups presented thicker inferomedial than superolateral cortices. Furthermore, the superolateral site exhibited a lower osteocyte lacunar density along with lower lacunar sphericity than the inferomedial site, independent of NSA. Importantly, BMD and corresponding T-scores correlated with microstructural parameters at the inferomedial but not superolateral neck. In conclusion, we provide micromorphological evidence for fracture vulnerability of the superolateral neck, which is independent of NSA and BMD. The presented bone qualitative data provide an explanation why DXA may be insufficient to predict a substantial proportion of femoral neck fractures.
The femoral neck, one of the most common fracture sites, is subject to a complex loading pattern. Site-specific differences (i.e., superolateral vs. inferomedial) in bone quality influence fracture risk, but it is unclear how this relates to hip geometry and bone mineral density (BMD) measurements in vivo. Here, we examine femoral neck specimens using a variety of high-resolution imaging techniques and demonstrate impaired bone quality in the superolateral compared to the inferomedial neck. Specifically, we found impaired cortical and trabecular microarchitecture, mineralization, and osteocyte properties, regardless of neck-shaft angle. Since BMD correlated with bone quality of the inferomedial but not the superolateral neck, our results illustrate why bone densitometry may not predict a substantial proportion of femoral neck fractures.
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| AbstractList | Skeletal adaptation is substantially influenced by mechanical loads. Osteocytes and their lacuno-canalicular network have been identified as a key player in load sensation and bone quality regulation. In the femoral neck, one of the most common fracture sites, a complex loading pattern with lower habitual loading in the superolateral neck and higher compressive stresses in the inferomedial neck is present. Variations in the femoral neck-shaft angle (NSA), i.e., coxa vara or coxa valga, provide the opportunity to examine the influence of loading patterns on bone quality. We obtained femoral neck specimens of 28 osteoarthritic human subjects with coxa vara, coxa norma and coxa valga during total hip arthroplasty. Bone mineral density (BMD) was assessed preoperatively by dual energy X-ray absorptiometry (DXA). Cortical and trabecular microstructure and three-dimensional osteocyte lacunar characteristics were assessed in the superolateral and inferomedial neck using ex vivo high resolution micro-computed tomography. Additionally, BMD distribution and osteocyte lacunar characteristics were analyzed by quantitative backscattered electron imaging (qBEI). All groups presented thicker inferomedial than superolateral cortices. Furthermore, the superolateral site exhibited a lower osteocyte lacunar density along with lower lacunar sphericity than the inferomedial site, independent of NSA. Importantly, BMD and corresponding T-scores correlated with microstructural parameters at the inferomedial but not superolateral neck. In conclusion, we provide micromorphological evidence for fracture vulnerability of the superolateral neck, which is independent of NSA and BMD. The presented bone qualitative data provide an explanation why DXA may be insufficient to predict a substantial proportion of femoral neck fractures.
The femoral neck, one of the most common fracture sites, is subject to a complex loading pattern. Site-specific differences (i.e., superolateral vs. inferomedial) in bone quality influence fracture risk, but it is unclear how this relates to hip geometry and bone mineral density (BMD) measurements in vivo. Here, we examine femoral neck specimens using a variety of high-resolution imaging techniques and demonstrate impaired bone quality in the superolateral compared to the inferomedial neck. Specifically, we found impaired cortical and trabecular microarchitecture, mineralization, and osteocyte properties, regardless of neck-shaft angle. Since BMD correlated with bone quality of the inferomedial but not the superolateral neck, our results illustrate why bone densitometry may not predict a substantial proportion of femoral neck fractures.
