Incidence of neoplasms in the most prevalent autoimmune rheumatic diseases: a systematic review

Machado, Roberta Ismael Lacerda; Braz, Alessandra de Sousa; Freire, Eutilia Andrade Medeiros

doi:10.1016/j.rbr.2014.03.008

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Review Article • Rev. Bras. Reumatol. 54 (2) • Mar-Apr 2014 • https://doi.org/10.1016/j.rbr.2014.03.008 copy

Incidence of neoplasms in the most prevalent autoimmune rheumatic diseases: a systematic review^☆ ☆ Study conducted at Universidade Federal da Paraíba (UFPB), João Pessoa, PB, Brazil.

Authorship SCIMAGO INSTITUTIONS RANKINGS

This article is a systematic review of the literature about the coexistence of cancer and autoimmune rheumatic diseases, their main associations, cancers and possible risk factors associated, with emphasis on existing population-based studies, besides checking the relation of this occur with the use of the drugs used in the treatment of autoimmune diseases. A search was conducted of scientific articles indexed in the Cochrane / BVS, Pubmed / Medline and Scielo / Lilacs in the period from 2002 to 2012. Also consulted was the IB-ICT (Brazilian digital library of theses and Masters), with descriptors in Portuguese and English for "Systemic sclerosis", "Rheumatoid Arthritis", " Systemic Lupus Erythematosus" and "Sjögren's syndrome", correlating each one with the descriptor AND "neoplasms". The results showed that in the database IBICT a thesis and a dissertation for the descriptor SLE met the inclusion criteria, none met RA one thesis to SS. Lilacs in the database/Scielo found two articles on "Rheumatoid Arthritis" AND "neoplasms". In Pubmed/Medline the inicial search resulted in 118 articles, and 41 were selected. The review noted the relationship between cancer and autoimmune rheumatic diseases, as well as a risk factor for protection, although the pathophysiological mechanisms are not known.

Neoplasm; Systemic lupus erythematosus; Sjögren's syndrome; Rheumatoid arthritis; Systemic sclerosis

