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Review article
peer-reviewed

Disease Milestones through Bibliometric Analysis of the Top 100 Cited Articles in Multiple Myeloma



Abstract

Multiple myeloma (MM) accounts for 1.6% of all cancers and 5%-10% of all hematologic malignancies in the United States (US). Despite marked progress in disease management, it remains incurable with high rates of relapse. We conducted a bibliographic analysis on the Web of Science (WOS) from July 25, 2017 and July 29, 2017. Among the top 100 most-cited articles (1901-2012), the most cited article received 2404 citations and least cited article received 336 citations. Forty-four of 100 articles were published in journals with impact factors greater than 20. We observed that over the years, the focus of research has shifted from diagnosis, staging, and pathogenesis to better treatment outcomes. A subgroup analysis of the top 100 cited articles published in the last five years (2012-2017) demonstrated that several landmark studies, which will likely change the landscape of treating multiple myeloma, were not included in the top 100 list. Interestingly, most of these articles were focused on novel therapeutic agents. This bibliographic analysis provides a list of the 100 top-cited articles in multiple myeloma along with the captivating comprehension of the history and development in various aspects of disease processes. The landscape of this disease is rapidly evolving, and bibliometric studies such as the one presented provide a valuable tool that can highlight the important transitions in the field.

Introduction & Background

Multiple myeloma (MM) accounts for 1.6% of all cancers and 5% to 10% of all hematologic malignancies in the United States (US) [1]. Worldwide, approximately 154,000 cases are diagnosed, and 101,000 deaths are attributed to MM every year [2]. Due to the advent of novel therapeutic agents, median overall survival has increased from one to two years to seven to eight years with a meaningful improvement in the quality of life [1]. Although there has been marked progress in disease management, MM remains incurable with high rates of relapse. Ongoing clinical trials have significantly contributed to favourable disease outcomes; however, many of these interventions remain unknown to clinicians. This highlights the need for citation analysis to reflect these advances and substantial progress in this field.

Citation analysis is a type of bibliometric analysis in which evaluation and ranking of an article or journal is done on the basis citation count [3]. It identifies the milestones completed in understanding core aspects of a disease and emphasizes on major developments made in the subject matter [4-5]. Clinicians often modify their disease management based on research published in high impact journals [6] thus if most important articles can be highlighted via citation analysis it will help clinicians in making better choices for their patients. So far, no such study has been performed to conclude the most influential articles in the field of MM. The aim of the current study is to identify the 100 top-cited publications in MM and highlight the most significant advances made in the field over the preceding several decades.

Review

Materials and methods

We conducted a bibliographic analysis on the Web of Science (WOS). The time covered in WOS is between 1900 and 2017. We included journals listed in the Science Citation Index Expanded, without specific restrictions on the journals. We retrieved articles for analysis by typing “Multiple Myeloma” into the WOS search box and conducted data search with the application of English language filter on July 25, 2017. We identified 27,718 articles that were published between 1901 and 2017, ranked the articles based on citation frequency from highest to lowest, and thereafter, shortlisted the top 100 cited articles. Statistical analysis of studies was not performed, and data were reported in the form of tables. To capture the most important and latest research, we conducted a second search on July 29, 2017 to limit articles to those published during the last five years.

Results

Among the top 100 included articles, the most cited article received 2404 citations while the least cited article received 336 citations. All articles were arranged according to citation frequency (Table 1). The top 100 cited articles were published between 1990 and 2007. In our analysis, we found that the highest number of articles were published in the year 2007 (Table 2). Forty-eight of the 100 articles were published in journals with impact factors (IF) greater than 20 (Table 3). The journal with the highest number of publications was Blood with 33% of the publications (IF 13.16) followed by New England Journal of Medicine (NEJM) with 20% of the publications (IF 72.406). The country of origin with the highest number of publications on the topic of MM was the US (n=73) followed by France (n=10), Italy, and Germany (Table 4). These 100 articles sourced from 50 major institutions, with top three most significant contributors being Dana Farber Cancer Institute, Mayo Clinic, and the University of Arkansas Medical Sciences (Table 5). Most articles focused on disease management followed by pathogenesis and disease staging respectively (Table 6).

