Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model

STEIJVERS, EMMA; Shi, Yunshong; LU, HONG; Zhang, Weixin; ZHANG, YITIAN; Zhao, Feihu; Wang, Baichuan; Hughes, Louise; Barralet, Jake E.; Degli-Alessandrini, Giulia; Kraev, Igor; Johnston, Richard; Shao, Zengwu; Ebetino, Frank H.; Triffitt, James T.; G., R. Graham; Deganello, Davide; Cao, Xu; Xia, Zhidao

doi:10.1016/j.bioactmat.2024.11.025

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Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model

EMMA STEIJVERS, Yunshong Shi, HONG LU, Weixin Zhang, YITIAN ZHANG, Feihu Zhao

, Baichuan Wang, Louise Hughes, Jake E. Barralet

, Giulia Degli-Alessandrini, Igor Kraev

, Richard Johnston

, Zengwu Shao, Frank H. Ebetino, James T. Triffitt, R. Graham G. Russell, Davide Deganello

, Xu Cao, Zhidao Xia

Bioactive Materials, Volume: 45, Pages: 257 - 273

Swansea University Authors: EMMA STEIJVERS, HONG LU, YITIAN ZHANG, Feihu Zhao , Richard Johnston , Davide Deganello , Zhidao Xia

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DOI (Published version): 10.1016/j.bioactmat.2024.11.025

Abstract

Biomaterials are widely used as orthopaedic implants and bone graft substitutes. We aimed to develop a rapid osteogenic assessment method using a murine tibial periosteal ossification model to evaluate the bone formation/remodelling potential of a biomaterial within 2–4 weeks. A novel hydroxyapatite...

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Published in:	Bioactive Materials
ISSN:	2452-199X
Published:	Elsevier BV 2025
Online Access:	Check full text
URI:	https://cronfa.swan.ac.uk/Record/cronfa68385

