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Editor Richard J. Bucala, MD, PhD Yale University School of Medicine, New Haven
Deputy Editor Daniel H. Solomon, MD, MPH, Boston
Co-Editors Joseph E. Craft, MD, New Haven David T. Felson, MD, MPH, Boston Richard F. Loeser Jr., MD, Chapel Hill Peter A. Nigrovic, MD, Boston Janet E. Pope, MD, MPH, FRCPC, London, Ontario Christopher T. Ritchlin, MD, MPH, Rochester Betty P. Tsao, PhD, Charleston John Varga, MD, Chicago
Co-Editor and Review Article Editor Robert Terkeltaub, MD, San Diego
Clinical Trials Advisor Michael E. Weinblatt, MD, Boston
Social Media Editor Paul H. Sufka, MD, St. Paul
Journal Publications Committee Shervin Assassi, MD, MS, Chair, Houston Vivian Bykerk, MD, FRCPC, New York Cecilia P. Chung, MD, MPH, Nashville Meenakshi Jolly, MD, MS, Chicago Kim D. Jones, RN, PhD, FNP, Portland Maximilian Konig, MD, Baltimore Linda C. Li, PT, MSc, PhD, Vancouver Uyen-Sa Nguyen, MPH, DSc, Fort Worth
Editorial Staff Jane S. Diamond, MPH, Managing Editor, Atlanta Maggie Parry, Assistant Managing Editor, Atlanta Lesley W. Allen, Senior Manuscript Editor, Atlanta Kelly Barraza, Manuscript Editor, Atlanta Jessica Hamilton, Manuscript Editor, Atlanta Ilani S. Lorber, MA, Manuscript Editor, Atlanta Emily W. Wehby, MA, Manuscript Editor, Atlanta Sara Omer, Editorial Coordinator, Atlanta Brittany Swett, Assistant Editor, New Haven Carolyn Roth, Senior Production Editor, Boston
Associate Editors Daniel Aletaha, MD, MS, Vienna Heather G. Allore, PhD, New Haven Daniel J. Clauw, MD, Ann Arbor Robert A. Colbert, MD, PhD, Bethesda Karen H. Costenbader, MD, MPH, Boston Nicola Dalbeth, MD, FRACP, Auckland Kevin D. Deane, MD, Denver Mark C. Genovese, MD, Palo Alto
Insoo Kang, MD, New Haven Wan-Uk Kim, MD, PhD, Seoul Carol Langford, MD, MHS, Cleveland Katherine Liao, MD, MPH, Boston S. Sam Lim, MD, MPH, Atlanta Anne-Marie Malfait, MD, PhD, Chicago Paul A. Monach, MD, PhD, Boston Chester V. Oddis, MD, Pittsburgh
Andras Perl, MD, PhD, Syracuse Jack Porrino, MD, New Haven Timothy R. D. J. Radstake, MD, PhD, Utrecht William Robinson, MD, PhD, Palo Alto Georg Schett, MD, Erlangen Nan Shen, MD, Shanghai Ronald van Vollenhoven, MD, PhD, Amsterdam Fredrick M. Wigley, MD, Baltimore
Advisory Editors Abhishek Abhishek, MD, PhD, Nottingham Tom Appleton, MD, PhD, London,
Ontario Bonnie Bermas, MD, Dallas Liana Fraenkel, MD, MPH, New Haven Monica Guma, MD, PhD, La Jolla Nigil Haroon, MD, PhD, Toronto
Erica Herzog, MD, PhD, New Haven Hui-Chen Hsu, PhD, Birmingham J. Michelle Kahlenberg, MD, PhD, Ann Arbor Mariana J. Kaplan, MD, Bethesda Jonathan Kay, MD, Worcester Francis Lee, MD, PhD, New Haven Sang-Il Lee, MD, PhD, Jinju
Rik Lories, MD, PhD, Leuven Bing Lu, PhD, Boston Suresh Mahalingam, PhD, Southport,
Queensland Aridaman Pandit, PhD, Utrecht Kevin Winthrop, MD, MPH, Portland Kazuki Yoshida, MD, MPH, MS, Boston
AMERICAN COLLEGE OF RHEUMATOLOGY
Paula Marchetta, MD, MBA, New York, President Ellen M. Gravallese, MD, Worcester, President-Elect David R. Karp, MD, PhD, Dallas, Treasurer
Kenneth G. Saag, MD, MSc, Birmingham, Secretary Steven Echard, IOM, CAE, Atlanta, Executive Vice-President
© 2019 American College of Rheumatology. All rights reserved. No part of this publication may be reproduced, stored or transmitted in any form or by any means without the prior permission in writing from the copyright holder. Authorization to copy items for internal and personal use is granted by the copyright holder for libraries and other users registered with their local Reproduction Rights Organization (RRO), e.g. Copyright Clearance Center (CCC), 222 Rosewood Drive, Danvers, MA 01923, USA (www.copyright.com), provided the ap- propriate fee is paid directly to the RRO. This consent does not extend to other kinds of copying such as copying for general distribution, for advertising or promotional purposes, for creating new collective works or for resale. Special requests should be addressed to: [email protected]
