Bone microarchitecture and turnover in the irradiated human mandible

H Dekker; E A J M Schulten; L van Ruijven; H W van Essen; G J Blom; E Bloemena; Chr M Ten Bruggenkate; A M Kullaa; N Bravenboer

doi:10.1016/j.jcms.2020.05.015

Bone microarchitecture and turnover in the irradiated human mandible

J Craniomaxillofac Surg. 2020 Aug;48(8):733-740. doi: 10.1016/j.jcms.2020.05.015. Epub 2020 Jun 9.

Authors

H Dekker¹, E A J M Schulten², L van Ruijven³, H W van Essen⁴, G J Blom⁵, E Bloemena⁶, Chr M Ten Bruggenkate⁷, A M Kullaa⁸, N Bravenboer⁹

Affiliations

¹ Amsterdam UMC, Academic Centre for Dentistry Amsterdam (ACTA), Vrije Universiteit Amsterdam, Department of Oral and Maxillofacial Surgery/Oral Pathology, Amsterdam, the Netherlands. Electronic address: ha.dekker@amsterdamumc.nl.
² Amsterdam UMC, Academic Centre for Dentistry Amsterdam (ACTA), Vrije Universiteit Amsterdam, Department of Oral and Maxillofacial Surgery/Oral Pathology, Amsterdam, the Netherlands. Electronic address: eajm.schulten@amsterdamumc.nl.
³ Department of Functional Anatomy, Academic Centre for Dentistry Amsterdam (ACTA), Amsterdam, the Netherlands. Electronic address: lvruijven@gmx.com.
⁴ Amsterdam UMC, Vrije Universiteit Amsterdam, Department of Clinical Chemistry, the Netherlands. Electronic address: hw.vanessen@amsterdamumc.nl.
⁵ Amsterdam UMC, Vrije Universiteit Amsterdam, Department of Radiotherapy, Amsterdam, the Netherlands. Electronic address: gj.blom@amsterdamumc.nl.
⁶ Amsterdam UMC, Academic Centre for Dentistry Amsterdam (ACTA), Vrije Universiteit Amsterdam, Department of Oral and Maxillofacial Surgery/Oral Pathology, Amsterdam, the Netherlands. Electronic address: e.bloemena@amsterdamumc.nl.
⁷ Amsterdam UMC, Academic Centre for Dentistry Amsterdam (ACTA), Vrije Universiteit Amsterdam, Department of Oral and Maxillofacial Surgery/Oral Pathology, Amsterdam, the Netherlands; Alrijne Hospital, Department of Oral and Maxillofacial Surgery, Leiderdorp, the Netherlands. Electronic address: cmtenbruggenkate@alrijne.nl.
⁸ Institute of Dentistry, University of Eastern Finland, Kuopio Campus, and Educational Dental Clinic, Kuopio University Hospital, Kuopio, Finland. Electronic address: arja.kullaa@uef.fi.
⁹ Amsterdam UMC, Vrije Universiteit Amsterdam, Department of Clinical Chemistry, the Netherlands; Leiden University Medical Center, Department of Internal Medicine, Division of Endocrinology and Center for Bone Quality, Leiden, the Netherlands. Electronic address: n.bravenboer@amsterdamumc.nl.

PMID: 32591131
DOI: 10.1016/j.jcms.2020.05.015

Abstract

Objectives: The aim of this study was to assess the microarchitecture and turnover in irradiated cancellous mandibular bone and the relation with radiation dose, to elucidate the effects of radiotherapy on the mandible.

Patients and methods: Mandibular cancellous bone biopsies were taken from irradiated patients and controls. Micro-CT scanning was performed to analyze microstructural bone parameters. Bone turnover was assessed by histomorphometry. Local radiation dose at the biopsy site (Dmax) was estimated from radiotherapy plans.

Results: Twenty-seven irradiated patients and 35 controls were included. Osteoid volume (Osteoid Volume/Bone Volume, OV/BV) [0.066/0.168 (median/interquartile range (IQR), OV/BV; %), P < 0.001], osteoid surface (Osteoid Surface/Bone Surface, OS/BS) [0.772/2.17 (median/IQR, OS/BS; %), P < 0.001] and osteoclasts number (Osteoclasts per millimetre bone surface, Ocl/mmBS; mm²) [0.026/0.123 (median/IQR, Ocl/mmBS; mm²), P < 0.001] were decreased; trabecular number (Tb.N) was lower [1.63/0.63 (median/IQR, Tb.N; 1/mm^-1), P = 0.012] and trabecular separation (Tb.Sp) [0.626/0.24 (median/IQR, Tb.Sp; μm), P = 0.038] was higher in irradiated mandibular bone. With higher Dmax, trabecular number increases (Spearman's correlation R = 0.470, P = 0.018) and trabecular separation decreases (Spearman's correlation R = -0.526, P = 0.007). Bone mineral density (BMD, milligrams hydroxyappetite per cubic centimetre, mgHA/cm³) [1016/99 (median/IQR, BMD; mgHA/cm³), P = 0.03] and trabecular separation [0.739/0.21 (median/IQR, Tb.Sp; μm), P = 0.005] are higher whereas connectivity density (Conn Dens) [3.94/6.71 (median/IQR, Conn Dens), P = 0.047] and trabecular number [1.48/0.44 (median/IQR, Tb.N; 1/mm^-1), P = 0.002] are lower in Dmax ≤50 Gy compared to controls.

Conclusions: Radiotherapy dramatically impairs bone turnover in the mandible. Deterioration in microarchitecture only affects bone irradiated with a Dmax of <50 Gy. The 50 Gy value seems to be a critical threshold to where the effects of the radiation is more detrimental.

Keywords: Bone turnover; Mandible; Oral cancer; Osteoradionecrosis; Radiotherapy.

MeSH terms

Biopsy
Bone Density*
Humans
Mandible*
X-Ray Microtomography