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

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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.

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References

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  3. 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 26:1296–1300

    CAS  PubMed  Google Scholar 

  4. 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):1262–1269

    Article  Google Scholar 

  5. 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 39:297–303

    Article  CAS  Google Scholar 

  6. 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):296–304

    Article  CAS  Google Scholar 

  7. 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 46:741–747

    Article  Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  11. Voulgarelis M, Tzioufas AG, Moutsopoulos HM (2008) Mortality in Sjögren’s syndrome. Clin Exp Rheumatol 26(5 Suppl 51):S66–S71

    CAS  PubMed  Google Scholar 

  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) 38:245–243

    Article  CAS  Google Scholar 

  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 60:467–472

    Article  CAS  Google Scholar 

  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) 45:187–191

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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) 49:571–577

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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):475–487

    Article  CAS  Google Scholar 

  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 63:2021–2030

    Article  Google Scholar 

  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 165:277–304

    Article  Google Scholar 

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

    Book  Google Scholar 

  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 24:2376–2380

    CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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 171:632–638

    Article  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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) 45:1012–1015

    Article  CAS  Google Scholar 

  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 65:796–803

    Article  CAS  Google Scholar 

  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):888–892

    Article  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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):121–129

    PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study is supported by Akdeniz University Scientific Research Projects Unit.

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Authors and Affiliations

  1. Department of Internal Medicine, Division of Rheumatology, Akdeniz Üniversitesi Hastanesi, Konyaaltı, Antalya, Turkey

    Veli Yazisiz, Funda Erbasan, İsmail Uçar, Bengisu Aslan, Şuayp Oygen, Edip Gökalp Gök & Mustafa Ender Terzioğlu

  2. Department of Internal Medicine, Division of Hematology, Antalya Education and Research Hospital, Antalya, Turkey

    Mesut Göçer

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  1. Veli Yazisiz
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  2. Mesut Göçer
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Contributions

VY contributed to conception and design of the study, analysis and interpretation of data, and drafting the manuscript; MG, İU, BA, ŞO, EG and FE collected data and reviewed the literature; ET was responsible for the revision of the manuscript for important intellectual content; all authors issued approval for the final version to be submitted.

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Correspondence to Veli Yazisiz.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the World Medical Association Helsinki Declaration 2018 and its later amendments or comparable ethical standards. The study was approved by the Ethics Committee of Akdeniz University School of Medicine (Approval number:2019-534).

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Yazisiz, V., Göçer, M., Erbasan, F. et al. Survival analysis of patients with Sjögren’s syndrome in Turkey: a tertiary hospital-based study. Clin Rheumatol 39, 233–241 (2020). https://doi.org/10.1007/s10067-019-04744-6

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