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The Risks of Cancer Development in Systemic Lupus Erythematosus

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The Risks of Cancer Development in Systemic Lupus Erythematosus Song et al. Arthritis Research & Therapy (2018) 20:270 https://doi.org/10.1186/s13075-018-1760-3 RESEARCH ARTICLE Open Access The risks of cancer development in systemic lupus erythematosus (SLE) patients: a systematic review and meta- analysis Lebin Song1†, Yi Wang2†, Jiayi Zhang2†, Ninghong Song2, Xiaoyun Xu1* and Yan Lu1* Abstract Background: Although accumulating data have suggested the development of cancer in systemic lupus erythematosus (SLE) patients, these results remain inconsistent. To examine such a putative association, this analysis reports the association between SLE and the risks of 24 cancer types. Methods: Online databases PubMed, EMBASE, and Web of Science were searched comprehensively for eligible studies, published up to 15 May 2018. Pooled standardized incidence rates (SIRs) with 95% confidence intervals (CIs) were utilized to reveal their associations. Results: A total of 24 eligible studies were ultimately enrolled. Our results indicated that SLE was associated with increased risk of overall cancers, cancer risk in both genders, non-Hodgkin’s lymphoma, Hodgkin’s lymphoma, leukemia, multiple myeloma, cervix, vagina/vulva, renal, bladder, esophagus, gastric, hepatobiliary, lung, oropharynx, larynx, non-melanoma skin, and thyroid cancers. Additionally, SLE could reduce the risk of prostate cancer and cutaneous melanoma; however, it was not significantly associated with breast, uterus, ovarian, pancreatic, colorectal, or brain cancers. Conclusions: Our results shed light SLE being correlated with increased risk for 16 involved cancers and decreased risk for prostate cancer and cutaneous melanoma. This comprehensive meta-analysis provides epidemiological evidence supporting the associations between SLE and cancer risk. This evidence could be utilized to drive public policies and to help guide personalized medicine to better manage SLE and reduce associated cancer morbidity and mortality. Keywords: Systemic lupus erythematosus, Cancer, Meta-analysis Background people with a female to male ratio of 10:1 [2], and the Systemic lupus erythematosus (SLE), defined as a com- kidneys and the skin are the most intensively affected or- plex and chronic inflammatory autoimmune disease, is gans [3, 4]. Regarding the incidence and prevalence of characterized by the production of autoantibodies, com- SLE, the highest estimates of disease are in North Amer- plement activation, and immune complex deposition, ica and in people of African ethnicity [5]. Major causes which can be directed against almost any organ system of morbidity and mortality in SLE patients include infec- in a heterogeneous array of clinical manifestations [1]. tion, cancer, renal failure, myocardial infarction, and SLE predominantly occurs in young and middle-aged central nervous system disease [6–9]. Due to early me- ticulous diagnosis and the progress of treatment, survival rates for SLE patients have increased remarkably in re- * Correspondence: [email protected]; [email protected] † cent decades. Despite their increased life expectancy, Lebin Song, Yi Wang and Jiayi Zhang contributed equally to this work. 1Department of Dermatology, The First Affiliated Hospital of Nanjing Medical these patients still have two- to five-times the risk of University, No. 300 Guangzhou Road, Nanjing 210029, China Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Song et al. Arthritis Research & Therapy (2018) 20:270 Page 2 of 13 Table 1 Main characteristics of individual studies included in this meta-analysis First author Year Data origin Calendar No.of SLE patients SLE Follow-up NOS period (gender) diagnosis scores Tallbacka [14] 2018 The Helsinki University 1967–1987 205 (182 females and ARA 25.7 years 7 Central Hospital 23 males) criteria Yun [11] 2017 National Health Insurance 2009–2013 17,495 (15,826 females and NA NA 8 System database 1669 males) Azrielant [13] 2017 Clalit Health Services 2013 5018 (all males) NA NA 6 Yu [21] 2016 The Taiwan National 1997–2010 15,623 (13,693 females and ACR 124,832.45 person- 8 Health Insurance Research 1930 males) criteria years Database (NHIRD) Waseem [22] 2015 2006 Medicare claims data 2006 18,423 (all females) NA NA 8 Bernatsky [24] 2013 Multi-center 1958–2009 16,409 (90% females) ACR 7.4 years/121,283 years 8 criteria Dey [23] 2013 The University College 1978–2010 595 ACR 14.7 years/8910.51 6 London Hospitals