Surgical revascularization in structural orthotopic bone allograft increases bone remodeling

Wouter F. Willems, Thomas Kremer, Patricia Friedrich, Allen Thorp Bishop

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Background: Osseous defects reconstructed with cryopreserved structural allografts are poorly revascularized and therefore are prone to nonunion, infection, deterioration of mechanical properties, and fracture. Whether this can be mitigated by specific interventions such as intramedullary surgical revascularization has been incompletely evaluated. Questions/purposes: We aimed to study surgical revascularization as a means to improve bone remodeling in cryopreserved allograft. Second, we questioned whether spatial histomorphometric differences occur in cortical bone areas after intramedullary surgical revascularization. Third, biomechanical properties of the graft-recipient construct in surgically revascularized allograft were compared with those of conventional allografts. Methods: Allografts were harvested from 10 Brown Norway rats, cryopreserved, and transplanted orthotopically in a 10-mm defect in two groups of 10 Lewis rats each (major histocompatibility mismatch). In the control group, no surgical revascularization was performed, whereas in the experimental group, a saphenous arteriovenous bundle was transposed in the bone marrow cavity. Bone remodeling was measured with histomorphometry, histology, and microcomputed tomography at 16 weeks. Spatial differences were analyzed with histomorphometry. To determine biomechanical properties, load at failure and structural stiffness in bending were evaluated by the three-point bend testing. In both groups, normal values of the contralateral femur also were analyzed. Results: Surgically revascularized allografts had increased bone remodeling (bone formation rate to bone surface ratio: 130 ± 47 μm 3/μm2/year versus 44 ± 43 μm 3/μm2/year, p = 0.006) and higher cortical osteocyte counts (18.6% ± 12.7% versus 3.1% ± 2.8%, p = 0.002) than nonrevascularized grafts. In nonrevascularized grafts, the bone formation rate to bone surface ratio was 35% of the contralateral normal values, whereas in surgically revascularized grafts, the bone formation rate to bone surface ratio in the grafts exceeded the contralateral values (110%). Microcomputed tomography did not show differences in bone volume between groups, however in both groups, bone volume was less in grafts compared with the contralateral femurs. Inner cortical bone formation rate to bone surface ratio was greater in surgically revascularized grafts (65 ± 30 μm3/μm2/year versus 13 ± 16 μm3/μm2/year in the control group, p = 0.012). Outer cortical bone formation rate to bone surface ratio also increased in surgically revascularized grafts (49 ± 31 μm 3/μm2/year versus 19 ± 21 μm 3/μm2/year, p = 0.032). No differences were found in load at failure and structural stiffness between both groups. In the control group, load at failure and structural stiffness were lower in grafts than in the contralateral femurs (p = 0.004 and p = 0.02, respectively). In the experimental group, surgically revascularized grafts also had lower load at failure and structural stiffness than the contralateral femurs (p = 0.008 and p = 0.02, respectively). Conclusions: Surgical revascularization of large segmental allografts improved bone remodeling and viability without an adverse effect on total bone volume or bending strength and stiffness in this short-term analysis. Clinical Relevance: Cryopreserved allografts remain largely necrotic and are associated with a high rate of complications. Surgical revascularization increases graft healing which could contribute to graft survival with time.

Original languageEnglish (US)
Pages (from-to)2870-2877
Number of pages8
JournalClinical Orthopaedics and Related Research
Volume472
Issue number9
DOIs
StatePublished - 2014

Fingerprint

Bone Remodeling
Allografts
Transplants
Bone and Bones
Osteogenesis
Femur
X-Ray Microtomography
Control Groups
Reference Values
Osteocytes
Histocompatibility
Graft Survival
Histology
Bone Marrow

ASJC Scopus subject areas

  • Orthopedics and Sports Medicine

Cite this

Surgical revascularization in structural orthotopic bone allograft increases bone remodeling. / Willems, Wouter F.; Kremer, Thomas; Friedrich, Patricia; Bishop, Allen Thorp.

In: Clinical Orthopaedics and Related Research, Vol. 472, No. 9, 2014, p. 2870-2877.

