Top

Published in:

01-01-2020 | Antimalaria | Original Article

Survival analysis of patients with Sjögren’s syndrome in Turkey: a tertiary hospital-based study

Authors: Veli Yazisiz, Mesut Göçer, Funda Erbasan, İsmail Uçar, Bengisu Aslan, Şuayp Oygen, Edip Gökalp Gök, Mustafa Ender Terzioğlu

Published in: Clinical Rheumatology | Issue 1/2020

Abstract

Objectives

This study was conducted to determine long-term survival rates and the factors associated with mortality in Turkish primary Sjögren syndrome (pSS) patients.

Methods

All patients diagnosed with pSS between 2004 and 2014 were included in this study. By January 2019, all subjects still living by the end of the study, as well as any death, were identified. Survival rates and standard mortality rates (SMRs) using general population mortality data were calculated. Mortality-related factors were determined by univariate and multivariate analysis.

Results

During follow-up, 33 cases of 372 pSS patients resulted in death (8.9%). Of those patients, they were typically older at disease onset, at recruitment, and had shorter follow-up times (p < 0.001 for all). The overall SMR of all pSS patients compared with the general population was 2.11 (95% confidence interval (CI) 1.39–2.83). Male pSS patients had a higher SMR than that of general male patients. Overall survival rates were 97.8% at five years, 90.2% at 10 years, and 87.1% at 15 years in patients with pSS. The survival rate of pSS patients was significantly lower than the general Turkish population (p = 0.011). Multivariate Cox regression analysis showed that older age at disease onset and the presence of interstitial lung disease (ILD) were independent risk factors for mortality.

Conclusions

Based on these data, mortality rates of Turkish pSS patients are higher compared with the general population. Survival significantly decreased in the pSS patients with ILD, especially in older male patients at disease onset. Male gender and malignancy may also be associated with a worse prognosis in pSS patients.

Key Point

• Mortality in Sjögren’s syndrome.

Fox RI (2005) Sjogren’s syndrome. Lancet 366(9482):321–331CrossRef

Kassan SS, Moutsopoulos HM (2004) Clinical manifestations and early diagnosis of Sjögren syndrome. Arch Intern Med 164:1275–1284CrossRef

Martens PB, Pillemer SR, Jacobsson LT, O’Fallon WM, Matteson EL (1999) Survivorship in a population based cohort of patients with Sjögren’s syndrome, 1976–1992. J Rheumatol 26:1296–1300PubMed

Theander E, Manthorpe R, Jacobsson LT (2004) Mortality and causes of death in primary Sjögren’s syndrome: a prospective cohort study. Arthritis Rheum 50(4):1262–1269CrossRef

Kruize AA, Hené RJ, van der Heide A, Bodeutsch C, de Wilde PC, van Bijsterveld OP, de Jong J, Feltkamp TE, Kater L, Bijlsma JW (1996) Long-term followup of patients. Arthritis Rheum 39:297–303CrossRef

Skopouli FN, Dafni U, Ioannidis JP, Moutsopoulos HM (2000) Clinical evolution, and morbidity and mortality of primary Sjögren’s syndrome. Semin Arthritis Rheum. 29(5):296–304CrossRef

Ioannidis JP, Vassiliou VA, Moutsopoulos HM (2002) Long-term risk of mortality and lymphoproliferative disease and predictive classification of primary Sjögren’s syndrome. Arthritis Rheum 46:741–747CrossRef

Weng MY, Huang YT, Liu MF, Lu TH (2011) Incidence and mortality of treated primary Sjogren’s syndrome in Taiwan: a population-based study. J Rheumatol 38(4):706–708. https://doi.org/10.3899/jrheum.100883 CrossRefPubMed

Moutsopoulos HM (2014) Sjögren’s syndrome: a forty-year scientific journey. J Autoimmun 51:1–9. https://doi.org/10.1016/j.jaut.2014.01.001 CrossRefPubMed

10.

Palm Q, Garen T, Enger TB, Jensen JL, Lund MB, Aalokken TM, Gran JT (2013) Clinical pulmonary involvement in primary Sjogren’s syndrome: prevalence, quality of life and mortality-a retrospective study based on registry data. Rheumatology (Oxford) 52(1):173–179. https://doi.org/10.1093/rheumatology/kes311 CrossRef

11.

Voulgarelis M, Tzioufas AG, Moutsopoulos HM (2008) Mortality in Sjögren’s syndrome. Clin Exp Rheumatol 26(5 Suppl 51):S66–S71PubMed

12.

Davidson BK, Kelly CA, Griffiths ID (1999) Primary Sjögren’s syndrome in the North East of England: a long-term follow-up study. Rheumatology (Oxford) 38:245–243CrossRef

13.