first_indexed	2024-11-29T13:46:46Z
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We aimed to develop a rapid osteogenic assessment method using a murine tibial periosteal ossification model to evaluate the bone formation/remodelling potential of a biomaterial within 2–4 weeks. A novel hydroxyapatite/aragonite (HAA) biomaterial was implanted into C57BL/6 mice juxtaskeletally between the tibia and tibialis anterior muscle. Rapid intramembranous bone formation was observed at 14 days, with 4- to 8-fold increases in bone thickness and callus volume in comparison with sham-operated animals (p < 0.0001), followed by bone remodelling and a new layer of cortical bone formation by 28 days after implantation. The addition of zoledronate, a clinically-utilised bisphosphonate, to HAA, promoted significantly more new bone formation than HAA alone over 28 days (p < 0.01). The osteogenic potential of HAA was further confirmed by implanting into a 3.5 mm diameter femoral cancellous bone defect in rats and a 5 mm diameter femoral cortical bone defect in minipigs. To understand the biodegradation and the cellular activity at the cell/biomaterial interfaces, non-decalcified specimens were resin embedded and sections subjected to combined scanning electron microscopy (SEM)/electron backscatter diffraction (EBSD)/energy dispersive X-ray spectrometry (EDS) analysis. We conclude that murine tibial periosteal ossification is a novel method for rapid assessment of the interaction of bioactive materials with osteogenic tissues. This study also highlights that combining calcium carbonate with hydroxyapatite enhances biodegradation and osteogenesis.</abstract><type>Journal Article</type><journal>Bioactive Materials</journal><volume>45</volume><journalNumber/><paginationStart>257</paginationStart><paginationEnd>273</paginationEnd><publisher>Elsevier BV</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint/><issnElectronic>2452-199X</issnElectronic><keywords/><publishedDay>1</publishedDay><publishedMonth>3</publishedMonth><publishedYear>2025</publishedYear><publishedDate>2025-03-01</publishedDate><doi>10.1016/j.bioactmat.2024.11.025</doi><url/><notes/><college>COLLEGE NANME</college><CollegeCode>COLLEGE CODE</CollegeCode><institution>Swansea University</institution><apcterm>Another institution paid the OA fee</apcterm><funders>This project was supported by Royal Society International Exchanges Grant 2021 (IES\R1\211128), Québec–Wales Collaboration Grant 2021 and Wales Innovation Network (WIN) Small Grants Fund (SG6-RIR1058-107). We would like to thank Prof. Cathy Thornton and Dr Ruth Jones for providing human umbilical cords, and Dr Christopher Von Ruhland, CBS, Cardiff University for supporting the resin embedding and sampling process.</funders><projectreference/><lastEdited>2024-11-29T11:40:00.2063490</lastEdited><Created>2024-11-29T11:17:10.1845807</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Biomedical Science</level></path><authors><author><firstname>EMMA</firstname><surname>STEIJVERS</surname><order>1</order></author><author><firstname>Yunshong</firstname><surname>Shi</surname><order>2</order></author><author><firstname>HONG</firstname><surname>LU</surname><order>3</order></author><author><firstname>Weixin</firstname><surname>Zhang</surname><order>4</order></author><author><firstname>YITIAN</firstname><surname>ZHANG</surname><order>5</order></author><author><firstname>Feihu</firstname><surname>Zhao</surname><orcid>0000-0003-0515-6808</orcid><order>6</order></author><author><firstname>Baichuan</firstname><surname>Wang</surname><order>7</order></author><author><firstname>Louise</firstname><surname>Hughes</surname><order>8</order></author><author><firstname>Jake E.</firstname><surname>Barralet</surname><orcid>0000-0003-3543-6042</orcid><order>9</order></author><author><firstname>Giulia</firstname><surname>Degli-Alessandrini</surname><order>10</order></author><author><firstname>Igor</firstname><surname>Kraev</surname><orcid>0000-0003-1822-278X</orcid><order>11</order></author><author><firstname>Richard</firstname><surname>Johnston</surname><orcid>0000-0003-1977-6418</orcid><order>12</order></author><author><firstname>Zengwu</firstname><surname>Shao</surname><order>13</order></author><author><firstname>Frank H.</firstname><surname>Ebetino</surname><order>14</order></author><author><firstname>James T.</firstname><surname>Triffitt</surname><order>15</order></author><author><firstname>R. 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spelling	2024-11-29T11:40:00.2063490 v2 68385 2024-11-29 Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model 0b8e2c94c5ea2b8bc99f5cdaea16883f EMMA STEIJVERS EMMA STEIJVERS true false faa87317ec00ad6c80972a7dcceefdd6 HONG LU HONG LU true true 854822570ef4cf2c85fcd497cf8d7a50 YITIAN ZHANG YITIAN ZHANG true true 1c6e79b6edd08c88a8d17a241cd78630 0000-0003-0515-6808 Feihu Zhao Feihu Zhao true false 23282e7acce87dd926b8a62ae410a393 0000-0003-1977-6418 Richard Johnston Richard Johnston true false ea38a0040bdfd3875506189e3629b32a 0000-0001-8341-4177 Davide Deganello Davide Deganello true false c9307abfed1b43987a19da0c0e30d7a4 0000-0002-2047-7282 Zhidao Xia Zhidao Xia true false 2024-11-29 Biomaterials are widely used as orthopaedic implants and bone graft substitutes. We aimed to develop a rapid osteogenic assessment method using a murine tibial periosteal ossification model to evaluate the bone formation/remodelling potential of a biomaterial within 2–4 weeks. A novel hydroxyapatite/aragonite (HAA) biomaterial was implanted into C57BL/6 mice juxtaskeletally between the tibia and tibialis anterior muscle. Rapid intramembranous bone formation was observed at 14 days, with 4- to 8-fold increases in bone thickness and callus volume in comparison with sham-operated animals (p < 0.0001), followed by bone remodelling and a new layer of cortical bone formation by 28 days after implantation. The addition of zoledronate, a clinically-utilised bisphosphonate, to HAA, promoted significantly more new bone formation than HAA alone over 28 days (p < 0.01). The osteogenic potential of HAA was further confirmed by implanting