Access Policy: Subject to restrictions on certain backfi les, access to the online version of this issue is available to all registered Wiley Online Library users 12 months after publication. Subscribers and eligible users at subscribing institutions have immediate access in accordance with the relevant subscription type. Please go to onlinelibrary.wiley.com for details.
The views and recommendations expressed in articles, letters, and other communications published in Arthritis & Rheumatology are those of the authors and do not necessar- ily refl ect the opinions of the editors, publisher, or American College of Rheumatology. The publisher and the American College of Rheumatology do not investigate the informa- tion contained in the classifi ed advertisements in this journal and assume no responsibility concerning them. Further, the publisher and the American College of Rheumatology do not guarantee, warrant, or endorse any product or service advertised in this journal.
Cover design: Todd Machen
This journal is printed on acid-free paper.∞
Arthritis & Rheumatology An Offi cial Journal of the American College of Rheumatology
www.arthritisrheum.org and wileyonlinelibrary.com
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Arthritis & Rheumatology An Offi cial Journal of the American College of Rheumatology
www.arthritisrheum.org and wileyonlinelibrary.com
In This Issue .............................................................................................................................................................................. A15 Clinical Connections ............................................................................................................................................................... A17
Special Articles Editorial: Evolving Use of Molecular Imaging in Research and in Practice
Ahmed Tawakol, Sebastian Unizony, Michael T. Osborne, Elena Massarotti, and Jon T. Giles ....................................................... 1207 Editorial: Picturing Giant Cell Arteritis: Projecting Into the Future
Sara K. Tedeschi and Ayaz Aghayev ....................................................................................................................................................... 1211 In Memoriam: Shaun Ruddy, MD, 1935–2019
Michael E. Weinblatt and William N. Kelley .......................................................................................................................................... 1115
Rheumatoid Arthritis Investigating Asthma, Allergic Disease, Passive Smoke Exposure, and Risk of Rheumatoid Arthritis
Vanessa L. Kronzer, Cynthia S. Crowson, Jeff rey A. Sparks, Robert Vassallo, and John M. Davis III ............................................... 1217 Derivation and Validation of a Major Toxicity Risk Score Among Nonsteroidal Antiinfl ammatory Drug Users Based on Data From a Randomized Controlled Trial
Daniel H. Solomon, Ming Shao, Kathy Wolski, Steven Nissen, M. Elaine Husni, and Nina Paynter ................................................ 1225 Development and Validation of an 18 F-Fluorodeoxyglucose–Positron Emission Tomography With Computed Tomography–Based Tool for the Evaluation of Joint Counts and Disease Activity in Patients With Rheumatoid Arthritis
Sang Jin Lee, Ju Hye Jeong, Chang-Hee Lee, Byeong-Cheol Ahn, Jung Su Eun, Na Ri Kim, Jong Whan Kang, Eon Jeong Nam, and Young Mo Kang .................................................................................................................................................... 1232
C itrullinated Inhibitor of DNA Binding 1 Is a Novel Autoantigen in Rheumatoid Arthritis Ray A. Ohara, Gautam Edhayan, Stephanie M. Rasmussen, Takeo Isozaki, Henriette A. Remmer, Thomas M. Lanigan, Phillip L. Campbell, Andrew G. Urquhart, Jeff rey N. Lawton, Kevin C. Chung, David A. Fox, and Jeff rey H. Ruth ......................... 1241