[Display omitted] Skeletal adaptation is substantially influenced by mechanical loads. Osteocytes and their lacuno-canalicular network have been identified as a key player in load sensation and bone quality regulation. In the femoral neck, one of the most common fracture sites, a complex loading pattern with lower habitual loading in the superolateral neck and higher compressive stresses in the inferomedial neck is present. Variations in the femoral neck-shaft angle (NSA), i.e., coxa vara or coxa valga, provide the opportunity to examine the influence of loading patterns on bone quality. We obtained femoral neck specimens of 28 osteoarthritic human subjects with coxa vara, coxa norma and coxa valga during total hip arthroplasty. Bone mineral density (BMD) was assessed preoperatively by dual energy X-ray absorptiometry (DXA). Cortical and trabecular microstructure and three-dimensional osteocyte lacunar characteristics were assessed in the superolateral and inferomedial neck using ex vivo high resolution micro-computed tomography. Additionally, BMD distribution and osteocyte lacunar characteristics were analyzed by quantitative backscattered electron imaging (qBEI). All groups presented thicker inferomedial than superolateral cortices. Furthermore, the superolateral site exhibited a lower osteocyte lacunar density along with lower lacunar sphericity than the inferomedial site, independent of NSA. Importantly, BMD and corresponding T-scores correlated with microstructural parameters at the inferomedial but not superolateral neck. In conclusion, we provide micromorphological evidence for fracture vulnerability of the superolateral neck, which is independent of NSA and BMD. The presented bone qualitative data provide an explanation why DXA may be insufficient to predict a substantial proportion of femoral neck fractures. STATEMENT OF SIGNIFICANCE: The femoral neck, one of the most common fracture sites, is subject to a complex loading pattern. Site-specific differences (i.e., superolateral vs. inferomedial) in bone quality influence fracture risk, but it is unclear how this relates to hip geometry and bone mineral density (BMD) measurements in vivo. Here, we examine femoral neck specimens using a variety of high-resolution imaging techniques and demonstrate impaired bone quality in the superolateral compared to the inferomedial neck. Specifically, we found impaired cortical and trabecular microarchitecture, mineralization, and osteocyte properties, regardless of neck-shaft angle. Since BMD correlated with bone quality of the inferomedial but not the superolateral neck, our results illustrate why bone densitometry may not predict a substantial proportion of femoral neck fractures. Skeletal adaptation is substantially influenced by mechanical loads. Osteocytes and their lacuno-canalicular network have been identified as a key player in load sensation and bone quality regulation. In the femoral neck, one of the most common fracture sites, a complex loading pattern with lower habitual loading in the superolateral neck and higher compressive stresses in the inferomedial neck is present. Variations in the femoral neck-shaft angle (NSA), i.e., coxa vara or coxa valga, provide the opportunity to examine the influence of loading patterns on bone quality. We obtained femoral neck specimens of 28 osteoarthritic human subjects with coxa vara, coxa norma and coxa valga during total hip arthroplasty. Bone mineral density (BMD) was assessed preoperatively by dual energy X-ray absorptiometry (DXA). Cortical and trabecular microstructure and three-dimensional osteocyte lacunar characteristics were assessed in the superolateral and inferomedial neck using ex vivo high resolution micro-computed tomography. Additionally, BMD distribution and osteocyte lacunar characteristics were analyzed by quantitative backscattered electron imaging (qBEI). All groups presented thicker inferomedial than superolateral cortices. Furthermore, the superolateral site exhibited a lower osteocyte lacunar density along with lower lacunar sphericity than the inferomedial site, independent of NSA. Importantly, BMD and corresponding T-scores correlated with microstructural parameters at the inferomedial but not superolateral neck. In conclusion, we provide micromorphological evidence for fracture vulnerability of the superolateral neck, which is independent of NSA and BMD. The presented bone qualitative data provide an explanation why DXA may be insufficient to predict a substantial proportion of femoral neck fractures. Skeletal adaptation is substantially influenced by mechanical loads. Osteocytes and their lacuno-canalicular network have been identified as a key player in load sensation and bone quality regulation. In the femoral neck, one of the most common fracture sites, a complex loading pattern with lower habitual loading in the superolateral neck and higher compressive stresses in the inferomedial neck is present. Variations in the femoral neck-shaft angle (NSA), i.e., coxa vara or coxa valga, provide the opportunity to examine the influence of loading patterns on bone quality. We obtained femoral neck specimens of 28 osteoarthritic human subjects with coxa vara, coxa norma