{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,27]],"date-time":"2026-05-27T20:28:36Z","timestamp":1779913716482,"version":"3.53.1"},"reference-count":28,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,4,7]],"date-time":"2020-04-07T00:00:00Z","timestamp":1586217600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2020,4,7]],"date-time":"2020-04-07T00:00:00Z","timestamp":1586217600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100008459","name":"University of Calgary","doi-asserted-by":"crossref","award":["McCaig Institute Encore Catalyst Grant, University of Calgary"],"award-info":[{"award-number":["McCaig Institute Encore Catalyst Grant, University of Calgary"]}],"id":[{"id":"10.13039\/100008459","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["unknown"],"award-info":[{"award-number":["unknown"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Med Imaging"],"published-print":{"date-parts":[[2020,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>Medical imaging plays an important role in determining the progression of joint damage in rheumatoid arthritis (RA). High resolution peripheral quantitative computed tomography (HR-pQCT) is a sensitive tool capable of evaluating bone microarchitecture and erosions, and 3D rigid image registration can be used to visualize and quantify bone remodeling over time. However, patient motion during image acquisition can cause a \u201cstack shift\u201d artifact resulting in loss of information and reducing the number of erosions that can be analyzed using HR-pQCT. The purpose of this study was to use image registration to improve the number of useable HR-pQCT scans and to apply image-based bone remodeling assessment to the metacarpophalangeal (MCP) joints of RA patients.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>Ten participants with RA completed HR-pQCT scans of the 2nd and 3rd MCP joints at enrolment to the study and at a 6-month follow-up interval. At 6-months, an additional repeat scan was acquired to evaluate reliability. HR-pQCT images were acquired in three individual 1\u2009cm acquisitions (stacks) with a 25% overlap. We completed analysis first using standard evaluation methods, and second with multi-stack registration. We assessed whether additional erosions could be evaluated after multi-stack registration. Bone remodeling analysis was completed using registration and transformation of baseline and follow-up images. We calculated the bone formation and resorption volume fractions with 6-month follow-up, and same-day repositioning as a negative control.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>13\/57 (23%) of erosions could not be analyzed from raw images due to a stack shift artifact. All erosions could be volumetrically assessed after multi-stack registration. We observed that there was a median bone formation fraction of 2.1% and resorption fraction of 3.8% in RA patients over the course of 6\u2009months. In contrast to the same-day rescan negative control, we observed median bone formation and resorption fractions of 0%.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Multi-stack image registration is a useful tool to improve the number of useable scans when analyzing erosions using HR-pQCT. Further, image registration can be used to longitudinally assess bone remodeling. These methods could be implemented in future studies to provide important pathophysiological information on the progression of bone damage.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12880-020-00437-8","type":"journal-article","created":{"date-parts":[[2020,4,7]],"date-time":"2020-04-07T10:03:04Z","timestamp":1586253784000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":31,"title":["The utility of multi-stack alignment and 3D longitudinal image registration to assess bone remodeling in rheumatoid arthritis patients from second generation HR-pQCT scans"],"prefix":"10.1186","volume":"20","author":[{"given":"Scott C.","family":"Brunet","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael T.","family":"Kuczynski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer L.","family":"Bhatla","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sophie","family":"Lemay","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yves","family":"Pauchard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Salat","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheryl","family":"Barnabe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah L.","family":"Manske","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,4,7]]},"reference":[{"issue":"11","key":"437_CR1","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1038\/nrrheum.2012.153","volume":"8","author":"G Schett","year":"2012","unstructured":"Schett G, Gravallese E. Bone erosion in rheumatoid arthritis: mechanisms, diagnosis and treatment. Nat Rev Rheumatol. 