Research output: Contribution to journalArticle

Willems, Wouter F. ; Kremer, Thomas ; Friedrich, Patricia ; Bishop, Allen Thorp. / Surgical revascularization in structural orthotopic bone allograft increases bone remodeling. In: Clinical Orthopaedics and Related Research. 2014 ; Vol. 472, No. 9. pp. 2870-2877.
@article{39631bf4292f4677aefaf6071317ac68,
title = "Surgical revascularization in structural orthotopic bone allograft increases bone remodeling",
abstract = "Background: Osseous defects reconstructed with cryopreserved structural allografts are poorly revascularized and therefore are prone to nonunion, infection, deterioration of mechanical properties, and fracture. Whether this can be mitigated by specific interventions such as intramedullary surgical revascularization has been incompletely evaluated. Questions/purposes: We aimed to study surgical revascularization as a means to improve bone remodeling in cryopreserved allograft. Second, we questioned whether spatial histomorphometric differences occur in cortical bone areas after intramedullary surgical revascularization. Third, biomechanical properties of the graft-recipient construct in surgically revascularized allograft were compared with those of conventional allografts. Methods: Allografts were harvested from 10 Brown Norway rats, cryopreserved, and transplanted orthotopically in a 10-mm defect in two groups of 10 Lewis rats each (major histocompatibility mismatch). In the control group, no surgical revascularization was performed, whereas in the experimental group, a saphenous arteriovenous bundle was transposed in the bone marrow cavity. Bone remodeling was measured with histomorphometry, histology, and microcomputed tomography at 16 weeks. Spatial differences were analyzed with histomorphometry. To determine biomechanical properties, load at failure and structural stiffness in bending were evaluated by the three-point bend testing. In both groups, normal values of the contralateral femur also were analyzed. Results: Surgically revascularized allografts had increased bone remodeling (bone formation rate to bone surface ratio: 130 ± 47 μm 3/μm2/year versus 44 ± 43 μm 3/μm2/year, p = 0.006) and higher cortical osteocyte counts (18.6{\%} ± 12.7{\%} versus 3.1{\%} ± 2.8{\%}, p = 0.002) than nonrevascularized grafts. In nonrevascularized grafts, the bone formation rate to bone surface ratio was 35{\%} of the contralateral normal values, whereas in surgically revascularized grafts, the bone formation rate to bone surface ratio in the grafts exceeded the contralateral values (110{\%}). Microcomputed tomography did not show differences in bone volume between groups, however in both groups, bone volume was less in grafts compared with the contralateral femurs. Inner cortical bone formation rate to bone surface ratio was greater in surgically revascularized grafts (65 ± 30 μm3/μm2/year versus 13 ± 16 μm3/μm2/year in the control group, p = 0.012). Outer cortical bone formation rate to bone surface ratio also increased in surgically revascularized grafts (49 ± 31 μm 3/μm2/year versus 19 ± 21 μm 3/μm2/year, p = 0.032). No differences were found in load at failure and structural stiffness between both groups. In the control group, load at failure and structural stiffness were lower in grafts than in the contralateral femurs (p = 0.004 and p = 0.02, respectively). In the experimental group, surgically revascularized grafts also had lower load at failure and structural stiffness than the contralateral femurs (p = 0.008 and p = 0.02, respectively). Conclusions: Surgical revascularization of large segmental allografts improved bone remodeling and viability without an adverse effect on total bone volume or bending strength and stiffness in this short-term analysis. Clinical Relevance: Cryopreserved allografts remain largely necrotic and are associated with a high rate of complications. Surgical revascularization increases graft healing which could contribute to graft survival with time.",
author = "Willems, {Wouter F.} and Thomas Kremer and Patricia Friedrich and Bishop, {Allen Thorp}",
year = "2014",
doi = "10.1007/s11999-014-3658-y",
language = "English (US)",
volume = "472",
pages = "2870--2877",
journal = "Clinical Orthopaedics and Related Research",
issn = "0009-921X",
publisher = "Springer New York",
number = "9",

}

TY - JOUR

T1 - Surgical revascularization in structural orthotopic bone allograft increases bone remodeling

AU - Willems, Wouter F.

AU - Kremer, Thomas

AU - Friedrich, Patricia

AU - Bishop, Allen Thorp

PY - 2014

Y1 - 2014

N2 - Background: Osseous defects reconstructed with cryopreserved structural allografts are poorly revascularized and therefore are prone to nonunion, infection, deterioration of mechanical properties, and fracture. Whether this can be mitigated by specific interventions such as intramedullary surgical revascularization has been incompletely evaluated. Questions/purposes: We aimed to study surgical revascularization as a means to improve bone remodeling in cryopreserved allograft. Second, we questioned whether spatial histomorphometric differences occur in cortical bone areas after intramedullary surgical revascularization. Third, biomechanical properties of the graft-recipient construct in surgically revascularized allograft were compared with those of conventional allografts. Methods: Allografts were harvested from 10 Brown Norway rats, cryopreserved, and transplanted orthotopically in a 10-mm defect in two groups of 10 Lewis rats each (major histocompatibility mismatch). In the control group, no surgical revascularization was performed, whereas in the experimental group, a saphenous arteriovenous bundle was transposed in the bone marrow cavity. Bone remodeling was measured with histomorphometry, histology, and microcomputed tomography at 16 weeks. Spatial differences were analyzed with histomorphometry. To determine biomechanical properties, load at failure and structural stiffness in bending were evaluated by the three-point bend testing. In both groups, normal values of the contralateral femur also were analyzed. Results: Surgically revascularized allografts had increased bone remodeling (bone formation rate to bone surface ratio: 130 ± 47 μm 3/μm2/year versus 44 ± 43 μm 3/μm2/year, p = 0.006) and higher cortical osteocyte counts (18.6% ± 12.7% versus 3.1% ± 2.8%, p = 0.002) than nonrevascularized grafts. In nonrevascularized grafts, the bone formation rate to bone surface ratio was 35% of the contralateral normal values, whereas in surgically revascularized grafts, the bone formation rate to bone surface ratio in the grafts exceeded the contralateral values (110%). Microcomputed tomography did not show differences in bone volume between groups, however in both groups, bone volume was less in grafts compared with the contralateral femurs. Inner cortical bone formation rate to bone surface ratio was greater in surgically revascularized grafts (65 ± 30 μm3/μm2/year versus 13 ± 16 μm3/μm2/year in the control group, p = 0.012). Outer cortical bone formation rate to bone surface ratio also increased in surgically revascularized grafts (49 ± 31 μm 3/μm2/year versus 19 ± 21 μm 3/μm2/year, p = 0.032). No differences were found in load at failure and structural stiffness between both groups. In the control group, load at failure and structural stiffness were lower in grafts than in the contralateral femurs (p = 0.004 and p = 0.02, respectively). In the experimental group, surgically revascularized grafts also had lower load at failure and structural stiffness than the contralateral femurs (p = 0.008 and p = 0.02, respectively). Conclusions: Surgical revascularization of large segmental allografts improved bone remodeling and viability without an adverse effect on total bone volume or bending strength and stiffness in this short-term analysis. Clinical Relevance: Cryopreserved allografts remain largely necrotic and are associated with a high rate of complications. Surgical revascularization increases graft healing which could contribute to graft survival with time.