No. Author Title Journal Number of Citations
1 Durie, BGM et al. Clinical staging system for multiple-myeloma - correlation of measured myeloma cell mass with presenting clinical features, response to treatment, and survival CANCER 1975;36(842);1182674; 2404
2 Attal, M A prospective, randomized trial of autologous bone marrow transplantation and chemotherapy in multiple myeloma New England journal of medicine 1996 Jul 11;335(2):91-7 1909
3 Singhal, S et al. Antitumor activity of thalidomide in refractory multiple myeloma. New England journal of medicine 1999;341(91);10564685 1665
4 Kawano, M et al. Autocrine generation and requirement of bsf-2/il-6 for human multiple myeloma Nature 1988;332(83);3258060 1547
5 Richardson, PG et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma New England journal of medicine 2005;352(2487);15958804 1564
6 Durie, BGM et al. International uniform response criteria for multiple myeloma Leukemia 2006;20(1467);16855634 1222
7 Child, JA et al. High-dose chemotherapy with hematopoietic stem-cell rescue for multiple myeloma New England journal of medicine 2003;348(1875);12736280 1070
8 Greipp, PR et al. International staging system for multiple myeloma Journal of clinical oncology 2005;23(3412);15809451 1064
9 Hideshima, T et al. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells Cancer research 2001;61(3071);11306489 1063
10 Kumar, Shaji et al. Improved survival in multiple myeloma and the impact of novel therapies Blood 2008;111(2516);17975015 1053
11 Kyle, RA et al. Criteria for the classification of monoclonal gammopathies, multiple myeloma and related disorders: a report of the International Myeloma Working Group British journal of Hematology 2003;121(749);12780789 998
12 San M et al. Bortezomib plus melphalan and prednisone for initial treatment of multiple myeloma NEJM 2008;359(906);18753647 983
13 Kyle RA et al. Drug therapy: Multiple myeloma NEJM 2004;351(1860);15509819 869
14 Tian, E et al. The role of the Wnt-signaling antagonist DKK1 in the development of osteolytic lesions in multiple myeloma NEJM 2003;349(2483);14695408 832
15 Dimopoulos, M et al. Lenalidomide plus dexamethasone for relapsed or refractory multiple myeloma NEJM 2007;357(2123);18032762 817
16 Kyle, RA et al. Review of 1027 patients with newly diagnosed multiple myeloma Mayo clinic proceedings 2003;78(21);12528874 786
17 Kyle, RA et al. Multiple-myeloma - review of 869 cases mayo clinic proceedings 1975;50(29);1110582 779
18 Palumbo, A et al. Medical progress multiple myeloma NEJM 2011;364(1046);21410373 750
19 Weber, DM et al. Lenalidomide plus dexamethasone for relapsed multiple myeloma in North America NEJM 2007;357(2133);18032763 743
20 Bernson, JR et al. Efficacy of pamidronate in reducing skeletal events in patients with advanced multiple myeloma NEJM 1996;334(488);8559201 703
21 Chapman, MA et al. Initial genome sequencing and analysis of multiple myeloma Nature 2011;471(467)21430775 671
22 Hideshima, T et al. NF-kappa B as a therapeutic target in multiple myeloma journal of biological chemistry 2002;277(16639);11872748 662
23 Attal, M et al. Single versus double autologous stem-cell transplantation for multiple myeloma NEJM 2003;349(2495);14695409 644
24 Hideshima, T et al. Thalidomide and its analogs overcome drug resistance of human multiple myeloma cells to conventional therapy Blood 2000;96(243);11049970 640
25 Dalton, WS et al. Drug-resistance in multiple-myeloma and non-Hodgkin’s lymphoma - detection of p-glycoprotein and potential circumvention by addition of verapamil to chemotherapy Journal of clinical oncology 1989;7(415);2564428 587
26 Davies, FE et al. Thalidomide and immunomodulatory derivatives augment natural killer cell cytotoxicity in multiple myeloma Blood 2001;98(210);11418482 586
27 Barlogie, B et al. Effective treatment of advanced multiple-myeloma refractory to alkylating-agents NEJM 1984;310(1353);6546971 586