Autoimmune disease	Standardized incidence ratio (SIR)/Confidence interval (CI) of 95%/References
Systemic lupus erythematosus
General risk	1.25¹⁹19. Tarr T, Gyorfy B, Szekanecz E, Bhattoa HP, Zeher M, Szegedi G, et al. Occurrence of malignancies in Hungarian patients with systemic lupus erythematosus: results from a single center. Ann N Y Acad Sci. 2007;1108:76-82. / 1.15²³23. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006;54:2550-7./1.14²¹21. Parikh-Patel A, White RH, Allen M, Cress R. Cancer risk in a cohort of patients with systemic lupus erythematosus (SLE) in California. Cancer Causes Control. 2008;19:887-94.
Blood cancer	2.75²³23. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006;54:2550-7.
Non-Hodkgin's lymphoma	2.86¹⁹19. Tarr T, Gyorfy B, Szekanecz E, Bhattoa HP, Zeher M, Szegedi G, et al. Occurrence of malignancies in Hungarian patients with systemic lupus erythematosus: results from a single center. Ann N Y Acad Sci. 2007;1108:76-82./ 3.64²³23. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006;54:2550-7.
Lung cancer	1.73¹⁹19. Tarr T, Gyorfy B, Szekanecz E, Bhattoa HP, Zeher M, Szegedi G, et al. Occurrence of malignancies in Hungarian patients with systemic lupus erythematosus: results from a single center. Ann N Y Acad Sci. 2007;1108:76-82. /1.37²³23. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006;54:2550-7.
Hepatobiliary cancer	2.6²³23. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006;54:2550-7./ 2.7²¹21. Parikh-Patel A, White RH, Allen M, Cress R. Cancer risk in a cohort of patients with systemic lupus erythematosus (SLE) in California. Cancer Causes Control. 2008;19:887-94.
Vulvovaginal cancer	3.27²¹21. Parikh-Patel A, White RH, Allen M, Cress R. Cancer risk in a cohort of patients with systemic lupus erythematosus (SLE) in California. Cancer Causes Control. 2008;19:887-94.
Prostate cancer	0.72²²22. Bernatsky S, Ramsey-Goldman R, Gordon C, Clarke AE. Prostate cancer in systemic lupus erythematosus. Int J Cancer. 2011;129:2966-9.
Sjogren's syndrome
Overall risk	3.25²⁷27. Zhang W, Feng S, Yan S, Zhao Y, Li M, Sun J, et al. Incidence of malignancy in primary Sjogren's syndrome in a Chinese cohort. Rheumatology (Oxford). 2010;49:571-7.
Non lymphoid overall risk	1.5²⁶26. Lazarus MN, Robinson D, Mak V, Moller H, Isenberg DA. Incidence of cancer in a cohort of patients with primary Sjogren's syndrome. Rheumatology (Oxford). 2006;45:1012-15.
Lymphoma	37.5²⁶26. Lazarus MN, Robinson D, Mak V, Moller H, Isenberg DA. Incidence of cancer in a cohort of patients with primary Sjogren's syndrome. Rheumatology (Oxford). 2006;45:1012-15. / 48.1²⁷27. Zhang W, Feng S, Yan S, Zhao Y, Li M, Sun J, et al. Incidence of malignancy in primary Sjogren's syndrome in a Chinese cohort. Rheumatology (Oxford). 2010;49:571-7.
Systemic sclerosis
Overall risk	1.5³³33. Olesen AB, Svaerke C, Farkas DK, Sorensen HT. Systemic sclerosis and the risk of cancer: A nationwide populationbased cohort study. Br J Dermatol. 2010;163:800-6.
Lung cancer	1.6³³33. Olesen AB, Svaerke C, Farkas DK, Sorensen HT. Systemic sclerosis and the risk of cancer: A nationwide populationbased cohort study. Br J Dermatol. 2010;163:800-6.
Blood cancer	2.5³³33. Olesen AB, Svaerke C, Farkas DK, Sorensen HT. Systemic sclerosis and the risk of cancer: A nationwide populationbased cohort study. Br J Dermatol. 2010;163:800-6.
Rheumatoid arthritis
Overall risk	1.05⁴¹41. Smitten AL, Simon TA, Hochberg MC, Suissa S. A metaanalysis of the incidence of malignancy in adult patients with rheumatoid arthritis. Arthritis Res Ther. 2008;10:R45.
Blood cancer	2.74²⁷27. Zhang W, Feng S, Yan S, Zhao Y, Li M, Sun J, et al. Incidence of malignancy in primary Sjogren's syndrome in a Chinese cohort. Rheumatology (Oxford). 2010;49:571-7.
Non-Hodgkin's lymphoma	3.54²⁷27. Zhang W, Feng S, Yan S, Zhao Y, Li M, Sun J, et al. Incidence of malignancy in primary Sjogren's syndrome in a Chinese cohort. Rheumatology (Oxford). 2010;49:571-7.
Lung cancer	1.63⁴¹41. Smitten AL, Simon TA, Hochberg MC, Suissa S. A metaanalysis of the incidence of malignancy in adult patients with rheumatoid arthritis. Arthritis Res Ther. 2008;10:R45.
Colorectal cancer	0.77⁴¹41. Smitten AL, Simon TA, Hochberg MC, Suissa S. A metaanalysis of the incidence of malignancy in adult patients with rheumatoid arthritis. Arthritis Res Ther. 2008;10:R45.
Breast cancer	0.84⁴¹41. Smitten AL, Simon TA, Hochberg MC, Suissa S. A metaanalysis of the incidence of malignancy in adult patients with rheumatoid arthritis. Arthritis Res Ther. 2008;10:R45.

