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Table of Contents
Vol. 85, No. 4, 2013
Issue release date: November 2013
Section title: Clinical Study
Free Access
Oncology 2013;85:235-240
(DOI:10.1159/000350165)

Non-Lymphoma Hematological Malignancies in Systemic Lupus Erythematosus

Lu M.a · Bernatsky S.a · Ramsey-Goldman R.e · Petri M.f · Manzi S.g · Urowitz M.B.b · Gladman D.b · Fortin P.R.c · Ginzler E.M.h · Yelin E.i · Bae S.-C.n · Wallace D.J.k · Jacobsen S.p · Dooley M.A.l · Peschken C.A.d · Alarcón G.S.m · Nived O.o · Gottesman L.h · Criswell L.A.j · Sturfelt G.o · Dreyer L.p · Lee J.L.a · Clarke A.E.a
aDivision of Clinical Epidemiology, McGill University Health Centre, Montreal, Que., bDepartment of Rheumatology, Toronto Western Hospital, Toronto, Ont., cDivision of Rheumatology, CHU de Québec and Université Laval, Quebec City, Que., and dDepartment of Rheumatology, University of Manitoba, Winnipeg, Man., Canada; eDepartment of Medicine/Rheumatology, Northwestern University Feinberg School of Medicine, Chicago, Ill., fDivision of Rheumatology, Johns Hopkins University School of Medicine, Baltimore, Md., gDepartment of Medicine, West Penn Allegheny Health System, Pittsburgh, Pa., hDivision of Rheumatology, Downstate Medical Center, State University of New York, Brooklyn, N.Y., iDivision of Rheumatology and jRosalind Russell Medical Research Center for Arthritis, Department of Medicine, University of California San Francisco, San Francisco, Calif., kCedars-Sinai Medical Center/David Geffen School of Medicine, University of California Los Angeles, Los Angeles, Calif., lDepartment of Rheumatology, University of North Carolina at Chapel Hill, Chapel Hill, N.C., mDepartment of Rheumatology, The University of Alabama, Birmingham, Ala., USA; nThe Hospital for Rheumatic Diseases, Hanyang University, Seoul, Korea; oDepartment of Rheumatology, Lund University Hospital, Lund, Sweden; pDepartment of Rheumatology, Rigshospitalet and Gentofte Hospital, Copenhagen University Hospital, Copenhagen, Denmark
email Corresponding Author

Abstract

Objective: To describe non-lymphoma hematological malignancies in systemic lupus erythematosus (SLE). Methods: A large SLE cohort was linked to cancer registries. We examined the types of non-lymphoma hematological cancers. Results: In 16,409 patients, 115 hematological cancers [including myelodysplastic syndrome (MDS)] occurred. Among these, 33 were non-lymphoma. Of the 33 non-lymphoma cases, 13 were of lymphoid lineage: multiple myeloma (n = 5), plasmacytoma (n = 3), B cell chronic lymphocytic leukemia (B-CLL; n = 3), precursor cell lymphoblastic leukemia (n = 1) and unspecified lymphoid leukemia (n = 1). The remaining 20 cases were of myeloid lineage: MDS (n = 7), acute myeloid leukemia (AML; n = 7), chronic myeloid leukemia (CML; n = 2) and 4 unspecified leukemias. Most of these malignancies occurred in female Caucasians, except for plasma cell neoplasms (4/5 multiple myeloma and 1/3 plasmacytoma cases occurred in blacks). Conclusions: In this large SLE cohort, the most common non-lymphoma hematological malignancies were myeloid types (MDS and AML). This is in contrast to the general population, where lymphoid types are 1.7 times more common than myeloid non-lymphoma hematological malignancies. Most (80%) multiple myeloma cases occurred in blacks; this requires further investigation.

© 2013 S. Karger AG, Basel


  

Key Words


  • Systemic lupus erythematosus
  • Malignancy
  • Cancer


 Introduction

Cancer risk in systemic lupus erythematosus (SLE) is a topic of increasing interest, but to date, much of the focus has been directed at lymphoma especially non-Hodgkin's lymphoma. Our purpose was to describe demographic factors and types of non-lymphoma hematological malignancies in a very large international, multisite SLE cohort.