Activation of the Peroxisome Proliferator–Activated Receptor γ Coactivator 1β/NFATc1 Pathway in Circulating Osteoclast Precursors Associated With Bone Destruction in Rheumatoid Arthriti s
Jian-Da Ma, Jun Jing, Jun-Wei Wang, Ying-Qian Mo, Qian-Hua Li, Jian-Zi Lin, Le-Feng Chen, Lan Shao, Pierre Miossec, and Lie Dai ................................................................................................................................................................................................ 1252
Amelioration of Autoimmune Arthritis in Mice Treated With the DNA Methyltransferase Inhibitor 5′-Azacytidine Dániel M. Tóth, Timea Ocskó, Attila Balog, Adrienn Markovics, Katalin Mikecz, László Kovács, Meenakshi Jolly, Aleksandra A. Bukiej, Andrew D. Ruthberg, András Vida, Joel A. Block, Tibor T. Glant, and Tibor A. Rauch ................................. 1265
Osteoarthritis Disease Burden in Osteoarthritis Is Similar to That of Rheumatoid Arthritis at Initial Rheumatology Visit and Signifi cantly Greater Six Months Late r
Jacquelin R. Chua, Shakeel Jamal, Mariam Riad, Isabel Castrejon, Anne-Marie Malfait, Joel A. Block, and Theodore Pincus ....................................................................................................................................................................................... 1276
Prioritization of PLEC and GRINA as Osteoarthritis Risk Genes Through the Identifi cation and Characterization of Novel Methylation Quantitative Trait Loci
Sarah J. Rice, Maria Tselepi, Antony K. Sorial, Guillaume Aubourg, Colin Shepherd, David Almarza, Andrew J. Skelton, Ioanna Pangou, David Deehan, Louise N. Reynard, and John Loughlin ............................................................ 1285
Systemic Lupus Erythematosus Evaluating the Properties of a Frailty Index and Its Association With Mortality Risk Among Patients With Systemic Lupus Erythematosus
Alexandra Legge, Susan Kirkland, Kenneth Rockwood, Pantelis Andreou, Sang-Cheol Bae, Caroline Gordon, Juanita Romero-Diaz, Jorge Sanchez-Guerrero, Daniel J. Wallace, Sasha Bernatsky, Ann E. Clarke, Joan T. Merrill, Ellen M. Ginzler, Paul Fortin, Dafna D. Gladman, Murray B. Urowitz, Ian N. Bruce, David A. Isenberg, Anisur Rahman, Graciela S. Alarcón, Michelle Petri, Munther A. Khamashta, M. A. Dooley, Rosalind Ramsey-Goldman, Susan Manzi, Kristjan Steinsson, Asad A. Zoma, Cynthia Aranow, Meggan Mackay, Guillermo Ruiz-Irastorza, S. Sam Lim, Murat Inanc, Ronald F. van Vollenhoven, Andreas Jonsen, Ola Nived, Manuel Ramos-Casals, Diane L. Kamen, Kenneth C. Kalunian, Soren Jacobsen, Christine A. Peschken, Anca Askanase, and John G. Hanly ................................................ 1297
Pim-1 as a Therapeutic Target in Lupus Nephritis Rong Fu, Yong Xia, Meirong Li, Renxiang Mao, Chaohuan Guo, Mianjing Zhou, Hechang Tan, Meiling Liu, Shuang Wang, Niansheng Yang, and Jijun Zhao .................................................................................................................................. 1308
Clinical Images Tracheobronchial Cobblestone in Relapsing Polychondritis
Eun Bong Lee and Jin Kyun Park ............................................................................................................................................................ 1318
VOLUME 71 • August 2019 • NO. 8
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Vasculitis Diagnostic Accuracy of Positron Emission Tomography/Computed Tomography of the Head, Neck, and Chest for Giant Cell Arteritis: A Prospective, Double-Blind, Cross-Sectional Study
Anthony M. Sammel, Edward Hsiao, Geoff rey Schembri, Katherine Nguyen, Janice Brewer, Leslie Schrieber, Beatrice Janssen, Peter Youssef, Clare L. Fraser, Elizabeth Bailey, Dale L. Bailey, Paul Roach, and Rodger Laurent ................... 1319
Glucocorticoid Dosages and Acute-Phase Reactant Levels at Giant Cell Arteritis Flare in a Randomized Trial of Tocilizumab
