{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T01:32:23Z","timestamp":1792805543082,"version":"4.5.0"},"reference-count":52,"publisher":"MDPI AG","issue":"17","license":[{"start":{"date-parts":[[2022,8,26]],"date-time":"2022-08-26T00:00:00Z","timestamp":1661472000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"the National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81771706"],"award-info":[{"award-number":["81771706"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"the National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["BYSYDL2021005"],"award-info":[{"award-number":["BYSYDL2021005"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"the Clinical Cohort Construction Program of Peking University Third Hospital","award":["81771706"],"award-info":[{"award-number":["81771706"]}],"id":[{"id":"https:\/\/ror.org\/04wwqze12","id-type":"ROR","asserted-by":"crossref"}]},{"name":"the Clinical Cohort Construction Program of Peking University Third Hospital","award":["BYSYDL2021005"],"award-info":[{"award-number":["BYSYDL2021005"]}],"id":[{"id":"https:\/\/ror.org\/04wwqze12","id-type":"ROR","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>It is important for clinicians to determine the risk of worsening trajectories in SSc patients. The Scleroderma Clinical Trials Consortium (SCTC) Damage Index (DI) has been developed to quantify organ damage and shows good capability for mortality and morbidity prediction in patients with SSc. This retrospective study aimed to describe the SCTC-DI in Chinese SSc patients and to find features predicting worse organ damage trajectories based on SCTC-DI. A total of 433 SSc patients who met the inclusion criteria in the Peking University Third Hospital (PKUTH-SSc) and People\u2019s Hospital SSc cohort (PKUPH-SSc) were recruited for our study. Organ damage was relatively mild in our Chinese SSc cohort compared to other cohorts, with a mean SCTC-DI of 5.21 \u00b1 4.60. We used both SCTC-DI \u2265 6 and \u22654 to define the high burden of organ damage and established two risk models by the LASSO algorithm, which revealed good identification of high organ damage burden (AUC = 0.689, 95% CI 0.636 to 0.742, p &lt; 0.001 in SCTC-DI \u2265 6 model; AUC = 0.694, 95% CI 0.641 to 0.746, p &lt; 0.001 in modified SCTC-DI \u2265 4 model). The anemia index at the baseline was included in these two models and was also independently related to organ damage progression (HR = 1.75, 95% CI 1.16 to 2.66, p = 0.008). In addition, the presence of an anti-Scl-70 autoantibody was also a predictor of progression (HR = 1.91, 95% CI 1.22 to 2.99, p = 0.005). In conclusion, anemia at the baseline was an important indicator for worse organ damage trajectories in SSc patients. We recommend using hemoglobin as a potential biomarker to evaluate organ damage in SSc patients.<\/jats:p>","DOI":"10.3390\/jcm11175013","type":"journal-article","created":{"date-parts":[[2022,8,29]],"date-time":"2022-08-29T03:34:56Z","timestamp":1661744096000},"page":"5013","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Anemia Is an Indicator for Worse Organ Damage Trajectories in Patients with Systemic Sclerosis: A Retrospective Study"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6169-7767","authenticated-orcid":false,"given":"Zhaohua","family":"Li","sequence":"first","affiliation":[{"name":"Department of Rheumatology and Immunology, Peking University Third Hospital, No.49 Huayuan North Road, Haidian District, Beijing 100191, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dan","family":"Xu","sequence":"additional","affiliation":[{"name":"Department of Rheumatology and Immunology, Peking University Third Hospital, No.49 Huayuan North Road, Haidian District, Beijing 100191, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xintong","family":"Jiang","sequence":"additional","affiliation":[{"name":"Department of Rheumatology and Immunology, Peking University People\u2019s Hospital, No.11 Xizhimen South Street, Xicheng District, Beijing 100044, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ting","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Rheumatology and Immunology, Peking University Third Hospital, No.49 Huayuan North Road, Haidian District, Beijing 100191, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yin","family":"Su","sequence":"additional","affiliation":[{"name":"Department of Rheumatology and Immunology, Peking University People\u2019s Hospital, No.11 Xizhimen South Street, Xicheng District, Beijing 100044, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rong","family":"Mu","sequence":"additional","affiliation":[{"name":"Department of Rheumatology and Immunology, Peking University Third Hospital, No.49 Huayuan North Road, Haidian District, Beijing 100191, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1186\/s13075-021-02548-1","article-title":"Clinical characteristics, visceral involvement, and mortality in at-risk or early diffuse systemic sclerosis: A longitudinal analysis of an observational prospective multicenter US cohort","volume":"23","author":"Jaafar","year":"2021","journal-title":"Arthritis Res. Ther."