Authors/year	Population basis/year of research	Observation
Bjornadal et al., 2002²⁰20. Bjornadal L, Lofstrom B, Yin L, Lundberg IE, Ekbom A. Increased cancer incidence in a Swedish cohort of patients with systemic lupus erythematosus. Scand J Rheumatol. 2002;31:66-71.	5.715 LES patients; Sweden (1964-1995)	443 cases of neoplasia
Bernatsky et al., 2006²³23. Bernatsky S, Boivin JF, Joseph L, Manzi S, Ginzler E, Gladman DD, et al. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006;54:2550-7.	9.547 LES patients; international multicentric (1970-2001)	431 cases of neoplasia observed; 114 deaths
Parikh-Patel et al., 2008²¹21. Parikh-Patel A, White RH, Allen M, Cress R. Cancer risk in a cohort of patients with systemic lupus erythematosus (SLE) in California. Cancer Causes Control. 2008;19:887-94.	30.478 LES patients; USA (1991-2002)	1.273 cases of neoplasia
Bernatsky et al., 2011²²22. Bernatsky S, Ramsey-Goldman R, Gordon C, Clarke AE. Prostate cancer in systemic lupus erythematosus. Int J Cancer. 2011;129:2966-9.	6.068 men with LES; follow- up for 6.3 years; Canada	Prostate cancer considered as a protective factor
Lazarus et al., 2006²⁶26. Lazarus MN, Robinson D, Mak V, Moller H, Isenberg DA. Incidence of cancer in a cohort of patients with primary Sjogren's syndrome. Rheumatology (Oxford). 2006;45:1012-15.	112 patients with SS; London (1979-2006)	25 cases of neoplasia
Zhang et al., 2010²⁷27. Zhang W, Feng S, Yan S, Zhao Y, Li M, Sun J, et al. Incidence of malignancy in primary Sjogren's syndrome in a Chinese cohort. Rheumatology (Oxford). 2010;49:571-7.	1.320 patients with SS; Peking (1990-2005)	Follow-up for 4.4 years: 29 cases of neoplasia
Olesen et al., 2010³³33. Olesen AB, Svaerke C, Farkas DK, Sorensen HT. Systemic sclerosis and the risk of cancer: A nationwide populationbased cohort study. Br J Dermatol. 2010;163:800-6.	2.040 patients with SSc; Denmark (1977-2006)	Follow-up for 6.4 years: 222 cases of neoplasia.
Chen et al., 2011³⁷37. Chen YJ, Chang YT, Wang CB, Wu CY. The risk of cancer in patients with rheumatoid arthritis: A nationwide cohort study in Taiwan. Arthritis Rheum. 2011;63:352-8.	23.644 patients with RA; Taiwan (1996-2007)	935 cases of cancer