2012;8(11):656\u201364. Available from:. https:\/\/doi.org\/10.1038\/nrrheum.2012.153.","journal-title":"Nat Rev Rheumatol"},{"issue":"1","key":"437_CR2","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1093\/rheumatology\/ket358","volume":"53","author":"P Geusens","year":"2014","unstructured":"Geusens P, van den Bergh J. Bone erosions in rheumatoid arthritis. Rheumatology. 2014;53(1):4\u20135.","journal-title":"Rheumatology."},{"key":"437_CR3","doi-asserted-by":"publisher","first-page":"1671","DOI":"10.1136\/ard.2009.114512","volume":"69","author":"A Fouque-Aubert","year":"2010","unstructured":"Fouque-Aubert A, Boutroy S, Marotte H, Vilayphiou N, Bacchetta J, Miossec P, Pierre Dominique Delmas RDC. Assessment of hand bone loss in rheumatoid arthritis by high-resolution peripheral quantitative CT. Ann Rheum Dis. 2010;69:1671\u20136.","journal-title":"Ann Rheum Dis"},{"key":"437_CR4","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1038\/nrrheum.2011.202","volume":"8","author":"S Lillegraven","year":"2012","unstructured":"Lillegraven S, van der Heijde D, Uhlig T, Kvien TKHE. What is the clinical relevance of erosions and joint space narrowing in RA? Nat Rev Rheumatol. 2012;8:117\u201320.","journal-title":"Nat Rev Rheumatol"},{"issue":"10","key":"437_CR5","doi-asserted-by":"publisher","first-page":"1540","DOI":"10.1016\/j.medengphy.2013.04.003","volume":"35","author":"C Barnabe","year":"2013","unstructured":"Barnabe C, Buie H, Kan M, Szabo E, Barr SG, Martin L, et al. Reproducible metacarpal joint space width measurements using 3D analysis of images acquired with high-resolution peripheral quantitative computed tomography. Med Eng Phys. 2013;35(10):1540\u20134. Available from. https:\/\/doi.org\/10.1016\/j.medengphy.2013.04.003.","journal-title":"Med Eng Phys"},{"issue":"12","key":"437_CR6","first-page":"2171","volume":"54","author":"D T\u00f6pfer","year":"2015","unstructured":"T\u00f6pfer D, Gerner B, Finzel S, Kraus S, Museyko O, Schett G, et al. Automated three-dimensional registration of high-resolution peripheral quantitative computed tomography data to quantify size and shape changes of arthritic bone erosions. Rheumatol (United Kingdom). 2015;54(12):2171\u201380.","journal-title":"Rheumatol (United Kingdom)."},{"issue":"12","key":"437_CR7","doi-asserted-by":"publisher","first-page":"2553","DOI":"10.1007\/s10439-013-0871-x","volume":"41","author":"AJ Burghardt","year":"2013","unstructured":"Burghardt AJ, Lee CH, Kuo D, Majumdar S, Imboden JB, Link TM, et al. Quantitative in vivo HR-pQCT imaging of 3D wrist and metacarpophalangeal joint space width in rheumatoid arthritis. Ann Biomed Eng. 2013;41(12):2553\u201364.","journal-title":"Ann Biomed Eng"},{"issue":"8","key":"437_CR8","doi-asserted-by":"publisher","first-page":"1580","DOI":"10.1002\/art.40148","volume":"69","author":"D Werner","year":"2017","unstructured":"Werner D, Simon D, Englbrecht M, Stemmler F, Simon C, Berlin A, et al. Early changes of the cortical Micro-Channel system in the bare area of the joints of patients with Rheumatoid Arthritis. Arthritis Rheumatol. 2017;69(8):1580\u20137.","journal-title":"Arthritis Rheumatol"},{"issue":"2","key":"437_CR9","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1093\/rheumatology\/39.2.122","volume":"39","author":"DL Scott","year":"2000","unstructured":"Scott DL, Pugner K, Kaarela K, Doyle DV, Woolf A, Holmes J, et al. The links between joint damage and disability in rheumatoid arthritis. Rheumatology. 2000;39(2):122\u201332.","journal-title":"Rheumatology."},{"issue":"10","key":"437_CR10","doi-asserted-by":"publisher","first-page":"1935","DOI":"10.3899\/jrheum.160648","volume":"43","author":"C Barnabe","year":"2016","unstructured":"Barnabe C, Toepfer D, Marotte H, Hauge E-M, Scharmga A, Kocijan R, et al. Definition for Rheumatoid Arthritis Erosions Imaged with High Resolution Peripheral Quantitative Computed Tomography and Interreader Reliability for Detection and Measurement. J Rheumatol. 2016;43(10):1935\u201340 Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/27698108.","journal-title":"J Rheumatol"},{"issue":"1","key":"437_CR11","first-page":"65","volume":"53","author":"D T\u00f6pfer","year":"2014","unstructured":"T\u00f6pfer D, Finzel S, Museyko O, Schett G, Engelke K. Segmentation and quantification of bone erosions in high-resolution peripheral quantitative computed tomography datasets of the metacarpophalangeal joints of patients with rheumatoid arthritis. Rheumatol (United Kingdom). 