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1002\/art.40027","article-title":"Early Mortality in a Multinational Systemic Sclerosis Inception Cohort","volume":"69","author":"Hao","year":"2017","journal-title":"Arthritis Rheumatol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1897","DOI":"10.1136\/annrheumdis-2017-211448","article-title":"Mapping and predicting mortality from systemic sclerosis","volume":"76","author":"Elhai","year":"2017","journal-title":"Ann. Rheum. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1186\/s13075-019-1867-1","article-title":"Survival and prognosis factors in systemic sclerosis: Data of a French multicenter cohort, systematic review, and meta-analysis of the literature","volume":"21","author":"Pokeerbux","year":"2019","journal-title":"Arthritis Res. Ther."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1186\/s13075-018-1735-4","article-title":"Prognostic profile of systemic sclerosis: Analysis of the clinical EUSTAR cohort in China","volume":"20","author":"Hu","year":"2018","journal-title":"Arthritis Res. Ther."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1136\/ard.2006.066340","article-title":"Survival and causes of death in 366 Hungarian patients with systemic sclerosis","volume":"67","author":"Nagy","year":"2008","journal-title":"Ann. Rheum. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1242","DOI":"10.1136\/annrheumdis-2019-215145","article-title":"Predictors of disease worsening defined by progression of organ damage in diffuse systemic sclerosis: A European Scleroderma Trials and Research (EUSTAR) analysis","volume":"78","author":"Becker","year":"2019","journal-title":"Ann. Rheum. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1136\/annrheumdis-2021-eular.1067","article-title":"Progressive interstitial lung disease in patients with systemic sclerosis-associated interstitial lung disease in the EUSTAR database","volume":"80","author":"Allanore","year":"2021","journal-title":"Ann. Rheum. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1002\/acr.24411","article-title":"Trends in Systemic Sclerosis Mortality Over Forty-Eight Years, 1968-2015: A US Population-Based Study","volume":"73","author":"Yen","year":"2021","journal-title":"Arthritis Care Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1183\/23120541.00309-2019","article-title":"Trends in systemic sclerosis and systemic sclerosis-related pulmonary arterial hypertension mortality in the USA","volume":"6","author":"Ratanawatkul","year":"2020","journal-title":"ERJ Open Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1002\/art.40906","article-title":"Phenotypes Determined by Cluster Analysis and Their Survival in the Prospective European Scleroderma Trials and Research Cohort of Patients With Systemic Sclerosis","volume":"71","author":"Sobanski","year":"2019","journal-title":"Arthritis Rheumatol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e137567","DOI":"10.1172\/jci.insight.137567","article-title":"Regulator combinations identify systemic sclerosis patients with more severe disease","volume":"5","author":"Wang","year":"2020","journal-title":"JCI Insight"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1136\/annrheumdis-2019-215894","article-title":"Global skin gene expression analysis of early diffuse cutaneous systemic sclerosis shows a prominent innate and adaptive inflammatory profile","volume":"79","author":"Skaug","year":"2020","journal-title":"Ann. Rheum. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1136\/annrheumdis-2019-215787","article-title":"Revised European Scleroderma Trials and Research Group Activity Index is the best predictor of short-term severity accrual","volume":"78","author":"Fasano","year":"2019","journal-title":"Ann. Rheum. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1111","DOI":"10.1093\/rheumatology\/kex015","article-title":"Predictive value of European Scleroderma Group Activity Index in an early scleroderma cohort","volume":"56","author":"Nevskaya","year":"2017","journal-title":"Rheumatology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1016\/j.autrev.2018.02.008","article-title":"Predictors of morbidity and mortality in early systemic sclerosis: Long-term follow-up data from a single-centre inception cohort","volume":"17","author":"Panopoulos","year":"2018","journal-title":"Autoimmun. Rev."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1136\/annrheumdis-2018-214764","article-title":"Development and validation of the Scleroderma Clinical Trials Consortium Damage Index (SCTC-DI): A novel instrument to quantify organ damage in systemic sclerosis","volume":"78","author":"Ferdowsi","year":"2019","journal-title":"Ann. Rheum. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Barbacki, A., Baron, M., Wang, M., Zhang, Y., Stevens, W., Sahhar, J., Proudman, S., Nikpour, M., and Man, A. (2022). Damage Trajectories in Systemic Sclerosis Using Group-Based Trajectory Modeling. Arthritis Care Res., published online ahead of print.","DOI":"10.1002\/acr.24873"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"151973","DOI":"10.1016\/j.semarthrit.2022.151973","article-title":"Associations between the Composite Response Index in Diffuse Cutaneous Systemic Sclerosis (CRISS), survival and other disease measures","volume":"53","author":"Zheng","year":"2022","journal-title":"Semin. Arthritis Rheum."