 Methods

Our assessment was based on a very large international, multisite cohort drawn from 30 centers, each linked to regional tumor registries to ascertain malignancies. We published recently on the overall cancer experience in this cohort [1]. In this paper, we describe the types of non-lymphoma hematological cancers occurring after SLE diagnosis and examine the distribution of demographic characteristics, including sex, race/ethnicity, age and SLE duration at the time of cancer diagnosis. The centers from which these non-lymphoma hematological cancers in SLE occurred included Canada (Montreal, Toronto and Winnipeg), the USA (Chicago, Baltimore, Pittsburgh, Brooklyn, San Francisco, Los Angeles, Chapel Hill and Birmingham), Korea (Seoul), Denmark (Copenhagen) and Sweden (Lund).

The cohort was followed from the date of cohort entry (date first seen in the clinic with confirmed SLE) up to the earliest of: date last seen in the clinic, death or end of cancer registry information. Cancer registries generally require a period of at least 1 year to have elapsed before they can confirm that their cancer data are adequately complete and accurate, so the end of the observation interval for the SLE cohort of each center was based on the earliest of that date, or the last date the patient was seen in the clinic (or the date of death, if relevant).

Regional general population cancer rates were obtained and used to generate the expected number of hematological malignancies. The total of cancers observed in our cohort, divided by this expected number, provides the standardized incidence ratio (SIR), representing the relative risk of hematologic malignancy in SLE compared to an age and sex-matched general population.

 Results

Sixteen thousand four hundred and nine patients were observed for an average of 7.4 person-years. Of these, 90% were female and the majority was Caucasian [1]. In these patients, 115 hematological cancers occurred and, based on age-matched general population cancer rates, the standardized incidence ratio (SIR) for all hematological cancers after SLE onset was 2.9 in females [95% confidence interval (CI) 2.3-3.6] and 3.6 in males (95% CI 2.2-5.5). The SIR for hematological cancers for SLE patients of <40 years was 4.1 (95% CI 2.5-6.3) in comparison with SLE patients >60 years where the point estimate was SIR 2.3 (95% CI 1.7-3.1) [1].

We assessed that a total of 33 non-lymphoma hematological malignancies [including myelodysplastic syndrome (MDS)] had occurred in these patients. To provide some context, figure 1 gives an outline of the cells from which hematological malignancies arise.

FIG01
Fig. 1. Hematological malignancies by cell lineage. ALL = Acute lymphocytic leukemia; CLL = chronic lymphocytic leukemia.

For these 33 non-lymphoma hematological cancers, the mean age at cancer diagnosis was 54.3 years [standard deviation (SD) 15.2, median 55] and the mean SLE duration at the time of cancer diagnosis was 14 years (SD 8.2, median 14). Most, i.e. 30/33 patients were female (90.91%), reflecting the female predominance of the SLE cohort. With respect to race/ethnicity, 18 were Caucasian (54.6%), 12 were black (of African or Caribbean descent, 36.4%), 2 were Asian (6%) and 1 was First Nations (Canadian native).

Of these 33 non-lymphoma cases, 13 were of lymphoid lineage. This included multiple myeloma (n = 5), plasmacytomas (n = 3), B cell chronic lymphocytic leukemia (B-CLL; n = 3), precursor cell lymphoblastic leukemia (n = 1) and lymphoid leukemia not otherwise specified (n = 1). The remaining 20 cases were of myeloid lineage. These included MDS (n = 7), acute myeloid leukemia (AML; n = 7), chronic myeloid leukemia (CML; n = 2) and 4 leukemias not otherwise specified.

All of the non-lymphoma lymphoid hematological malignancies in SLE occurred in female Caucasians, except in the plasma cell neoplasms, where 4/5 multiple myeloma cases and 2/3 plasmacytoma cases were black (the others being Asian and Caucasian, respectively) (table 1). Regarding age, in B-CLL, the median age of SLE subjects at the time of onset was 65 (range 58-83) years. The median age at onset for this cancer in the female general population is 74 years [2]. At the time of multiple myeloma diagnosis in SLE, median age was 49 (range 45-57) years, while for the 3 plasmacytoma SLE cases, median age was 35 (range 25-62) years. In the female general population, the median age at time of diagnosis for multiple myeloma is 70 years [2], and 55 years for plasmacytomas [3].