28 Keats, JJ et al. Promiscuous mutations activate the noncanonical NF-kappa B pathway in multiple myeloma Cancer Cell 2007;12(131);17692805 580
29 Richardson, PG et al. Immunomodulatory drug CC-5013 overcomes drug resistance and is well tolerated in patients with relapsed multiple myeloma Blood 2002;100(3063);12384400 567
30 Hallek, M et al. Multiple myeloma: Increasing evidence for a multistep transformation process Blood 1998;91(3);9414264 565
31 Annunziata, CM et al. Frequent engagement of the classical and alternative NF-kappa B pathways by diverse genetic abnormalities in multiple myeloma Cancer Cell 2007;12(115);17692804 552
32 Rajkumar, SV et al. Phase III clinical trial of thalidomide plus dexamethasone compared with dexamethasone alone in newly diagnosed multiple myeloma: A clinical trial coordinated by the eastern cooperative oncology group Journal of clinical oncology 2006;24(431);16365178 551
33 Palumbo, A et al. Oral melphalan and prednisone chemotherapy plus thalidomide compared with melphalan and prednisone alone in elderly patients with multiple myeloma: randomised controlled-trial Lancet 2006;367(825);16530576 549
34 Rosen, LS et al. Zoledronic acid versus pamidronate in the treatment of skeletal metastases in patients with breast cancer or osteolytic lesions of multiple myeloma: A phase III, double-blind, comparative trial Cancer Journal 2001;7(377);11693896 530
35 Facon, T et al. Melphalan and prednisone plus thalidomide versus melphalan and prednisone alone or reduced-intensity autologous stem cell transplantation in elderly patients with multiple myeloma (IFM 99-06): a randomised trial Lancet 2007;370(1209);17920916 529
36 Mitsiades, N et al. Molecular sequelae of proteasome inhibition in human multiple myeloma cells Proceedings of the national academy of sciences of USA 2002;99(14374);12391322 514
37 Mitsiades, N et al. The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications Blood 2003;101(2377);12424198 505
38 Peterson,TR et al. DEPTOR Is an mTOR Inhibitor Frequently Overexpressed in Multiple Myeloma Cells and Required for Their Survival Cell 2009;137(873);19446321 504
39 Zhan, F et al. The molecular classification of multiple myeloma Blood 2006;108(2020);16728703 502
40 Rosen, LS et al. Long-term efficacy and safety of zoledronic acid compared with pamidronate disodium in the treatment of skeletal complications in patients with advanced multiple myeloma or breast carcinoma - A randomized, double-blind, multicentre, comparative trial Cancer 2003;98(1735);14534891 493
41 Alexanian, R et al. Treatment for multiple myeloma - combination chemotherapy with different melphalan dose regimens Journal of American Medical Association 1969;208(1689);5818682 493
42 Chesi, M et al. Frequent translocation t(4;14) (p16.3; q32.3) in multiple myeloma is associated with increased expression and activating mutations of fibroblast growth factor receptor 3 Nature Genetics 1997;16(260);9207791 491
43 Gutterman, JU et al. Leukocyte interferon-induced tumor-regression in human metastatic breast-cancer, multiple-myeloma, and malignant-lymphoma Annals of Internal Medicine 1980;93(399);6159812 489
44 Barlogie, B et al. Thalidomide and hematopoietic-cell transplantation for multiple myeloma NEJM 2006;354(1021);16525139 487
45 Kuehl, WM et al. Multiple myeloma: Evolving genetic events and host interactions Nature Reviews Cancer 2002;2(175);11990854 486
46 Obeng, EA et al. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells Blood 2006;107(4907);16507771 483
47 Matsui, W et al. Characterization of clonogenic multiple myeloma cells Blood 2004;103(2332);14630803 477
48 Rajkumar, SV et al. Lenalidomide plus high-dose dexamethasone versus lenalidomide plus low-dose dexamethasone as initial therapy for newly diagnosed multiple myeloma: an open-label randomised controlled trial Lancet Oncology 2010;11(29);19853510 474