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"721","DOI":"10.55563\/clinexprheumatol\/sd1exj","article-title":"A multi-predictor model to predict risk of scleroderma renal crisis in systemic sclerosis: A multicentre, retrospective, cohort study","volume":"39","author":"Xu","year":"2021","journal-title":"Clin. Exp. Rheumatol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2737","DOI":"10.1002\/art.38098","article-title":"2013 classification criteria for systemic sclerosis: An American College of Rheumatology\/European League against Rheumatism collaborative initiative","volume":"65","author":"Khanna","year":"2013","journal-title":"Arthritis Rheum."},{"key":"ref_22","first-page":"202","article-title":"Scleroderma (systemic sclerosis): Classification, subsets and pathogenesis","volume":"15","author":"LeRoy","year":"1988","journal-title":"J. Rheumatol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4662","DOI":"10.1093\/rheumatology\/keab075","article-title":"Defining the optimal disease duration of early diffuse systemic sclerosis for clinical trial design","volume":"60","author":"Domsic","year":"2021","journal-title":"Rheumatology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1111\/ijlh.12693","article-title":"ICSH recommendations for modified and alternate methods measuring the erythrocyte sedimentation rate","volume":"39","author":"Kratz","year":"2017","journal-title":"Int. J. Lab. Hematol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1747","DOI":"10.1182\/blood-2005-07-3046","article-title":"The definition of anemia: What is the lower limit of normal of the blood hemoglobin concentration?","volume":"107","author":"Beutler","year":"2006","journal-title":"Blood"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e017684","DOI":"10.1161\/JAHA.120.017684","article-title":"Elevated Pulmonary Pressure Noted on Echocardiogram: A Simplified Approach to Next Steps","volume":"10","author":"Kanwar","year":"2021","journal-title":"J. Am. Heart Assoc."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1111\/j.1467-9868.2011.00771.x","article-title":"Regression shrinkage and selection via the lasso: A retrospective","volume":"73","author":"Tibshirani","year":"2011","journal-title":"J. R. Stat. Soc. Ser. B"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"787","DOI":"10.3899\/jrheum.080915","article-title":"Ethnic influence on disease manifestations and autoantibodies in Chinese-descent patients with systemic sclerosis","volume":"36","author":"Low","year":"2009","journal-title":"J. Rheumatol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.3899\/jrheum.180042","article-title":"Ethnic Variations in Systemic Sclerosis Disease Manifestations, Internal Organ Involvement, and Mortality","volume":"46","author":"Ahmad","year":"2019","journal-title":"J. Rheumatol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1878","DOI":"10.1093\/rheumatology\/kez532","article-title":"The clinical and economic burden of systemic sclerosis related interstitial lung disease","volume":"59","author":"Morrisroe","year":"2020","journal-title":"Rheumatology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1684","DOI":"10.1093\/rheumatology\/kez486","article-title":"Racial differences in systemic sclerosis disease presentation: A European Scleroderma Trials and Research group study","volume":"59","author":"Jaeger","year":"2020","journal-title":"Rheumatology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2986","DOI":"10.1002\/art.34482","article-title":"A clinical and serologic comparison of African American and Caucasian patients with systemic sclerosis","volume":"64","author":"Steen","year":"2012","journal-title":"Arthritis Rheum."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"799","DOI":"10.3899\/jrheum.160574","article-title":"Antifibrillarin Antibodies Are Associated with Native North American Ethnicity and Poorer Survival in Systemic Sclerosis","volume":"44","author":"Assassi","year":"2017","journal-title":"J. Rheumatol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"3401","DOI":"10.1093\/rheumatology\/keab929","article-title":"Screening and management of subclinical interstitial lung disease in systemic sclerosis: An international survey","volume":"61","author":"Hoa","year":"2021","journal-title":"Rheumatology"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1002\/art.1780340405","article-title":"Predictors of survival in systemic sclerosis (scleroderma)","volume":"34","author":"Altman","year":"1991","journal-title":"Arthritis Rheum."