TAB01
Table 1. Demographics of the SLE patients who developed non-lymphoma hematologic malignancies of the lymphoid line

Of 20 myeloid malignancies, 3 (15%) occurred in males, and 7 (35%) occurred in blacks (table 2). In female AML cases, the median age at AML diagnosis was 48 (range 34-72) years versus 66 years in the female general population. The 7 MDS cases (6 females) occurred at a median age of 48 (range 36 - 59) years versus 76 years in the general population [2]. The age at time of diagnosis for the 2 CML cases (1 female) were similar to the general population median (65 years).

TAB02
Table 2. Demographic characteristics of the SLE patients who developed myeloid malignancies

 Discussion

Most of the hematological malignancies that developed in our SLE cohort were female, which reflected the fact that 90% of SLE patient are female. In the general population, the risk of hematological cancers is significantly greater in males than females; for example, males have almost twice the risk for B-CLL. Our international cohort study included over 16,000 individuals and 10% of them were male. Given this, only 2-3 lymphoid malignancies would have been expected in our male SLE subjects. Thus while it may seem unusual that none of the non-lymphoma lymphoid malignancies were male, this may have just been a chance finding due to the low number of males with SLE, and the relative rarity of these cancers in general. Though our SIR point estimate for hematological cancers in males with SLE (SIR 3.6) was slightly higher than that for females (SIR 2.9), the CIs did overlap.

Five cases of multiple myeloma occurred in our SLE cohort. Although previous studies were unable to demonstrate that SLE patients have any increased risk for multiple myeloma [4,5], 1 large study did demonstrate that patients with a family history of SLE do indeed have an increased risk of developing multiple myeloma [4]. Furthermore, there is also an increased occurrence of SLE in first-degree relatives of people with multiple myeloma [6].We were somewhat surprised that most (80%) of these 5 multiple myeloma cases in our SLE cohort occurred in blacks. In the general population, black populations do have a 2-fold greater multiple myeloma prevalence when compared to Caucasian populations [2]. However, blacks were a minority in our cohort. In our recent review of case reports and case series in the literature, out of 20 SLE patients that developed multiple myeloma [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24], only 1 patient was black [22]. We are unable to explain the high proportion of multiple myeloma cases in blacks in our cohort.

A striking finding in our study was the young age at diagnosis for the majority of the neoplasms. Of course, given the relatively few number of cases, the results should be interpreted with caution. Still, with the exception of CML, median onset age for patients in this cohort was 10-20 years earlier than the general population median. While this, in part, reflects the young age of our cohort, it further emphasizes the increased risk of hematological malignancies in this population. The SIR for hematological cancers according to age suggests that it is indeed the youngest SLE patients who have the highest relative risk when comparing to age- and sex-matched general population rates.

The most common non-lymphoma hematological malignancies observed in our SLE cohort were myeloid types (MDS and AML). This is in contrast to the general population, where lymphoid types are 1.7 times more common than myeloid types, when lymphomas are excluded [2]. Our observation is similar to previous studies on myeloid malignancies and autoimmune conditions in the literature. A population-based case-control study of hematopoietic malignancies, using SEER-Medicare data of 13,486 myeloid malignancy patients and 160,086 population-based controls, found that SLE patients had an increased risk of both AML [odds ratio (OR) 1.92] and MDS (OR 1.82) [25]. Another article on a nested case-control study, using Swedish registers as well as published case reports of SLE and AML, concluded that not only do SLE patients have an increased risk of developing myeloid leukemia, but that this risk is actually restricted to a subset of patients with hematological aberrations such as prolonged leukopenia (OR 14) and to a lesser extent, thrombocytopenia (OR 3.3) [26]. Furthermore, this study demonstrated that 30.4% of their AML cases were preceded by MDS - a rate comparable to the general population [27].

A limitation of our study is that most of our participating centers did not provide information on clinical features, such as disease activity or drugs. We were therefore unable to look at these variables in the cases. Moreover, with only 9 myeloid leukemia cases (7 AML and 2 CML), we would have difficulty confirming any previously reported association of this malignancy with cytopenias.