49 Vacca, A et al. Bone-marrow angiogenesis and progression in multiple-myeloma British Journal of Hematology 1994;87(503);7527645 474
50 Kyle, RA et al. Criteria for diagnosis, staging, risk stratification and response assessment of multiple myeloma Leukemia 2009;23(3);18971951 472
51 Chauhan, D et al. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib Cancer Cell 2005;8(407);16286248 472
52 Vacca, A et al. Bone marrow neovascularization, plasma cell angiogenic potential, and matrix metalloproteinase-2 secretion parallel progression of human multiple myeloma Blood 1999;93(3064);10216103 467
53 Bharti, AC et al. Curcumin (diferuloylmethane) down-regulates the constitutive activation of nuclear factor-kappa B and I kappa B alpha kinase in human multiple myeloma cells, leading to suppression of proliferation and induction of apoptosis Blood 2003;101(1053);12393461 458
54 Mitsiades, N et al. Apoptotic signalling induced by immunomodulatory thalidomide analogs in human multiple myeloma cells: therapeutic implications Blood 2002;99(4525);12036884 458
55 Avet, LH et al. Genetic abnormalities and survival in multiple myeloma: the experience of the Intergroupe Francophone du Myelome Blood 2007;109(3489);17209057 453
56 Mitsiades, CS et al. Inhibition of the insulin-like growth factor receptor-1 tyrosine kinase activity as a therapeutic strategy for multiple myeloma, other hematologic malignancies, and solid tumors Cancer Cell 2004;5(221);15050914 449
57 Klein, B et al. Interleukin-6 in human multiple-myeloma Blood 1995;85(863);7849308 449
58 Hideshima, T et al. Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets Nature Reviews Cancer 2007;7(585);17646864 447
59 Barlogie, B et al. Total therapy with tandem transplants for newly diagnosed multiple myeloma Blood 1999;9355);9864146 442
60 Broder, S et al. Impaired synthesis of polyclonal (non-paraprotein) immunoglobulins by circulating lymphocytes from patients with multiple-myeloma - role of suppressor cells NEJM 1975;293(887);1080834 442
61 McCarthy, PL et al. Lenalidomide after Stem-Cell Transplantation for Multiple Myeloma NEJM 2012;366(1770);22571201 441
62 Zhan, F et al. Global gene expression profiling of multiple myeloma, monoclonal gammopathy of undetermined significance, and normal bone marrow plasma cells Blood 2002;99(1745);11861292 436
63 Ludwig, H et al. Erythropoietin treatment of anemia associated with multiple-myeloma NEJM 1990;322(1693);2342535 434
64 Kunzmann, V et al. Stimulation of gamma delta T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma Blood 2000;96(384);10887096 433
65 Henry, DH et al. Randomized, Double-Blind Study of Denosumab Versus Zoledronic Acid in the Treatment of Bone Metastases in Patients with Advanced Cancer (Excluding Breast and Prostate Cancer) or Multiple Myeloma Journal of Clinical Oncology 2011;29(1125);21343556 428
66 Attal, M et al. Maintenance, therapy with thalidomide improves survival in patients with multiple myeloma Blood 2006;108(3289);16873668 426
67 Barlogie, B et al. Superiority of tandem autologous transplantation over standard therapy for previously untreated multiple myeloma Blood 1997;89(789);9028309 425
68 Hideshima, T et al. Advances in biology of multiple myeloma: clinical applications Blood 2004;104(607);15090448 424
69 Orlowski, RZ et al. Randomized phase III study of PEGylated liposomal doxorubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: Combination therapy improves time to progression Journal of Clinical Oncology 2007;25(3892);17679727 423
70 Shaughnessy, JD et al. A validated gene expression model of high-risk multiple myeloma is defined by deregulated expression of genes mapping to chromosome 1 Blood 2007;109(2276);17105813 422
71 Berenson, JR et al. Long-term pamidronate treatment of advanced multiple myeloma patients reduces skeletal events Journal of Clinical Oncology 1998;16(593);9469347 419