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1616","DOI":"10.1002\/art.38381","article-title":"Derivation and validation of a prediction rule for two-year mortality in early diffuse cutaneous systemic sclerosis","volume":"66","author":"Domsic","year":"2014","journal-title":"Arthritis Rheumatol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1631","DOI":"10.1007\/s10067-016-3245-6","article-title":"Predictors of inpatient mortality in patients with systemic sclerosis: A case control study","volume":"35","author":"Sehra","year":"2016","journal-title":"Clin. Rheumatol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2279","DOI":"10.1007\/s00296-018-4156-4","article-title":"High burden of skin sclerosis is associated with severe organ involvement in patients with systemic sclerosis and systemic sclerosis overlap syndrome","volume":"38","author":"Wannarong","year":"2018","journal-title":"Rheumatol. Int."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2460","DOI":"10.1007\/s12325-020-01330-0","article-title":"Healthcare Resource Utilization Among Patients in England with Systemic Sclerosis-Associated Interstitial Lung Disease: A Retrospective Database Analysis","volume":"37","author":"Gayle","year":"2020","journal-title":"Adv. Ther."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1136\/annrheumdis-2013-204487","article-title":"Disease progression in systemic sclerosis-overlap syndrome is significantly different from limited and diffuse cutaneous systemic sclerosis","volume":"74","author":"Moinzadeh","year":"2015","journal-title":"Ann. Rheum. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"v54","DOI":"10.1093\/rheumatology\/ken307","article-title":"Renal manifestations of systemic sclerosis--clinical features and outcome assessment","volume":"47","author":"Denton","year":"2008","journal-title":"Rheumatology"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"603","DOI":"10.3899\/jrheum.090600","article-title":"Gastric antral vascular ectasia in systemic sclerosis: Demographics and disease predictors","volume":"37","author":"Ingraham","year":"2010","journal-title":"J. Rheumatol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.1681\/ASN.2013010030","article-title":"Plasticity of renal erythropoietin-producing cells governs fibrosis","volume":"24","author":"Souma","year":"2013","journal-title":"J. Am. Soc. Nephrol. JASN"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.kint.2022.04.026","article-title":"Lineage tracing analysis defines erythropoietin-producing cells as a distinct subpopulation of resident fibroblasts with unique behaviors","volume":"102","author":"Kaneko","year":"2022","journal-title":"Kidney Int."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4075","DOI":"10.1038\/s41467-020-17942-7","article-title":"Micro-environmental sensing by bone marrow stroma identifies IL-6 and TGFbeta1 as regulators of hematopoietic ageing","volume":"11","author":"Valletta","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1182\/blood-2018-06-856500","article-title":"Anemia of inflammation","volume":"133","author":"Weiss","year":"2019","journal-title":"Blood"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1989","DOI":"10.1002\/art.39655","article-title":"Toll-like Receptor 9 Signaling Is Augmented in Systemic Sclerosis and Elicits Transforming Growth Factor beta-Dependent Fibroblast Activation","volume":"68","author":"Fang","year":"2016","journal-title":"Arthritis Rheumatol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Akilesh, H.M., Buechler, M.B., Duggan, J.M., Hahn, W.O., Matta, B., Sun, X., Gessay, G., Whalen, E., Mason, M., and Presnell, S.R. (2019). Chronic TLR7 and TLR9 signaling drives anemia via differentiation of specialized hemophagocytes. Science, 363.","DOI":"10.1126\/science.aao5213"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1186\/s13075-019-2057-x","article-title":"Inflammatory stays inflammatory: A subgroup of systemic sclerosis characterized by high morbidity and inflammatory resistance to cyclophosphamide","volume":"21","author":"Mitev","year":"2019","journal-title":"Arthritis Res. Ther."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1002\/art.38994","article-title":"Clinical and immunologic predictors of scleroderma renal crisis in Japanese systemic sclerosis patients with anti-RNA polymerase III autoantibodies","volume":"67","author":"Hamaguchi","year":"2015","journal-title":"Arthritis Rheumatol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1111\/1346-8138.12722","article-title":"Demographic and clinical features of systemic sclerosis patients with anti-RNA polymerase III antibodies","volume":"42","author":"Motegi","year":"2015","journal-title":"J. Dermatol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1007\/s10067-019-04806-9","article-title":"Analysis of anti-RNA polymerase III antibodies in Chinese Han systemic sclerosis patients","volume":"39","author":"Liu","year":"2020","journal-title":"Clin. Rheumatol."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/17\/5013\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:15:53Z","timestamp":1760141753000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/17\/5013"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,26]]},"references-count":52,"journal-issue":{"issue":"17","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["jcm11175013"],"URL":"https:\/\/doi.org\/10.3390\/jcm11175013","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,26]]}}}