Lupus Clinic criteria person-years Hemminki [25] 2012 Swedish Hospital Discharge 1964–1986 7624 NA 11.9 years/86,640 8 Register person-years Dreyer [26] 2011 Central Population Register 1951–2006 576 (508 females and ACR 13.2 years/7803 years 7 68 males) criteria Kang [27] 2010 Kangnam St. Mary’s Hospital 1997–2007 914 (all females) ACR 5716 person-years 8 criteria Chen [15] 2010 National Health Insurance 1996–2007 11,763 (10,394 females and ARA 6.1 years 5 Research Database 1369 males) criteria Gadalla [28] 2009 Surveillance, Epidemiology 1993–2002 340 NA NA 8 and End Results-Medicare-linked database Parikh-Patel [29] 2008 Statewide patient discharge 1991–2002 30,478 (27,133 females and NA 5.1 years/157,969 years 6 data 3345 males) Tunde [30] 2007 A single center 1970–2004 860 (771 female and ACR 13.4 years 8 89 male) criteria Bernatsky [31] 2005 Multi-center 1958–2000 9547 (8607 females and 940 ACR 8.0 years/76,948 7 males) criteria person-years Ragnarsson [32] 2003 Icelandic SLE database 1957–2001 238 (213 females and ARA 12.8 years/2774 years 8 25 males) criteria Bjornadal [33] 2002 Swedish National Board 1964–1995 5715 (4201 females and 1514 NA 50,246 person-years 8 of Health and Welfare males) recorded data Cibere [34] 2001 University-based Rheumatic 1975–1994 297 (84% females) ACR 12 years 7 Disease UniT criteria Sultan [35] 2000 Board of Health and 1978–1999 276 (93.5% females) ARA 4.8 years/1695 years 7 Welfare recorded data criteria Ramsey- 1998 NA NA 616 NA NA 5 Goldman [36] Mellemkjaer [37] 1997 Nationwide Danish Hospital 1977–1989 1585 (1308 females and 277 ACR 6.8 years/10,807 6 Discharge Register males) criteria personyears Abu-Shakra [38] 1996 The University of Toronto NA 724 (627 females and ACR 7233 person-years 6 Lupus Clinic Database 97 males) criteria Sweeney [39] 1995 NA NA 219 NA NA 5 Pettersson [40] 1992 Fourth Department of 1967–1987 205 (182 females and ARA 2340 person-years 5 Medicine, Helsinki University 23 males) criteria Central Hospital SLE systemic lupus erythematosus, ACR criteria American College of Rheumatology criteria, ARA criteria American Rheumatism Association criteria, NA not available. Song et al. Arthritis Research & Therapy (2018) 20:270 Page 3 of 13 death compared with the general population, not only follow-up, Tallbacka et al. confirmed that patients with for all-cause mortality but also for mortality from cancer SLE had an increased risk of cancer, particularly [10]. As a result, more attention should be paid to the non-Hodgkin’s lymphoma and kidney cancer [14]. More- risks of cancer development in patients with SLE. over, Chen et al. reported a decreased risk of prostate Until now, a growing amount of research has cancer and bladder cancer in a cohort of 11,763 lupus attempted to reveal the incidence of cancers in SLE pa- patients in Taiwan [15]. There are also several studies tients, and several studies have successfully demon- suggesting that no direct associations exist between par- strated that SLE is significantly associated with increased ticular cancers and SLE. For instance, Rezaieyazdi et al. risks of thyroid cancer [11], cervix cancer [12], and suggested that SLE was not dramatically related with the hematologic cancer [13]. With more than 25 years of risk of breast cancer [16]. However, their results were Table 2 Meta-analysis results for included studies of the relationship between SLE and risks of various cancers Variables NO.of studies Effects model SIR (95%CI) I-squared (%) P values Relationship Publication bias Overall characteristics Overall cancers 10 Random 1.28 (1.16–1.42) 71.9% <0.001 Increased risks None Female 4 Random 1.49 (1.15–1.93) 72.7% 0.012 Increased risks None Male 5 Random 1.59 (1.18–2.14) 78.8% 0.001 Increased risks None SLE associated with Lymphatic and haematopoietic cancers Non-Hodgkin’s lymphoma 11 Random 4.93 (3.81–6.36) 55.2% 0.014 Increased risks None Hodgkin’s lymphoma 8 Fixed 2.60 (2.14–3.17) 0.0% 0.660 Increased risks Existence Leukemia 10 Fixed 2.01 (1.64–2.47) 24.3% 0.220 Increased risks None Multiple myeloma 4 Fixed 1.48 (1.02–2.14) 0.0% 0.744 Increased risks None SLE associated with Reproductive cancers Breast cancer 19 Random 0.89 (0.77–1.04) 70.1% < 0.001 No association None Uterus cancer 6 Random 0.70 (0.46–1.07) 58.3% 0.035 No association None Cervix cancer 11 Fixed 1.56 (1.29–1.88) 4.1% 0.404 Increased risks None Ovarian cancer 11 Fixed 0.92 (0.74–1.33) 14.2% 0.309 No association None Vagina/vulva cancer 8 Fixed 3.48 (2.69–4.50) 0.0% 0.813 Increased risks None SLE associated with Urinary cancers
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