John H. Stone, Katie Tuckwell, Sophie Dimonaco, Micki Klearman, Martin Aringer, Daniel Blockmans, Elisabeth Brouwer, Maria C. Cid, Bhaskar Dasgupta, Juergen Rech, Carlo Salvarani, Hendrik Schulze-Koops, Georg Schett, Robert Spiera, Sebastian H. Unizony, and Neil Collinson ........................................................................................... 1329
Systemic Sclerosis Prevalence, Treatment, and Outcomes of Coexistent Pulmonary Hypertension and Interstitial Lung Disease in Systemic Sclerosis
Amber Young, Dharshan Vummidi, Scott Visovatti, Kate Homer, Holly Wilhalme, Eric S. White, Kevin Flaherty, Vallerie McLaughlin, and Dinesh Khanna ............................................................................................................................................. 1339
I dentifi cation of Cysteine-Rich Angiogenic Inducer 61 as a Potential Antifi brotic and Proangiogenic Mediator in Scleroderma
Pei-Suen Tsou, Dinesh Khanna, and Amr H. Sawalha ......................................................................................................................... 1350
Myositis The IgG2 Isotype of Anti–Transcription Intermediary Factor 1γ Autoantibodies Is a Biomarker of Cancer and Mortality in Adult Dermatomyositis
Audrey Aussy, Manuel Fréret, Laure Gallay, Didier Bessis, Thierry Vincent, Denis Jullien, Laurent Drouot, Fabienne Jouen, Pascal Joly, Isabelle Marie, Alain Meyer, Jean Sibilia, Brigitte Bader-Meunier, Eric Hachulla, Mohammed Hamidou, Sophie Huë, Jean-Luc Charuel, Nicole Fabien, Pierre-Julien Viailly, Yves Allenbach, Olivier Benveniste, Nadège Cordel, Olivier Boyer, and the OncoMyositis Study Group ................................................................... 1360
Brief Report: Myositis Autoantigen Expression Correlates With Muscle Regeneration but Not Autoantibody Specifi city
Iago Pinal-Fernandez, David R. Amici, Cassie A. Parks, Assia Derfoul, Maria Casal-Dominguez, Katherine Pak, Richard Yeker, Paul Plotz, Jose C. Milisenda, Josep M. Grau-Junyent, Albert Selva-O'Callaghan, Julie J. Paik, Jemima Albayda, Andrea M. Corse, Thomas E. Lloyd, Lisa Christopher-Stine, and Andrew L. Mammen ...................................... 1371
Expression of Concern Expression of Concern Regarding “Eff ects of Hypoxia on the Expression and Activity of Cyclooxygenase 2 in Fibroblast-Like Synoviocytes: Interactions With Monocyte-Derived Soluble Mediators” (Arthritis Rheum 2004;50:2441–9) ..........................................................................................................................................................................................1376
Pediatric Rheumatology Galectin-9 and CXCL10 as Biomarkers for Disease Activity in Juvenile Dermatomyositis: A Longitudinal Cohort Study and Multicohort Validatio n
Judith Wienke, Felicitas Bellutti Enders, Johan Lim, Jorre S. Mertens, Luuk L. van den Hoogen, Camiel A. Wijngaarde, Joo Guan Yeo, Alain Meyer, Henny G. Otten, Ruth D. E. Fritsch-Stork, Sylvia S. M. Kamphuis, Esther P. A. H. Hoppenreijs, Wineke Armbrust, J. Merlijn van den Berg, Petra C. E. Hissink Muller, Janneke Tekstra, Jessica E. Hoogendijk, Claire T. Deakin, Wilco de Jager, Joël A. G. van Roon, W. Ludo van der Pol, Kiran Nistala, Clarissa Pilkington, Marianne de Visser, Thaschawee Arkachaisri, Timothy R. D. J. Radstake, Anneke J. van der Kooi, Stefan Nierkens, Lucy R. Wedderburn, Annet van Royen-Kerkhof, and Femke van Wijk .............................................................................................. 1377
Letter Excess Deaths Upon Cessation of Xanthine Oxidase Inhibitor Treatment—Data From the Cardiovascular Safety of Febuxostat and Allopurinol in Patients With Gout and Cardiovascular Morbidities Trial: Comment on the Article by Choi et al
Michael R. Bubb ....................................................................................................................................................................................... 1391