 Conclusion

In summary, we described the demographics of those who developed hematological malignancies in our international cohort of 16,409 SLE patients. Myeloid malignancies such as MDS and AML were the most common; a finding which has been reported before but has not, to date, received much attention. Most of our non-lymphoma hematological malignancy cases were younger than the general population median age-of-onset, although this could simply reflect our cohort demographics. We were surprised by the very high predominance of black race/ethnicity among the SLE patients who developed multiple myeloma. This requires further investigation.

 Acknowledgments

We acknowledge the assistance of Elizabeth Turnbull. This research was made possible through the endorsement and support of the Systemic Lupus International Collaborating Clinics (SLICC) research network. This research was funded by CIHR/TAS grants RG06/092 and NIH grant 1R03CA128052-01. We also acknowledge the grant that supports the Chicago Lupus Database (NIH/NIAMS P60 2 AR30692) and the grants that support the UCSF Lupus Outcomes Study (NIH/NIAMS P60 AR053308 and NIH/NIAMS R01 5R01AR56476-9) and the grant that supports the Hopkins Lupus Cohort (NIH R01 AR43727). Support for the McGill University Health Centre cohort comes from Singer Family Fund for Lupus Research. L.A.C. would like to acknowledge support from the Alliance for Lupus Research and from a Kirkland Scholar Award. S.-C.B.'s work is supported by the Korea Healthcare technology R&D Project, Ministry for Health and Welfare, Republic of Korea (A120404). M.L. was supported by a research bursary from the Canadian Arthritis Network and the Arthritis Society.


References

  1. Bernatsky S, Clarke A, Petri MA, et al: Further defining cancer risk in systemic lupus: updated results in an expanded international multi-centre cohort. J Autoimmun 2013, in press.
  2. Howlader N, Noone AM, Krapcho M, et al (eds): SEER Cancer Statistics Review, 1975-2009 (Vintage 2009 Populations). Bethesda, National Cancer Institute, 2009.
  3. Knowling MA, Harwood AR, Bergsagel DE: Comparison of extramedullary plasmacytomas with solitary and multiple plasma cell tumors of bone. JCO 1983;1:255-262.

    External Resources

  4. Landgren O, Linet MS, McMaster ML, Gridley G, Hemminki K, Gold LR: Familial characteristics of autoimmune and hematologic disorders in 8,406 multiple myeloma patients: A population-based case-control study. Int J Cancer 2006;118:3095-3098.
  5. Anderson LA, Gadalla S, Morton LM, Landgren O, Pfeiffer R, Warren JL, Berndt SI, Ricker W, Parsons R, Engels EA: Population-based study of autoimmune conditions and the risk of specific lymphoid malignancies. Int J Cancer 2009;125:398-405.
  6. Linet MS, McLaughlin J, Harlow SD, Fraumeni JF: Family history of autoimmune disorders and cancer in multiple myeloma. Int J Epidemiology 1988;17:512-513.
  7. Canoso JJ, Cohen AS: Malignancy in a series of 70 patients with systemic lupus erythematosus. Arthritis Rheum 1974;17:383-390.
  8. Pehamberger H, Diem E, Konrad K: Systemic lupus erythematosus with multiple myeloma. Acta Derm Venereol 1978;58:527-530.

    External Resources

  9. Jordan E, Burnstein SL, Calabro JJ, Henderson ES: Multiple myeloma complicating the course of seronegative systemic lupus erythematosus. Arthritis Rheum 1978;21:260-265.
  10. Butler RC, Thomas SM, Thompson JM, Keat AC: Anaplastic myeloma in systemic lupus erythematosus. Ann Rheum Dis 1984;43:653-655.

    External Resources

  11. Solary E, Caillot D, Guy H, Olsson NO, Tanter Y, Chalopin JM: Systemic lupus erythematosus occurring in a patient with multiple myeloma. Arthritis Rheum 1986;29:933-934.
  12. Sendagorta E, Matarredona J, Brieva JA, Rodriguez ML, Ledo A: Systemic lupus erythematosus in association with smoldering multiple myeloma. J Am Acad Dermatol 1987;16:135-136.