2014;53(1):65\u201371.","journal-title":"Rheumatol (United Kingdom)"},{"issue":"1","key":"437_CR12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12880-018-0255-7","volume":"18","author":"M Peters","year":"2018","unstructured":"Peters M, de Jong J, Scharmga A, van Tubergen A, Geusens P, Loeffen D, et al. An automated algorithm for the detection of cortical interruptions and its underlying loss of trabecular bone; a reproducibility study. BMC Med Imaging. 2018;18(1):1\u201310.","journal-title":"BMC Med Imaging"},{"issue":"7","key":"437_CR13","doi-asserted-by":"publisher","first-page":"1494","DOI":"10.3899\/jrheum.120218","volume":"39","author":"C Barnabe","year":"2012","unstructured":"Barnabe C, Feehan L. SPECTRA (study GrouP for XTrEme-CT in RA). High-resolution peripheral quantitative computed tomography imaging protocol for metacarpophalangeal joints in inflammatory arthritis: the SPECTRA collaboration. J Rheumatol. 2012;39(7):1494\u20135.","journal-title":"J Rheumatol"},{"issue":"9","key":"437_CR14","doi-asserted-by":"publisher","first-page":"1676","DOI":"10.1002\/jbmr.3466","volume":"33","author":"M Peters","year":"2018","unstructured":"Peters M, van Tubergen A, Scharmga A, Driessen A, van Rietbergen B, Loeffen D, et al. Assessment of cortical interruptions in the finger joints of patients with Rheumatoid Arthritis using HR-pQCT, radiography, and MRI. J Bone Miner Res. 2018;33(9):1676\u201385. Available from. https:\/\/doi.org\/10.1002\/jbmr.3466.","journal-title":"J Bone Miner Res"},{"issue":"4","key":"437_CR15","first-page":"1","volume":"12","author":"M Peters","year":"2017","unstructured":"Peters M, Scharmga A, De Jong J, Van Tubergen A, Geusens P, Arts JJ, et al. An automated algorithm for the detection of cortical interruptions on high resolution peripheral quantitative computed tomography images of finger joints. PLoS One. 2017;12(4):1\u201315.","journal-title":"PLoS One"},{"issue":"6","key":"437_CR16","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1007\/s00223-019-00523-2","volume":"104","author":"M Peters","year":"2019","unstructured":"Peters M, van den Bergh JP, Geusens P, Scharmga A, Loeffen D, Weijers R, et al. Prospective follow-up of cortical interruptions, bone density, and micro-structure detected on HR-pQCT: a study in patients with Rheumatoid Arthritis and healthy subjects. Calcif Tissue Int. 2019;104(6):571\u201381. Available from:. https:\/\/doi.org\/10.1007\/s00223-019-00523-2.","journal-title":"Calcif Tissue Int"},{"key":"437_CR17","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/ncomms5855","volume":"5","author":"P Christen","year":"2014","unstructured":"Christen P, Ito K, Ellouz R, Boutroy S, Sornay-Rendu E, Chapurlat RD, et al. Bone remodelling in humans is load-driven but not lazy. Nat Commun. 2014;5:1\u20135. Available from. https:\/\/doi.org\/10.1038\/ncomms5855.","journal-title":"Nat Commun"},{"issue":"1","key":"437_CR18","doi-asserted-by":"publisher","first-page":"e0191369","DOI":"10.1371\/journal.pone.0191369","volume":"13","author":"P Christen","year":"2018","unstructured":"Christen P, Boutroy S, Ellouz R, Chapurlat R, van Rietbergen B. Least-detectable and age-related local in vivo bone remodelling assessed by time-lapse HR-pQCT. PLoS One. 2018;13(1):e0191369. Roeder RK, editor. Available from. https:\/\/doi.org\/10.1371\/journal.pone.0191369.","journal-title":"PLoS One"},{"key":"437_CR19","unstructured":"Barber CEH, Sandhu N, Rankin JA, MacMullan P, Marshall DA, Barnabe C, et al. Rheum4U: Development and testing of a web-based tool for improving the quality of care for patients with rheumatoid arthritis. Clin Exp Rheumatol. 2018; Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/30183602."},{"issue":"9","key":"437_CR20","doi-asserted-by":"publisher","first-page":"2569","DOI":"10.1002\/art.27584","volume":"62","author":"D Aletaha","year":"2010","unstructured":"Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology\/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 2010;62(9):2569\u201381 Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/20872595.","journal-title":"Arthritis Rheum"},{"issue":"2","key":"437_CR21","first-page":"243","volume":"31","author":"C Barnabe","year":"2012","unstructured":"Barnabe C, Szabo E, Martin L, Boyd SK, Barr SG. Quantification of small joint space width, periarticular bone microstructure and erosions using high-resolution peripheral quantitative computed tomography in rheumatoid arthritis. Clin Exp Rheumatol. 