Clinical Images Dual-Energy Computed Tomography for the Noninvasive Diagnosis of Coexisting Gout and Calcium Pyrophosphate Deposition Disease
Rami Hajri, Steven D. Hajdu, Thomas Hügle, Pascal Zuff erey, Laurent Guiral, and Fabio Becce ................................................... 1392
Cover image: The fi gure on the cover (from Sammel et al, page 1319) is a fusion axial head PET/CT slice from a patient with acute biopsy-positive giant cell arteritis. Intense FDG tracer uptake is depicted by the orange/yellow color. This is seen in the bilateral superfi cial temporal arteries (anterior to the auditory canals) and maxillary arteries (adjacent to the pterygomaxillary fi ssures) and indicates active arteritis. Uptake in the cerebellum is a normal fi nding on PET/CT.
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In this Issue Highlights from this issue of A&R | By Lara C. Pullen, PhD
Frailty Index for Patients With Systemic Lupus Erythematosus In this issue, Legge et al (p. 1297) report on their derivation and evaluation of the properties of a frailty index (FI) constructed using data from the Systemic
Lupus International Collaborating Clinics (SLICC) inception
cohort. They used a well-characterized, international cohort of patients, who were enrolled within 15 months of systemic lupus erythematosus (SLE) diagnosis, to create a novel, internally validated health measure for SLE.
The baseline data set included 1,683 patients with SLE, 89% of whom were female. The patients had a mean ± SD age of 35.7 ± 13.4 years and a mean ± SD disease duration of 18.8 ± 15.7 months. At baseline, the mean ± SD SLICC-FI score was 0.17 ± 0.08, and the baseline SLICC- FI values exhibited the expected measure- ment properties, such as their associations with sex and age, that had been consis- tently demonstrated by other frailty indices
in non-lupus populations. The baseline SLICC-FI values were also only weakly correlated with baseline SLICC/American College of Rheumatology Damage Index (SDI) scores. After adjusting for age, sex, steroid use, ethnicity/region, and base- line SDI scores, higher baseline SLICC- FI values were associated with increased
mortality risk. The investigators concluded that the SLICC-FI score is potentially valu- able for quantifying vulnerability among patients with SLE and, therefore, adds to existing prognostic scores, especially with predicting future risk of mortality. Frailty also may prove useful in assessing clinical outcome from experimental interventions.
Positron emission tomography (PET) can identify the presence and intensity of infl ammation in arthritic joints. However, it is still unclear to what extent PET-assessed joint counts might be useful in clarifying positive fi ndings of synovitis on clinical joint counts or the extent
of disease activity. While clinical joint count assessment is important for detecting synovitis, its reliability is a subject of controversy. In this
issue, Lee et al (p. 1232) report on their study in which they assess the correlation of PET-derived parameters in 68 joints with disease activity and compare the reliability of joint counts between PET with computed tomography (CT) and clinical assessment in patients with rheumatoid arthritis (RA). Their data indicate that PET-CT could serve as a sensitive and reliable method for evaluating disease activity in RA patients.
The investigators found that the number of PET-positive joints was signifi cantly correlated with the swollen joint count (SJC),
the tender joint count (TJC), and the Disease Activity Score in 28 joints using the erythrocyte sedimentation rate (DAS28-ESR). Moreover, the intraobserver and interobserver reliability of PET for the affected joint counts was excellent. Specifi cally, interobserver reliability between nuclear medicine physicians and rheumatologists was good for the SJC and TJC in both 28 joints and 68 joints.