into a 3.5 mm diameter femoral cancellous bone defect in rats and a 5 mm diameter femoral cortical bone defect in minipigs. To understand the biodegradation and the cellular activity at the cell/biomaterial interfaces, non-decalcified specimens were resin embedded and sections subjected to combined scanning electron microscopy (SEM)/electron backscatter diffraction (EBSD)/energy dispersive X-ray spectrometry (EDS) analysis. We conclude that murine tibial periosteal ossification is a novel method for rapid assessment of the interaction of bioactive materials with osteogenic tissues. This study also highlights that combining calcium carbonate with hydroxyapatite enhances biodegradation and osteogenesis. Journal Article Bioactive Materials 45 257 273 Elsevier BV 2452-199X 1 3 2025 2025-03-01 10.1016/j.bioactmat.2024.11.025 COLLEGE NANME COLLEGE CODE Swansea University Another institution paid the OA fee This project was supported by Royal Society International Exchanges Grant 2021 (IES\R1\211128), Québec–Wales Collaboration Grant 2021 and Wales Innovation Network (WIN) Small Grants Fund (SG6-RIR1058-107). We would like to thank Prof. Cathy Thornton and Dr Ruth Jones for providing human umbilical cords, and Dr Christopher Von Ruhland, CBS, Cardiff University for supporting the resin embedding and sampling process. 2024-11-29T11:40:00.2063490 2024-11-29T11:17:10.1845807 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science EMMA STEIJVERS 1 Yunshong Shi 2 HONG LU 3 Weixin Zhang 4 YITIAN ZHANG 5 Feihu Zhao 0000-0003-0515-6808 6 Baichuan Wang 7 Louise Hughes 8 Jake E. Barralet 0000-0003-3543-6042 9 Giulia Degli-Alessandrini 10 Igor Kraev 0000-0003-1822-278X 11 Richard Johnston 0000-0003-1977-6418 12 Zengwu Shao 13 Frank H. Ebetino 14 James T. Triffitt 15 R. Graham G. Russell 16 Davide Deganello 0000-0001-8341-4177 17 Xu Cao 18 Zhidao Xia 0000-0002-2047-7282 19
title	Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model
spellingShingle	Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model EMMA STEIJVERS HONG LU YITIAN ZHANG Feihu Zhao Richard Johnston Davide Deganello Zhidao Xia
title_short	Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model
title_full	Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model
title_fullStr	Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model
title_full_unstemmed	Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model
title_sort	Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model
author_id_str_mv	0b8e2c94c5ea2b8bc99f5cdaea16883f faa87317ec00ad6c80972a7dcceefdd6 854822570ef4cf2c85fcd497cf8d7a50 1c6e79b6edd08c88a8d17a241cd78630 23282e7acce87dd926b8a62ae410a393 ea38a0040bdfd3875506189e3629b32a c9307abfed1b43987a19da0c0e30d7a4
author_id_fullname_str_mv	0b8e2c94c5ea2b8bc99f5cdaea16883f_*_EMMA STEIJVERS faa87317ec00ad6c80972a7dcceefdd6__HONG LU 854822570ef4cf2c85fcd497cf8d7a50__YITIAN ZHANG 1c6e79b6edd08c88a8d17a241cd78630__Feihu Zhao 23282e7acce87dd926b8a62ae410a393__Richard Johnston ea38a0040bdfd3875506189e3629b32a__Davide Deganello c9307abfed1b43987a19da0c0e30d7a4_**_Zhidao Xia
author	EMMA STEIJVERS HONG LU YITIAN ZHANG Feihu Zhao Richard Johnston Davide Deganello Zhidao Xia
author2	EMMA STEIJVERS Yunshong Shi HONG LU Weixin Zhang YITIAN ZHANG Feihu Zhao Baichuan Wang Louise Hughes Jake E. Barralet Giulia Degli-Alessandrini Igor Kraev Richard Johnston Zengwu Shao Frank H. Ebetino James T. Triffitt R. Graham G. Russell Davide Deganello Xu Cao Zhidao Xia
format	Journal article
container_title	Bioactive Materials
container_volume	45
container_start_page	257
publishDate	2025
institution	Swansea University
issn	2452-199X
doi_str_mv	10.1016/j.bioactmat.2024.11.025
publisher	Elsevier BV
college_str	Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id	facultyofmedicinehealthandlifesciences
hierarchy_top_title	Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id	facultyofmedicinehealthandlifesciences
hierarchy_parent_title	Faculty of Medicine, Health and Life Sciences
department_str	Swansea University Medical School - Biomedical Science{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Biomedical Science
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description	Biomaterials are widely used as orthopaedic implants and bone graft substitutes. We aimed to develop a rapid osteogenic assessment method using a murine tibial periosteal ossification model to evaluate the bone formation/remodelling potential of a biomaterial within 2–4 weeks. A novel hydroxyapatite/aragonite (HAA) biomaterial was implanted into C57BL/6 mice juxtaskeletally between the tibia and tibialis anterior muscle. Rapid intramembranous bone formation was observed at 14 days, with 4- to 8-fold increases in bone thickness and callus volume in comparison with sham-operated animals (p < 0.0001), followed by bone remodelling and a new layer of cortical bone formation by 28 days after implantation. The addition of zoledronate, a clinically-utilised bisphosphonate, to HAA, promoted significantly more new bone formation than HAA alone over 28 days (p < 0.01). The osteogenic potential of HAA was further confirmed by implanting into a 3.5 mm diameter femoral cancellous bone defect in rats and a 5 mm diameter femoral cortical bone defect in minipigs. To understand the biodegradation and the cellular activity at the cell/biomaterial interfaces, non-decalcified specimens were resin embedded and sections subjected to combined scanning electron microscopy (SEM)/electron backscatter diffraction (EBSD)/energy dispersive X-ray spectrometry (EDS) analysis. We conclude that murine tibial periosteal ossification is a novel method for rapid assessment of the interaction of bioactive materials with osteogenic tissues. This study also highlights that combining calcium carbonate with hydroxyapatite enhances biodegradation and osteogenesis.
published_date	2025-03-01T08:36:44Z
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score	11.047739

Rapid assessment of the osteogenic capacity of hydroxyapatite/aragonite using a murine tibial periosteal ossification model

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