    External Resources

  13. Umemura T, Hirai S, Ohashi M: Systemic lupus erythematosus with multiple myeloma. Nihon Hifuka Gakkai Zasshi 1988;98:1495-1503.

    External Resources

  14. Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 30-1995. A 69-year-old woman with lupus erythematosus and painful skin lesions of the feet. N Engl J Med 1995;333:862-868.
  15. Afeltra A, Amoroso A, Garzia P, Addessi MA, Pulsoni A, Bonomo L: Systemic lupus erythematosus and multiple myeloma: a rare association. Semin Arthritis Rheum 1997;26:845-849.
  16. Xu Y, Wiernik PH: Systemic lupus erythematosus and B cell hematologic neoplasm. Lupus 2001;10:841-850.
  17. Lee S, Lee S, Kim Y, Park M, Lee J, Kim H: A case of multiple myeloma in a patient with systemic lupus erythematosus. J Korean Rheum Association 2002:325-329.
  18. Vaiopoulos G, Konstantopoulos K, Mantzourani M, Kaklamanis P: Multiple myeloma associated with systemic lupus erythematosus. Leuk Lymphoma 2003;44:373-374.
  19. Urbanska-Rys H, Robak E, Kordek R, Bartkowiak J, Rieske P, Wozniacka A, et al: Multiple myeloma in a patient with systemic lupus erythematosus, myasthenia gravis and non-familial diffuse palmoplantar keratoderma. Leuk Lymphoma 2004;45:1913-1918.
  20. Bila J, Suvajdzic N, Elezovic I, et al: SLE and IgA multiple myeloma: a rare association? Med Oncol 2007;24:445-448.
  21. Maamar M, Tazi MZ, Harmouche H, Adnaoui M, Aouni M, Maaouni A: Systemic lupus erythematosus and multiple myeloma: an uncommon association. Two cases and literature review. Clin Exp Rheumatol 2008;26:667-670.

    External Resources

  22. Okoli K, Irani F, Horvath W: Multiple myeloma and systemic lupus erythematosus in a young woman. JCR 2009;15:292-294.
  23. Choi JW, Han SW, Kwon KT, Kim GW: Early onset multiple myeloma in a patient with systemic lupus erythematosus: a case report and a literature review. Clin Rheumatol 2010;29:1323-1326.
  24. Frohlich K, Holle JU, Aries PM, Gross WL, Moosig F: Successful use of bortezomib in a patient with systemic lupus erythematosus and multiple myeloma. Ann Rheum Dis 2011;70:1344-1345.
  25. Anderson LA, Pfeiffer RM, Landgren O, Gadalla S, Berndt SI, Engels EA: Risks of myeloid malignancies with autoimmune conditions. B J Cancer 2009;100:822-828.
  26. Löfström B, Backlin C, Sundström C, Hellström-Lindberg E, Ekbom A, Lundberg IE: Myeloid leukaemia in systemic lupus erythematosus - a nested case-control study based on Swedish registers. Rheum 2009;48:1222-1226.
  27. Juliusson G, Antunovic P, Derolf A, Lehmann S, Möllgård L, Stockelberg D, Tidefelt U, Wahlin A, Höglund M: Age and acute myeloid leukemia: real world data on decision to treat and outcomes from the Swedish Acute Leukemia Registry. Blood 2009;113:4179-4187.

  

Author Contacts

Dr. Sasha Bernatsky
687 Pine Avenue West
V-Building
Montreal, Quebec, H3A 1A1 (Canada)
E-Mail sasha.bernatsky@mail.mcgill.ca

  

Article Information

Received: January 2, 2013
Accepted after revision: February 21, 2013
Published online: October 2, 2013
Number of Print Pages : 6
Number of Figures : 1, Number of Tables : 2, Number of References : 27

  

Publication Details

Oncology (International Journal for Cancer Research and Treatment)

Vol. 85, No. 4, Year 2013 (Cover Date: November 2013)

Journal Editor: Markman M. (Philadelphia, Pa.)
ISSN: 0030-2414 (Print), eISSN: 1423-0232 (Online)