Pertovaara M, Pukkala E, Laippala P, Miettinen A, Pasternack A (2001) A longitudinal cohort study of Finnish patients with primary Sjögren’s syndrome: clinical, immunological, and epidemiological aspects. Ann Rheum Dis 60:467–472CrossRef

14.

Alamanos Y, Tsifetaki N, Voulgari PV, Venetsanopoulou AI, Siozos C, Drosos AA (2006) Epidemiology of primary Sjögren’s syndrome in north-west Greece, 1982–2003. Rheumatology (Oxford) 45:187–191CrossRef

15.

Brito-Zerón P, Kostov B, Solans R, Fraile G, Suárez-Cuervo C, Casanovas A, Rascón FJ, Qanneta R, Pérez-Alvarez R, Ripoll M, Akasbi M, Pinilla B, Bosch JA, Nava-Mateos J, Díaz-López B, Morera-Morales ML, Gheitasi H, Retamozo S, Ramos-Casals M, SS Study Group, Autoimmune Diseases Study Group (GEAS), Spanish Society of Internal Medicine (SEMI) (2016) Systemic activity and mortality in primary Sjögren syndrome: predicting survival using the EULAR-SS Disease Activity Index (ESSDAI) in 1045 patients. Ann Rheum Dis 75(2):348–355. https://doi.org/10.1136/annrheumdis-2014-206418 CrossRefPubMed

16.

Zhang W, Feng S, Yan S, Zhao Y, Li M, Sun J, Zhang FC, Cui Q, Dong Y (2010) Incidence of malignancy in primary Sjogren’s syndrome in a Chinese cohort. Rheumatology (Oxford) 49:571–577CrossRef

17.

Panchovska M, Sheitanov Y, Uzunov N (2004) Mortality of Bulgarian patients with primary and secondary Sjogren’s syndrome. Bratisl Lek Listy 105(12):434PubMed

18.

Kim HJ, Kim KH, Hann HJ, Han S, Kim Y, Lee SH, Kim DS, Ahn HS (2017) Incidence, mortality, and causes of death in physician-diagnosed primary Sjögren’s syndrome in Korea: a nationwide, population-based study. Semin Arthritis Rheum 47(2):222–227. https://doi.org/10.1016/j.semarthrit.2017.03.004 CrossRefPubMed

19.

Kabasakal Y, Kitapçıoğlu G, Karabulut G, Tezcan M, Balkarlı A, Aksoy A, Yavuz Ş, Yılmaz S, Kaşifoğlu T, Kalyoncu U, Dalkılıç E, Tufan A, Mercan R, Yıldız F, Şentürk T, Önen F, Bes C, Erken E, Tunç E, Kamalı S, Tarhan E, Yazıcı A, Düzgün N, Bıçakçıgil M, Yılmaz S, Özmen M, Öcal L, Alibaz-Öner F, Solmaz D, Çobankara V, Nalbant S, Kasapoğlu Günal E, Kaşkari D, Göker B (2017) Criteria sets for primary Sjogren’s syndrome are not adequate for those presenting with extraglandular organ involvements as their dominant clinical features. Rheumatol Int 37(5):675–684. https://doi.org/10.1007/s00296-017-3691-8 CrossRefPubMed

20.

Shiboski SC, Shiboski CH, Criswell LA, Baer AN, Challacombe S, Lanfranchi H, Schiødt M, Umehara H, Vivino F, Zhao Y, Dong Y, Greenspan D, Heidenreich AM, Helin P, Kirkham B, Kitagawa K, Larkin G, Li M, Lietman T, Lindegaard J, McNamara N, Sack K, Shirlaw P, Sugai S, Vollenweider C, Whitcher J, Wu A, Zhang S, Zhang W, Greenspan JS, Daniels TE, Sjögren’s International Collaborative Clinical Alliance (SICCA) Research Groups (2012) American College of Rheumatology classification criteria for Sjögren’s syndrome: a data-driven, expert consensus approach in the Sjögren’s International Collaborative Clinical Alliance Cohort. Arthritis Care Res 64(4):475–487CrossRef

21.

Daniels TE, Cox D, Shiboski CH, Schiødt M, Wu A, Lanfranchi H, Umehara H, Zhao Y, Challacombe S, Lam MY, de Souza Y, Schiødt J, Holm H, Bisio PAM, Gandolfo MS, Sawaki T, Li M, Zhang W, Varghese-Jacob B, Ibsen P, Keszler A, Kurose N, Nojima T, Odell E, Criswell LA, Jordan R, Greenspan JS, Sjögren’s International Collaborative Clinical Alliance Research Groups (2011) Associations between salivary gland histopathologic diagnoses and phenotypic features of Sjögren’s syndrome among 1,726 registry participants. Arthritis Rheum 63:2021–2030CrossRef

22.