and coxa valga during total hip arthroplasty. Bone mineral density (BMD) was assessed preoperatively by dual energy X-ray absorptiometry (DXA). Cortical and trabecular microstructure and three-dimensional osteocyte lacunar characteristics were assessed in the superolateral and inferomedial neck using ex vivo high resolution micro-computed tomography. Additionally, BMD distribution and osteocyte lacunar characteristics were analyzed by quantitative backscattered electron imaging (qBEI). All groups presented thicker inferomedial than superolateral cortices. Furthermore, the superolateral site exhibited a lower osteocyte lacunar density along with lower lacunar sphericity than the inferomedial site, independent of NSA. Importantly, BMD and corresponding T-scores correlated with microstructural parameters at the inferomedial but not superolateral neck. In conclusion, we provide micromorphological evidence for fracture vulnerability of the superolateral neck, which is independent of NSA and BMD. The presented bone qualitative data provide an explanation why DXA may be insufficient to predict a substantial proportion of femoral neck fractures. STATEMENT OF SIGNIFICANCE: The femoral neck, one of the most common fracture sites, is subject to a complex loading pattern. Site-specific differences (i.e., superolateral vs. inferomedial) in bone quality influence fracture risk, but it is unclear how this relates to hip geometry and bone mineral density (BMD) measurements in vivo. Here, we examine femoral neck specimens using a variety of high-resolution imaging techniques and demonstrate impaired bone quality in the superolateral compared to the inferomedial neck. Specifically, we found impaired cortical and trabecular microarchitecture, mineralization, and osteocyte properties, regardless of neck-shaft angle. Since BMD correlated with bone quality of the inferomedial but not the superolateral neck, our results illustrate why bone densitometry may not predict a substantial proportion of femoral neck fractures.Skeletal adaptation is substantially influenced by mechanical loads. Osteocytes and their lacuno-canalicular network have been identified as a key player in load sensation and bone quality regulation. In the femoral neck, one of the most common fracture sites, a complex loading pattern with lower habitual loading in the superolateral neck and higher compressive stresses in the inferomedial neck is present. Variations in the femoral neck-shaft angle (NSA), i.e., coxa vara or coxa valga, provide the opportunity to examine the influence of loading patterns on bone quality. We obtained femoral neck specimens of 28 osteoarthritic human subjects with coxa vara, coxa norma and coxa valga during total hip arthroplasty. Bone mineral density (BMD) was assessed preoperatively by dual energy X-ray absorptiometry (DXA). Cortical and trabecular microstructure and three-dimensional osteocyte lacunar characteristics were assessed in the superolateral and inferomedial neck using ex vivo high resolution micro-computed tomography. Additionally, BMD distribution and osteocyte lacunar characteristics were analyzed by quantitative backscattered electron imaging (qBEI). All groups presented thicker inferomedial than superolateral cortices. Furthermore, the superolateral site exhibited a lower osteocyte lacunar density along with lower lacunar sphericity than the inferomedial site, independent of NSA. Importantly, BMD and corresponding T-scores correlated with microstructural parameters at the inferomedial but not superolateral neck. In conclusion, we provide micromorphological evidence for fracture vulnerability of the superolateral neck, which is independent of NSA and BMD. The presented bone qualitative data provide an explanation why DXA may be insufficient to predict a substantial proportion of femoral neck fractures. STATEMENT OF SIGNIFICANCE: The femoral neck, one of the most common fracture sites, is subject to a complex loading pattern. Site-specific differences (i.e., superolateral vs. inferomedial) in bone quality influence fracture risk, but it is unclear how this relates to hip geometry and bone mineral density (BMD) measurements in vivo. Here, we examine femoral neck specimens using a variety of high-resolution imaging techniques and demonstrate impaired bone quality in the superolateral compared to the inferomedial neck. Specifically, we found impaired cortical and trabecular microarchitecture, mineralization, and osteocyte properties, regardless of neck-shaft angle. Since BMD correlated with bone quality of the inferomedial but not the superolateral neck, our results illustrate why bone densitometry may not predict a substantial proportion of femoral neck fractures.  | 
    