For additional information: http://www.karger.com/OCL


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

Objective: To describe non-lymphoma hematological malignancies in systemic lupus erythematosus (SLE). Methods: A large SLE cohort was linked to cancer registries. We examined the types of non-lymphoma hematological cancers. Results: In 16,409 patients, 115 hematological cancers [including myelodysplastic syndrome (MDS)] occurred. Among these, 33 were non-lymphoma. Of the 33 non-lymphoma cases, 13 were of lymphoid lineage: multiple myeloma (n = 5), plasmacytoma (n = 3), B cell chronic lymphocytic leukemia (B-CLL; n = 3), precursor cell lymphoblastic leukemia (n = 1) and unspecified lymphoid leukemia (n = 1). The remaining 20 cases were of myeloid lineage: MDS (n = 7), acute myeloid leukemia (AML; n = 7), chronic myeloid leukemia (CML; n = 2) and 4 unspecified leukemias. Most of these malignancies occurred in female Caucasians, except for plasma cell neoplasms (4/5 multiple myeloma and 1/3 plasmacytoma cases occurred in blacks). Conclusions: In this large SLE cohort, the most common non-lymphoma hematological malignancies were myeloid types (MDS and AML). This is in contrast to the general population, where lymphoid types are 1.7 times more common than myeloid non-lymphoma hematological malignancies. Most (80%) multiple myeloma cases occurred in blacks; this requires further investigation.

© 2013 S. Karger AG, Basel


  

Author Contacts

Dr. Sasha Bernatsky
687 Pine Avenue West
V-Building
Montreal, Quebec, H3A 1A1 (Canada)
E-Mail sasha.bernatsky@mail.mcgill.ca

  

Article Information

Received: January 2, 2013
Accepted after revision: February 21, 2013
Published online: October 2, 2013
Number of Print Pages : 6
Number of Figures : 1, Number of Tables : 2, Number of References : 27

  

Publication Details

Oncology (International Journal for Cancer Research and Treatment)

Vol. 85, No. 4, Year 2013 (Cover Date: November 2013)

Journal Editor: Markman M. (Philadelphia, Pa.)
ISSN: 0030-2414 (Print), eISSN: 1423-0232 (Online)

For additional information: http://www.karger.com/OCL


Article / Publication Details

First-Page Preview
Abstract of Clinical Study

Received: 1/2/2013 9:00:23 PM
Accepted: 2/21/2013
Published online: 10/2/2013
Issue release date: November 2013

Number of Print Pages: 6
Number of Figures: 1
Number of Tables: 2

ISSN: 0030-2414 (Print)
eISSN: 1423-0232 (Online)

For additional information: http://www.karger.com/OCL


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Bernatsky S, Clarke A, Petri MA, et al: Further defining cancer risk in systemic lupus: updated results in an expanded international multi-centre cohort. J Autoimmun 2013, in press.
  2. Howlader N, Noone AM, Krapcho M, et al (eds): SEER Cancer Statistics Review, 1975-2009 (Vintage 2009 Populations). Bethesda, National Cancer Institute, 2009.
  3. Knowling MA, Harwood AR, Bergsagel DE: Comparison of extramedullary plasmacytomas with solitary and multiple plasma cell tumors of bone. JCO 1983;1:255-262.

    External Resources

  4. Landgren O, Linet MS, McMaster ML, Gridley G, Hemminki K, Gold LR: Familial characteristics of autoimmune and hematologic disorders in 8,406 multiple myeloma patients: A population-based case-control study. Int J Cancer 2006;118:3095-3098.
  5. Anderson LA, Gadalla S, Morton LM, Landgren O, Pfeiffer R, Warren JL, Berndt SI, Ricker W, Parsons R, Engels EA: Population-based study of autoimmune conditions and the risk of specific lymphoid malignancies. Int J Cancer 2009;125:398-405.
  6. Linet MS, McLaughlin J, Harlow SD, Fraumeni JF: Family history of autoimmune disorders and cancer in multiple myeloma. Int J Epidemiology 1988;17:512-513.
  7. Canoso JJ, Cohen AS: Malignancy in a series of 70 patients with systemic lupus erythematosus. Arthritis Rheum 1974;17:383-390.
  8. Pehamberger H, Diem E, Konrad K: Systemic lupus erythematosus with multiple myeloma. Acta Derm Venereol 1978;58:527-530.