Drug	Pathogenic paths
Methotrexate.⁴²42. Bologna C, Picot MC, Jorgensen C, Viu P, Verdier R, Sany J. Study of eight cases of cancer in 426 rheumatoid arthritis patients treated with methotrexate. Ann Rheum Dis. 1997;56:97-102.	Antagonizes dihydrofolate reductase, inhibits DNA synthesis and proliferation of B and T cells
	Exhibits no increased risk⁴²42. Bologna C, Picot MC, Jorgensen C, Viu P, Verdier R, Sany J. Study of eight cases of cancer in 426 rheumatoid arthritis patients treated with methotrexate. Ann Rheum Dis. 1997;56:97-102.
Azathioprine⁴³43. Sobral FRS. Proposta de guia para a realização de estudos não clínicos de segurança, necessários ao desenvolvimento de medicamentos antineoplásicos. 2006. [Dissertação de Mestrado na área de Vigilância Sanitária]. Brasília (DF): Universidade Federal da Bahia; 2006.^,⁴⁶46. Almeida VL, Leitão A, Reina LDCB, Montanari CA, Donnici CL. Câncer e agentes antineoplásicos ciclo-celular específicos e ciclo-celular não específicos que interagem com o DNA: uma introdução. Quim Nova. 2005;28:118-29.	Inhibits the biosynthesis of adenine and guanine, interfering with cell multiplication
	Inactivate body immunosurveillance.
	Possible increased risk of lymphoproliferative disorders⁴³43. Sobral FRS. Proposta de guia para a realização de estudos não clínicos de segurança, necessários ao desenvolvimento de medicamentos antineoplásicos. 2006. [Dissertação de Mestrado na área de Vigilância Sanitária]. Brasília (DF): Universidade Federal da Bahia; 2006.^,⁴⁶46. Almeida VL, Leitão A, Reina LDCB, Montanari CA, Donnici CL. Câncer e agentes antineoplásicos ciclo-celular específicos e ciclo-celular não específicos que interagem com o DNA: uma introdução. Quim Nova. 2005;28:118-29.
Cyclophosphamide⁴³43. Sobral FRS. Proposta de guia para a realização de estudos não clínicos de segurança, necessários ao desenvolvimento de medicamentos antineoplásicos. 2006. [Dissertação de Mestrado na área de Vigilância Sanitária]. Brasília (DF): Universidade Federal da Bahia; 2006.^,⁴⁶46. Almeida VL, Leitão A, Reina LDCB, Montanari CA, Donnici CL. Câncer e agentes antineoplásicos ciclo-celular específicos e ciclo-celular não específicos que interagem com o DNA: uma introdução. Quim Nova. 2005;28:118-29. 47. Silva HRM, Borges AC, Pizza M, Borsato ML, Castro HC; Luporini SM, BP. Osteossarcoma e leucemia mieloide aguda - dois casos em crianças. Rev Bras Hematol Hemoter. 2006;28:76.^-⁴⁸48. Ognenovski VM, Marder W, Somers EC, Johnston CM, Farrehi JG, Selvaggi SM, et al. Increased incidence of cervical intraepithelial neoplasia in women with systemic lupus erythematosus treated with intravenous cyclophosphamide. J Rheumatol. 2004; 31:1763-67.	Crosslinkage with DNA strands prevent replication
	Increased risk of cervical intraepithelial neoplasm⁴⁸48. Ognenovski VM, Marder W, Somers EC, Johnston CM, Farrehi JG, Selvaggi SM, et al. Increased incidence of cervical intraepithelial neoplasia in women with systemic lupus erythematosus treated with intravenous cyclophosphamide. J Rheumatol. 2004; 31:1763-67.
Biological agents⁵⁰50. Solomon DH, Mercer E, Kavanaugh A. Observational studies on the risk of cancer associated with tumor necrosis factor inhibitors in rheumatoid arthritis: A review of their methodologies and results. Arthritis Rheum. 2012;64:21-32. 51. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: Systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006;295:2275-85. 52. Smith PC, Keller ET. Anti-interleukin-6 monoclonal antibody induces regression of human prostate cancer xenografts in nude mice. Prostate. 2001;48:47-53. 53. Simon TA, Smitten AL, Franklin J, Askling J, Lacaille D, Wolfe F, et al. Malignancies in the rheumatoid arthritis abatacept clinical development programme: An epidemiological assessment. Ann Rheum Dis. 2009;68:1819-26.^-⁵⁴54. Genovese M C, Hochberg MC, Cohen RB, Weinblatt ME, Kaine J, Keystone E, et al. Prolonged exposure to subcutaneous and intravenous abatacept in patients with rheumatoid arthritis does not affect rates of infection, malignancy and autoimmune events: Results from pooled clinical trial data. Congresso Americano de Reumatologia; 9-13/11/2012; Washington - DC. Arthritis Rheum. 2012;64:1695, S725.	Immunomodulation
	Infliximab and adalimumab with an increased risk of cancer, especially lymphoma and rectal, breast and lung cancer⁵¹51. Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: Systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006;295:2275-85.
	Abatacept: no increased risk of malignancies was found⁵³53. Simon TA, Smitten AL, Franklin J, Askling J, Lacaille D, Wolfe F, et al. Malignancies in the rheumatoid arthritis abatacept clinical development programme: An epidemiological assessment. Ann Rheum Dis. 2009;68:1819-26.^,⁵⁴54. Genovese M C, Hochberg MC, Cohen RB, Weinblatt ME, Kaine J, Keystone E, et al. Prolonged exposure to subcutaneous and intravenous abatacept in patients with rheumatoid arthritis does not affect rates of infection, malignancy and autoimmune events: Results from pooled clinical trial data. Congresso Americano de Reumatologia; 9-13/11/2012; Washington - DC. Arthritis Rheum. 2012;64:1695, S725.

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[1] Corresponding author. E-mail: alessabraz@gmail.com (A.S. Braz).

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Incidence of neoplasms in the most prevalent autoimmune rheumatic diseases: a systematic review☆ ☆ Study conducted at Universidade Federal da Paraíba (UFPB), João Pessoa, PB, Brazil.

Incidence of neoplasms in the most prevalent autoimmune rheumatic diseases: a systematic review^☆ ☆ Study conducted at Universidade Federal da Paraíba (UFPB), João Pessoa, PB, Brazil.