AB - Background: Osseous defects reconstructed with cryopreserved structural allografts are poorly revascularized and therefore are prone to nonunion, infection, deterioration of mechanical properties, and fracture. Whether this can be mitigated by specific interventions such as intramedullary surgical revascularization has been incompletely evaluated. Questions/purposes: We aimed to study surgical revascularization as a means to improve bone remodeling in cryopreserved allograft. Second, we questioned whether spatial histomorphometric differences occur in cortical bone areas after intramedullary surgical revascularization. Third, biomechanical properties of the graft-recipient construct in surgically revascularized allograft were compared with those of conventional allografts. Methods: Allografts were harvested from 10 Brown Norway rats, cryopreserved, and transplanted orthotopically in a 10-mm defect in two groups of 10 Lewis rats each (major histocompatibility mismatch). In the control group, no surgical revascularization was performed, whereas in the experimental group, a saphenous arteriovenous bundle was transposed in the bone marrow cavity. Bone remodeling was measured with histomorphometry, histology, and microcomputed tomography at 16 weeks. Spatial differences were analyzed with histomorphometry. To determine biomechanical properties, load at failure and structural stiffness in bending were evaluated by the three-point bend testing. In both groups, normal values of the contralateral femur also were analyzed. Results: Surgically revascularized allografts had increased bone remodeling (bone formation rate to bone surface ratio: 130 ± 47 μm 3/μm2/year versus 44 ± 43 μm 3/μm2/year, p = 0.006) and higher cortical osteocyte counts (18.6% ± 12.7% versus 3.1% ± 2.8%, p = 0.002) than nonrevascularized grafts. In nonrevascularized grafts, the bone formation rate to bone surface ratio was 35% of the contralateral normal values, whereas in surgically revascularized grafts, the bone formation rate to bone surface ratio in the grafts exceeded the contralateral values (110%). Microcomputed tomography did not show differences in bone volume between groups, however in both groups, bone volume was less in grafts compared with the contralateral femurs. Inner cortical bone formation rate to bone surface ratio was greater in surgically revascularized grafts (65 ± 30 μm3/μm2/year versus 13 ± 16 μm3/μm2/year in the control group, p = 0.012). Outer cortical bone formation rate to bone surface ratio also increased in surgically revascularized grafts (49 ± 31 μm 3/μm2/year versus 19 ± 21 μm 3/μm2/year, p = 0.032). No differences were found in load at failure and structural stiffness between both groups. In the control group, load at failure and structural stiffness were lower in grafts than in the contralateral femurs (p = 0.004 and p = 0.02, respectively). In the experimental group, surgically revascularized grafts also had lower load at failure and structural stiffness than the contralateral femurs (p = 0.008 and p = 0.02, respectively). Conclusions: Surgical revascularization of large segmental allografts improved bone remodeling and viability without an adverse effect on total bone volume or bending strength and stiffness in this short-term analysis. Clinical Relevance: Cryopreserved allografts remain largely necrotic and are associated with a high rate of complications. Surgical revascularization increases graft healing which could contribute to graft survival with time.

UR - http://www.scopus.com/inward/record.url?scp=84905963471&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84905963471&partnerID=8YFLogxK

U2 - 10.1007/s11999-014-3658-y

DO - 10.1007/s11999-014-3658-y

M3 - Article

C2 - 25011908

AN - SCOPUS:84905963471

VL - 472

SP - 2870

EP - 2877

JO - Clinical Orthopaedics and Related Research

JF - Clinical Orthopaedics and Related Research

SN - 0009-921X

IS - 9

ER -