    External Resources

  9. Jordan E, Burnstein SL, Calabro JJ, Henderson ES: Multiple myeloma complicating the course of seronegative systemic lupus erythematosus. Arthritis Rheum 1978;21:260-265.
  10. Butler RC, Thomas SM, Thompson JM, Keat AC: Anaplastic myeloma in systemic lupus erythematosus. Ann Rheum Dis 1984;43:653-655.

    External Resources

  11. Solary E, Caillot D, Guy H, Olsson NO, Tanter Y, Chalopin JM: Systemic lupus erythematosus occurring in a patient with multiple myeloma. Arthritis Rheum 1986;29:933-934.
  12. Sendagorta E, Matarredona J, Brieva JA, Rodriguez ML, Ledo A: Systemic lupus erythematosus in association with smoldering multiple myeloma. J Am Acad Dermatol 1987;16:135-136.

    External Resources

  13. Umemura T, Hirai S, Ohashi M: Systemic lupus erythematosus with multiple myeloma. Nihon Hifuka Gakkai Zasshi 1988;98:1495-1503.

    External Resources

  14. Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 30-1995. A 69-year-old woman with lupus erythematosus and painful skin lesions of the feet. N Engl J Med 1995;333:862-868.
  15. Afeltra A, Amoroso A, Garzia P, Addessi MA, Pulsoni A, Bonomo L: Systemic lupus erythematosus and multiple myeloma: a rare association. Semin Arthritis Rheum 1997;26:845-849.
  16. Xu Y, Wiernik PH: Systemic lupus erythematosus and B cell hematologic neoplasm. Lupus 2001;10:841-850.
  17. Lee S, Lee S, Kim Y, Park M, Lee J, Kim H: A case of multiple myeloma in a patient with systemic lupus erythematosus. J Korean Rheum Association 2002:325-329.
  18. Vaiopoulos G, Konstantopoulos K, Mantzourani M, Kaklamanis P: Multiple myeloma associated with systemic lupus erythematosus. Leuk Lymphoma 2003;44:373-374.
  19. Urbanska-Rys H, Robak E, Kordek R, Bartkowiak J, Rieske P, Wozniacka A, et al: Multiple myeloma in a patient with systemic lupus erythematosus, myasthenia gravis and non-familial diffuse palmoplantar keratoderma. Leuk Lymphoma 2004;45:1913-1918.
  20. Bila J, Suvajdzic N, Elezovic I, et al: SLE and IgA multiple myeloma: a rare association? Med Oncol 2007;24:445-448.
  21. Maamar M, Tazi MZ, Harmouche H, Adnaoui M, Aouni M, Maaouni A: Systemic lupus erythematosus and multiple myeloma: an uncommon association. Two cases and literature review. Clin Exp Rheumatol 2008;26:667-670.

    External Resources

  22. Okoli K, Irani F, Horvath W: Multiple myeloma and systemic lupus erythematosus in a young woman. JCR 2009;15:292-294.
  23. Choi JW, Han SW, Kwon KT, Kim GW: Early onset multiple myeloma in a patient with systemic lupus erythematosus: a case report and a literature review. Clin Rheumatol 2010;29:1323-1326.
  24. Frohlich K, Holle JU, Aries PM, Gross WL, Moosig F: Successful use of bortezomib in a patient with systemic lupus erythematosus and multiple myeloma. Ann Rheum Dis 2011;70:1344-1345.
  25. Anderson LA, Pfeiffer RM, Landgren O, Gadalla S, Berndt SI, Engels EA: Risks of myeloid malignancies with autoimmune conditions. B J Cancer 2009;100:822-828.
  26. Löfström B, Backlin C, Sundström C, Hellström-Lindberg E, Ekbom A, Lundberg IE: Myeloid leukaemia in systemic lupus erythematosus - a nested case-control study based on Swedish registers. Rheum 2009;48:1222-1226.
  27. Juliusson G, Antunovic P, Derolf A, Lehmann S, Möllgård L, Stockelberg D, Tidefelt U, Wahlin A, Höglund M: Age and acute myeloid leukemia: real world data on decision to treat and outcomes from the Swedish Acute Leukemia Registry. Blood 2009;113:4179-4187.