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A robust, semi-automated approach for counting cementum increments imaged with synchrotron X-ray computed tomography

A robust, semi-automated approach for counting cementum increments imaged with synchrotron X-ray computed tomography
A robust, semi-automated approach for counting cementum increments imaged with synchrotron X-ray computed tomography
Cementum, the tissue attaching mammal tooth roots to the periodontal ligament, grows appositionally throughout life, displaying a series of circum-annual incremental features. These have been studied for decades as a direct record of chronological lifespan. The majority of previous studies on cementum have used traditional thin-section histological methods to image and analyse increments. However, several caveats have been raised in terms of studying cementum increments in thin-sections. Firstly, the limited number of thin-sections and the two-dimensional perspective they impart provide an incomplete interpretation of cementum structure, and studies often struggle or fail to overcome complications in increment patterns that complicate or inhibit increment counting. Increments have been repeatedly shown to both split and coalesce, creating accessory increments that can bias increment counts. Secondly, identification and counting of cementum increments using human vision is subjective, and it has led to inaccurate readings in several experiments studying individuals of known age. Here, we have attempted to optimise a recently introduced imaging modality for cementum imaging; X-ray propagation-based phase-contrast imaging (PPCI). X-ray PPCI was performed for a sample of rhesus macaque (Macaca mulatta) lower first molars (n = 10) from a laboratory population of known age. PPCI allowed the qualitative identification of primary/annual versus intermittent secondary increments formed by splitting/coalescence. A new method for semi-automatic increment counting was then integrated into a purpose-built software package for studying cementum increments, to count increments in regions with minimal complications. Qualitative comparison with data from conventional cementochronology, based on histological examination of tissue thin-sections, confirmed that X-ray PPCI reliably and non-destructively records cementum increments (given the appropriate preparation of specimens prior to X-ray imaging). Validation of the increment counting algorithm suggests that it is robust and provides accurate estimates of increment counts. In summary, we show that our new increment counting method has the potential to overcome caveats of conventional cementochronology approaches, when used to analyse three-dimensional images provided by X-ray PPCI.
1932-6203
Newham, Elis
30b25d76-7f4e-47e8-9547-7a0d13619c08
Gill, Pamela G.
a68e7f37-5076-4f86-9193-88ad79c57cd0
Robson Brown, Kate
595850c3-7396-4ae1-b970-24a7b2876b66
Gostling, Neil J.
4840aa40-cb6c-4112-a0b9-694a869523fc
Corfe, Ian J.
5fa0fcee-7d67-4c22-a4d3-532307b072fa
Schneider, Philipp
a810f925-4808-44e4-8a4a-a51586f9d7ad
Newham, Elis
30b25d76-7f4e-47e8-9547-7a0d13619c08
Gill, Pamela G.
a68e7f37-5076-4f86-9193-88ad79c57cd0
Robson Brown, Kate
595850c3-7396-4ae1-b970-24a7b2876b66
Gostling, Neil J.
4840aa40-cb6c-4112-a0b9-694a869523fc
Corfe, Ian J.
5fa0fcee-7d67-4c22-a4d3-532307b072fa
Schneider, Philipp
a810f925-4808-44e4-8a4a-a51586f9d7ad

Newham, Elis, Gill, Pamela G., Robson Brown, Kate, Gostling, Neil J., Corfe, Ian J. and Schneider, Philipp (2021) A robust, semi-automated approach for counting cementum increments imaged with synchrotron X-ray computed tomography. PLoS ONE, 16 (11 November 202), [e0249743]. (doi:10.1371/journal.pone.0249743).

Record type: Article

Abstract

Cementum, the tissue attaching mammal tooth roots to the periodontal ligament, grows appositionally throughout life, displaying a series of circum-annual incremental features. These have been studied for decades as a direct record of chronological lifespan. The majority of previous studies on cementum have used traditional thin-section histological methods to image and analyse increments. However, several caveats have been raised in terms of studying cementum increments in thin-sections. Firstly, the limited number of thin-sections and the two-dimensional perspective they impart provide an incomplete interpretation of cementum structure, and studies often struggle or fail to overcome complications in increment patterns that complicate or inhibit increment counting. Increments have been repeatedly shown to both split and coalesce, creating accessory increments that can bias increment counts. Secondly, identification and counting of cementum increments using human vision is subjective, and it has led to inaccurate readings in several experiments studying individuals of known age. Here, we have attempted to optimise a recently introduced imaging modality for cementum imaging; X-ray propagation-based phase-contrast imaging (PPCI). X-ray PPCI was performed for a sample of rhesus macaque (Macaca mulatta) lower first molars (n = 10) from a laboratory population of known age. PPCI allowed the qualitative identification of primary/annual versus intermittent secondary increments formed by splitting/coalescence. A new method for semi-automatic increment counting was then integrated into a purpose-built software package for studying cementum increments, to count increments in regions with minimal complications. Qualitative comparison with data from conventional cementochronology, based on histological examination of tissue thin-sections, confirmed that X-ray PPCI reliably and non-destructively records cementum increments (given the appropriate preparation of specimens prior to X-ray imaging). Validation of the increment counting algorithm suggests that it is robust and provides accurate estimates of increment counts. In summary, we show that our new increment counting method has the potential to overcome caveats of conventional cementochronology approaches, when used to analyse three-dimensional images provided by X-ray PPCI.

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Accepted/In Press date: 22 October 2021
Published date: 4 November 2021

Identifiers

Local EPrints ID: 452467
URI: http://eprints.soton.ac.uk/id/eprint/452467
ISSN: 1932-6203
PURE UUID: cf4832ef-dcd7-41b8-8d30-270837f75c98
ORCID for Neil J. Gostling: ORCID iD orcid.org/0000-0002-5960-7769
ORCID for Philipp Schneider: ORCID iD orcid.org/0000-0001-7499-3576

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Date deposited: 11 Dec 2021 11:05
Last modified: 28 Apr 2022 02:10

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Contributors

Author: Elis Newham
Author: Pamela G. Gill
Author: Kate Robson Brown
Author: Ian J. Corfe

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