American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias (2002) This joint statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS board of directors, June 2001 and by the ERS Executive Committee, June 2001. Am J Respir Crit Care Med 165:277–304CrossRef

23.

Andersen PK, Borgan O, Gill RD et al (1993) Statistical models based on counting processes, vol 18. Springer-Verlag, New York, p 322CrossRef

24.

Valesini G, Priori R, Bavoillot D, Osborn J, Danieli MG, Del Papa N et al (1997) Differential risk of non-Hodgkin’s lymphoma in Italian patients with primary Sjögren’s syndrome. J Rheumatol 24:2376–2380PubMed

25.

Maciel G, Crowson CS, Matteson EL, Cornec D (2017) Incidence and mortality of physician-diagnosed primary Sjögren syndrome: time trends over a 40-year period in a population-based US cohort. Mayo Clin Proc 92(5):734–743. https://doi.org/10.1016/j.mayocp.2017.01.020 CrossRefPubMedPubMedCentral

26.

Singh AG, Singh S, Matteson EL (2016) Rate, risk factors and causes of mortality in patients with Sjögren’s syndrome: a systematic review and meta-analysis of cohort studies. Rheumatology (Oxford) 55(3):450–460. https://doi.org/10.1093/rheumatology/kev354 CrossRef

27.

Yazısız V, Avcı AB, Erbasan F, Kiriş E, Terzioğlu E (2009) Diagnostic performance of minor salivary gland biopsy, serological and clinical data in Sjogren’s syndrome: a retrospective analysis. Rheumatol Int 29:403–409. https://doi.org/10.1007/s00296-008-0698-1 CrossRefPubMed

28.

Yazısız V, Arslan G, Özbudak AH, Türker S, Erbasan F, Avcı AB, Ozbudak O, Terzioglu (2010) Lung involvement in patients with primary Sjögren’s syndrome: what are the predictors? Rheumatol Int 30:1317–1324. https://doi.org/10.1007/s00296-009-1152-8 CrossRefPubMed

29.

Ramos-Casals M, Solans R, Rosas J, Camps MT, Gil A, Del Pino-Montes J, Alvo-Alen J, Jiménez-Alonso J, Micó ML, Beltrán J, Belenguer R, Pallarés L, GEMESS Study Group (2008) Primary Sjögren syndrome in Spain: clinical and immunologic expression in 1010 patients. Medicine (Baltimore) 87(4):210–219. https://doi.org/10.1097/MD.0b013e318181e6af CrossRef

30.

Ibn Yacoub Y, Rostom S, Laatiris A, Hajjaj-Hassouni N (2012) Primary Sjögren’s syndrome in Moroccan patients: characteristics, fatigue and quality of life. Rheumatol Int 32(9):2637–2643. https://doi.org/10.1007/s00296-011-2009-5 CrossRefPubMed

31.

Nannini C, Jebakumar AJ, Crowson CS, Ryu JH, Matteson EL (2013) Primary Sjogren’s syndrome 1976-2005 and associated interstitial lung disease: a population-based study of incidence and mortality. BMJ Open 3(11):e003569. https://doi.org/10.1136/bmjopen-2013-003569 CrossRefPubMedPubMedCentral

32.

Ito I, Nagai S, Kitaichi M, Nicholson AG, Johkoh T, Noma S, Kim DS, Handa T, Izumi T, Mishima M (2005) Pulmonary manifestations of primary Sjogren’s syndrome: a clinical, radiologic, and pathologic study. Am J Respir Crit Care Med 171:632–638CrossRef

33.

Enomoto Y, Takemura T, Hagiwara E, Iwasawa T, Fukuda Y, Yanagawa N, Sakai F, Baba T, Nagaoka S, Ogura T (2013) Prognostic factors in interstitial lung disease associated with primary Sjogren’s syndrome: a retrospective analysis of 33 pathologically-proven cases. PLoS One 8:e73774. https://doi.org/10.1371/journal.pone.0073774 CrossRefPubMedPubMedCentral

34.

Gao H, Zhang XW, He J, Zhang J, An Y, Sun Y, Jia RL, Li SG, Zhang LJ, Li ZG (2018) Prevalence, risk factors, and prognosis of interstitial lung disease in a large cohort of Chinese primary Sjögren syndrome patients: a case-control study. Medicine (Baltimore) 97(24):e11003. https://doi.org/10.1097/MD.0000000000011003 CrossRef

35.

Roca F, Dominique S, Schmidt J, Smail A, Duhaut P, Lévesque H, Marie I (2017) Interstitial lung disease in primary Sjogren’s syndrome. Autoimmun Rev 16:48–54. https://doi.org/10.1016/j.autrev.2016.09.017 CrossRefPubMed

36.