The researchers performed multivariate analyses that included the ESR and patient global assessment of disease activity (PtGA), in addition to PET-derived parameters, and derived the PET/DAS as follows: (0.063 × number of PET-positive joints in 28 joints) + (0.011 × ESR) + (0.030 × PtGA). In the validation group they found a signifi cant correlation between the PET/DAS and the DAS28-ESR. The results suggest that the PET/DAS might be a useful research tool, particularly in clinical trials.
Development and Validation of a PET-CT Tool for Rheumatoid Arthritis
p. 1297
p. 1232
Figure 1. Observed distribution of the SLICC-FI scores at baseline (n = 1,682) (SLICC-FI scores could not be calculated in 1 patient due to missing data) and at last follow-up visit (n = 1,507) among SLE patients in the SLICC SLE inception cohort.
15
Derivation and Validation of a Major Toxicity Risk Score for NSAID Use Nonsteroidal antiinflammatory drugs (NSAIDs) are commonly prescribed, even though they may cause major toxicity. A more precise understanding
of the risk associ- ated with this class of drugs would make it
possible for rheumatologists to more accu- rately calculate the risk/benefi t ratio for a given patient. In this issue, Solomon et al (p. 1225) report on their derivation and validation of a risk score for major toxicity among a large cohort of well-phenotyped
NSAID users enrolled in a randomized clinical trial.
The researchers found multiple signif- icant variables in their derivation cohort: age, male sex, history of cardiovascular disease, hypertension, diabetes mellitus, tobacco use, statin use, elevated serum creatinine level, hematocrit level, and type of arthritis. They assigned patients to 3 risk groups (low, intermediate, and high) and found that the risk score could accurately categorize the 1-year risk of major toxicity among NSAID users with a C-index of 0.73
Both osteoarthritis (OA) and rheumatoid arthritis (RA) have primary symptoms of pain and functional disability. Although historically RA has been regarded as a more severe form of arthritis than OA, one previous study suggested a similar or greater disease burden in OA compared
to RA, which may have been explained by better RA treatments. In this issue, Chua et al (p. 1276) report their analysis of disease burden in OA
using Multidimensional Health Assessment Questionnaire (MDHAQ)/ Routine Assessment of Patient Index Data (RAPID3) scores at the initial visit and a 6-month follow-up visit to one rheumatology site. The investigators used RA as a benchmark for high disease burden and compared the OA scores to the RA scores.
The retrospective study included patients at the Rush University Medical Center in Chicago, Illinois, at which all patients complete the MDHAQ in paper form at all visits in routine care. Responses are saved as PDF fi les in the electronic health record. The researchers examined responses for new OA and RA patients seen between May 2011 and February 2017, and calculated 0–10 MDHAQ scores for physical function, pain, and global assessment compiled into composite 0–30 RAPID3 scores, at the initial and the 6-month follow-up visits. They classifi ed patients as self- or physician referred, and RA patients were classifi ed as disease-modifying antirheumatic drug (DMARD) naive or as having had prior DMARD treatment.
Compared to RA patients, OA patients had higher age, body mass index (BMI), and disease duration, and all analyses were adjusted for these variables. The investigators found no signifi cant difference in RAPID3 scores between OA versus RA patients, whether DMARD naive or having prior DMARD treatment or
whether self- or physician-referred. After 6 months, however, while all patients were improved, RAPID3 scores were improved signifi cantly more in RA patients than in OA patients following adjustment for age, BMI, disease duration, education level, and ethnicity. Thus, while mean MDHAQ/RAPID3 scores were similar in OA and RA patients at the initial visit, 6 months later mean scores were higher in OA patients, although at an individual level, some patients with RA had higher disease than OA patients and vice versa. These fi ndings likely refl ect superior RA treatments. The results also suggest that the same MDHAQ/RAPID3 allows comparison of disease burdens in different diseases.
Disease Burden of OA Similar to RA at Initial Visit to a Rheumatology Site
in the validation cohort and 0.71 in the total cohort. When the investigators applied the model to the total population with complete data (n = 23,735), they found that 4.6% had a predicted 1-year risk of major toxicity of <1%, 68.6% had a predicted risk of 1–4%, and 26.9% had a predicted risk of >4%. Although it is still important to…