2012;31(2):243\u201350 Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/23331665.","journal-title":"Clin Exp Rheumatol"},{"issue":"6","key":"437_CR22","doi-asserted-by":"publisher","first-page":"1304","DOI":"10.1016\/j.bone.2012.03.003","volume":"50","author":"Y Pauchard","year":"2012","unstructured":"Pauchard Y, Liphardt AM, Macdonald HM, Hanley DA, Boyd SK. Quality control for bone quality parameters affected by subject motion in high-resolution peripheral quantitative computed tomography. Bone. 2012;50(6):1304\u201310. Available from:. https:\/\/doi.org\/10.1016\/j.bone.2012.03.003.","journal-title":"Bone"},{"key":"437_CR23","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-84628-968-2","volume-title":"Digital image processing","author":"W Burger","year":"2008","unstructured":"Burger W, Burge MJ. Digital image processing. London: Springer London; 2008. Available from: www.imagingbook.com. Cited 2019 Sep 5."},{"issue":"5","key":"437_CR24","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1080\/10255842.2012.699526","volume":"17","author":"FA Schulte","year":"2014","unstructured":"Schulte FA, Lambers FM, Mueller TL, Stauber M, M\u00fcller R. Image interpolation allows accurate quantitative bone morphometry in registered micro-computed tomography scans. Comput Methods Biomech Biomed Engin. 2014;17(5):539\u201348.","journal-title":"Comput Methods Biomech Biomed Engin"},{"issue":"suppl10","key":"437_CR25","first-page":"9","volume":"70","author":"S Brunet","year":"2018","unstructured":"Brunet S, Manske S, Engelke K, Boyd SK, Barnabe C. Joint repair while initiating biologic therapy in Rheumatoid Arthritis. Arthritis Rheumatol. 2018;70(suppl10):9\u201311 Available from: https:\/\/acrabstracts.org\/abstract\/joint-repair-while-initiating-biologic-therapy-in-rheumatoid-arthritis\/.","journal-title":"Arthritis Rheumatol"},{"key":"437_CR26","doi-asserted-by":"publisher","first-page":"370","DOI":"10.1016\/j.bone.2015.07.037","volume":"81","author":"AR Altman","year":"2015","unstructured":"Altman AR, Tseng W-J, de Bakker CMJ, Chandra A, Lan S, Huh BK, et al. Quantification of skeletal growth, modeling, and remodeling by in vivo micro computed tomography. Bone. 2015;81:370\u20139 Available from: https:\/\/www.sciencedirect.com\/science\/article\/pii\/S8756328215003142. Cited 2020 Mar 12.","journal-title":"Bone"},{"key":"437_CR27","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1016\/j.bone.2014.12.061","volume":"73","author":"CMJ de Bakker","year":"2015","unstructured":"de Bakker CMJ, Altman AR, Tseng W-J, Tribble MB, Li C, Chandra A, et al. \u03bcCT-based, in vivo dynamic bone histomorphometry allows 3D evaluation of the early responses of bone resorption and formation to PTH and alendronate combination therapy. Bone. 2015;73:198\u2013207 Available from: https:\/\/www.sciencedirect.com\/science\/article\/pii\/S8756328214005213. Cited 2020 Mar 12.","journal-title":"Bone"},{"issue":"7","key":"437_CR28","doi-asserted-by":"publisher","first-page":"e0179413","DOI":"10.1371\/journal.pone.0179413","volume":"12","author":"JJA de Jong","year":"2017","unstructured":"de Jong JJA, Christen P, Plett RM, Chapurlat R, Geusens PP, van den Bergh JPW, et al. Feasibility of rigid 3D image registration of high-resolution peripheral quantitative computed tomography images of healing distal radius fractures. PLoS One. 2017;12(7):e0179413 Available from: https:\/\/www.ncbi.nlm.nih.gov\/pmc\/articles\/PMC5526550\/. Cited 2020 Mar 12.","journal-title":"PLoS One"}],"container-title":["BMC Medical Imaging"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12880-020-00437-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12880-020-00437-8\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12880-020-00437-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,4,6]],"date-time":"2021-04-06T19:16:09Z","timestamp":1617736569000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcmedimaging.biomedcentral.com\/articles\/10.1186\/s12880-020-00437-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,7]]},"references-count":28,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2020,12]]}},"alternative-id":["437"],"URL":"https:\/\/doi.org\/10.1186\/s12880-020-00437-8","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.2.14575\/v3","asserted-by":"object"},{"id-type":"doi","id":"10.21203\/rs.2.14575\/v1","asserted-by":"object"},{"id-type":"doi","id":"10.21203\/rs.2.14575\/v2","asserted-by":"object"}]},"ISSN":["1471-2342"],"issn-type":[{"value":"1471-2342","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,4,7]]},"assertion":[{"value":"9 September 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 March 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 April 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"All participants provided written informed consent prior to participation. Approval for all procedures was obtained by the Conjoint Health Research Ethics Board at the University of Calgary (REB17\u20130188).","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"36"}}