Chen MH, Chou HP, Lai CC, Chen YD, Chen MH, Lin HY, Huang DF (2014) Lung involvement in primary Sjogren’s syndrome: correlation between high-resolution computed tomography score and mortality. J Chin Med Assoc 77:75–82. https://doi.org/10.1016/j.jcma.2013.11.001 CrossRefPubMed

37.

Rubio-Rivas M, Royo C, Simeón CP, Corbella X, Fonollosa V (2014) Mortality and survival in systemic sclerosis: systematic review and meta-analysis. Semin Arthritis Rheum 44(2):208–219. https://doi.org/10.1016/j.semarthrit.2014.05.010 CrossRefPubMed

38.

Hyldgaard C, Hilberg O, Pedersen AB, Ulrichsen SP, Løkke A, Bendstrup E, Ellingsen T (2017) A population-based cohort study of rheumatoid arthritis-associated interstitial lung disease: comorbidity and mortality. Ann Rheum Dis 76(10):1700–1706. https://doi.org/10.1136/annrheumdis-2017-211138 CrossRefPubMed

39.

Lazarus MN, Robinson D, Mak V, Moller H, Isenberg DA (2006) Incidence of cancer in a cohort of patients with primary Sjogren’s syndrome. Rheumatology (Oxford) 45:1012–1015CrossRef

40.

Theander E, Henriksson G, Ljungberg O, Mandl T, Manthorpe R, Jacobsson LTH (2006) Lymphoma and other malignancies in primary Sjogren’s syndrome: a cohort study on cancer incidence and lymphoma predictors. Ann Rheum Dis 65:796–803CrossRef

41.

Kassan SS, Thomas TL, Moutsopoulos HM, Hoover R, Kimberly RP, Budman DR, Costa J, Decker JL, Chused TM (1978) Increased risk of lymphoma in sicca syndrome. Ann Intern Med 89(6):888–892CrossRef

42.

Liang Y, Yang Z, Qin B, Zhong R (2014) Primary Sjogren’s syndrome and malignancy risk: a systematic review and meta-analysis. Ann Rheum Dis 73(6):1151–1156. https://doi.org/10.1136/annrheumdis-2013-203305 CrossRefPubMed

43.

Flores-Chávez A, Kostov B, Solans R, Fraile G, Maure B, Feijoo-Massó C, Rascón FJ, Pérez-Alvarez R, Zamora-Pasadas M, García-Pérez A, Lopez-Dupla M, Duarte-Millán MÁ, Ripoll M, Fonseca-Aizpuru E, Guisado-Vasco P, Pinilla B, dela Red G, Chamorro AJ, Morcillo C, Fanlo P, Soto-Cárdenas MJ, Retamozo S, Ramos-Casals M, Brito-Zerón P, GEAS-SS SEMI Registry (2018) Severe, life-threatening phenotype of primary Sjögren’s syndrome: clinical characterisation and outcomes in 1580 patients (GEAS-SS Registry). Clin Exp Rheumatol 36 Suppl 112(3):121–129PubMed

44.

Teh CL, Wan SA, Ling GR (2018) Severe infections in systemic lupus erythematosus: disease pattern and predictors of infection-related mortality. Clin Rheumatol 37(8):2081–2086. https://doi.org/10.1007/s10067-018-4102-6 CrossRefPubMed

Title: Survival analysis of patients with Sjögren’s syndrome in Turkey: a tertiary hospital-based study
Authors: Veli Yazisiz
Mesut Göçer
Funda Erbasan
İsmail Uçar
Bengisu Aslan
Şuayp Oygen
Edip Gökalp Gök
Mustafa Ender Terzioğlu
Publication date: 01-01-2020
Publisher: Springer London
Keyword: Antimalaria
Published in: Clinical Rheumatology / Issue 1/2020
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI: https://doi.org/10.1007/s10067-019-04744-6

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

STEP AAG HeroTeaserCollection image/© Tarek / Generated with AI / Stock.adobe.com, ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

At a glance: The STEP trials

Springer Medicine

Abstract

Objectives

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2020

Malnutrition, associated clinical factors, and depression in systemic sclerosis: a cross-sectional study

The important role of central sensitization in chronic musculoskeletal pain seen in different rheumatic diseases

Assessment of adherence to disease-modifying anti-rheumatic drugs in rheumatoid arthritis

Effectiveness and safety of abatacept for the treatment of patients with primary Sjögren’s syndrome

The predictive role of lung ultrasound in progression of scleroderma interstitial lung disease

Clinical and laboratory features of African-Brazilian patients with systemic sclerosis

Highlights from the ACC 2024 Congress

ACC 2024 Congress Coverage