| Author | von Kroge, Simon Rolvien, Tim Hubert, Jan Stürznickel, Julian Amling, Michael Busse, Björn Beil, Frank Timo Eissele, Julian Bechler, Ulrich Stockhausen, Kilian Elia  | 
    
| Author_xml | – sequence: 1 givenname: Simon orcidid: 0000-0002-2898-5732 surname: von Kroge fullname: von Kroge, Simon organization: Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, Hamburg 22529, Germany – sequence: 2 givenname: Julian orcidid: 0000-0002-5218-8442 surname: Stürznickel fullname: Stürznickel, Julian organization: Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, Hamburg 22529, Germany – sequence: 3 givenname: Ulrich orcidid: 0000-0002-8311-602X surname: Bechler fullname: Bechler, Ulrich organization: Department of Trauma and Orthopaedic Surgery, Division of Orthopaedics, University Medical Center Hamburg-Eppendorf, Germany – sequence: 4 givenname: Kilian Elia orcidid: 0000-0001-8923-8936 surname: Stockhausen fullname: Stockhausen, Kilian Elia organization: Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, Hamburg 22529, Germany – sequence: 5 givenname: Julian surname: Eissele fullname: Eissele, Julian organization: Department of Trauma and Orthopaedic Surgery, Division of Orthopaedics, University Medical Center Hamburg-Eppendorf, Germany – sequence: 6 givenname: Jan orcidid: 0000-0001-6457-9195 surname: Hubert fullname: Hubert, Jan organization: Department of Trauma and Orthopaedic Surgery, Division of Orthopaedics, University Medical Center Hamburg-Eppendorf, Germany – sequence: 7 givenname: Michael surname: Amling fullname: Amling, Michael organization: Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, Hamburg 22529, Germany – sequence: 8 givenname: Frank Timo surname: Beil fullname: Beil, Frank Timo organization: Department of Trauma and Orthopaedic Surgery, Division of Orthopaedics, University Medical Center Hamburg-Eppendorf, Germany – sequence: 9 givenname: Björn surname: Busse fullname: Busse, Björn organization: Department of Osteology and Biomechanics, University Medical Center Hamburg-Eppendorf, Lottestr. 59, Hamburg 22529, Germany – sequence: 10 givenname: Tim orcidid: 0000-0003-1058-1307 surname: Rolvien fullname: Rolvien, Tim email: t.rolvien@uke.de organization: Department of Trauma and Orthopaedic Surgery, Division of Orthopaedics, University Medical Center Hamburg-Eppendorf, Germany  | 
    
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| Keywords | Femoral neck Bone microstructure Electron microscopy Osteocyte High resolution micro-CT  | 
    
| Language | English | 
    
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| SubjectTerms | Backscattering Biomedical materials Bone density Bone Density - physiology Bone microstructure Bone mineral density Compressive properties Computed tomography Coxa Coxa Valga Coxa Vara Dual energy X-ray absorptiometry Electron imaging Electron microscopy Femoral neck Femoral Neck Fractures Femur Femur Neck - diagnostic imaging Fractures High resolution micro-CT Hip Humans Mechanical loading Microstructure Osteoarthritis Osteocyte Osteocytes Qualitative analysis Sensation Total hip arthroplasty X-Ray Microtomography  | 
    
| Title | Impaired bone quality in the superolateral femoral neck occurs independent of hip geometry and bone mineral density | 
    
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