72 Richardson, PG et al. Lenalidomide, bortezomib, and dexamethasone combination therapy in patients with newly diagnosed multiple myeloma Blood 2010;116(679);20385792 416
73 Attal, M et al. Lenalidomide Maintenance after Stem-Cell Transplantation for Multiple Myeloma NEJM 2012;366(1782);22571202 411
74 Mitsiades, CS et al. Transcriptional signature of histone deacetylase inhibition in multiple myeloma: Biological and clinical implications proceeding of the national academy of sciences of the united states of America 2004;101(540);14695887 404
75 Chauhan, D et al. Multiple myeloma cell adhesion-induced interleukin-6 expression in bone marrow stromal cells involves activation of NF-kappa B Blood 1996;87(1104);8562936 403
76 Cavo, M et al. Bortezomib with thalidomide plus dexamethasone compared with thalidomide plus dexamethasone as induction therapy before, and consolidation therapy after, double autologous stem-cell transplantation in newly diagnosed multiple myeloma: a randomised phase 3 study Lancet 2010;376(2075);21146205 402
77 Dankbar, B et al. Vascular endothelial growth factor and interleukin-6 in paracrine tumor-stromal cell interactions in multiple myeloma Blood 2000;95(2630);10753844 396
78 Retting, MB et al. Kaposi's sarcoma-associated herpesvirus infection of bone marrow dendritic cells from multiple myeloma patients Science 1997;276(1851);9188529 396
79 Weber, DM et al. Thalidomide alone or with dexamethasone for previously untreated multiple myeloma Journal of Clinical Oncology 2003;21(16);12506164 394
80 Moreau, P et al. Subcutaneous versus intravenous administration of bortezomib in patients with relapsed multiple myeloma: a randomised, phase 3, non-inferiority study Lancet Oncology 2011;12(431);21507715 392
81 Barlogie, B et al. Extended survival in advanced and refractory multiple myeloma after single-agent thalidomide: identification of prognostic factors in a phase 2 study of 169 patients Blood 2001;98(492);11435324 391
82 Kyle RA et al. Multiple myeloma Blood 2008;111(2962);18332230 386
83 Tricot, G et al. Peripheral-blood stem-cell transplants for multiple-myeloma - identification of favourable variables for rapid engraftment in 225 patients Blood 1995;85(588);7529066 383
84 Bataille, R et al. Multiple myeloma NEJM 1997;336(1657);9171069 375
85 Fonseca, R et al. International Myeloma Working Group molecular classification of multiple myeloma: spotlight review Leukemia 2009;23(2210);19798094 372
86 Hideshima, T et al. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma proceedings of the national academy of sciences of the united states of America 2005;102(8567);15937109 372
87 Sonneveld, P et al. Modulation of multidrug-resistant multiple-myeloma by cyclosporine Lancet 1992;340(255);1353189 362
88 Raab, MS et al. Multiple myeloma Lancet 2009;374(324);19541364 357
89 Mitsiades, CS et al. Activation of NF-kappa B and upregulation of intracellular anti-apoptotic proteins via the IGF-1/Akt signalling in human multiple myeloma cells: therapeutic implications Oncogene 2002;21(5673);12173037 357
90 Loeffler, D et al. Interleukin-6-dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer Blood 2007;110(1330);17496199 355
91 Bergsagel, PL et al. Cyclin D dysregulation: an early and unifying pathogenic event in multiple myeloma Blood 2005;106(296);15755896 355
92 DiPersio, JF et al. Plerixafor and G-CSF versus placebo and G-CSF to mobilize hematopoietic stem cells for autologous stem cell transplantation in patients with multiple myeloma Blood 200;113(5720);19363221 354
93 Mandelli, F et al. Maintenance treatment with recombinant interferon alfa-2b in patients with multiple-myeloma responding to conventional induction chemotherapy NEJM 190;322(1430);2184356 352
94 Landgren, O et al. Monoclonal gammopathy of undetermined significance (MGUS) consistently precedes multiple myeloma: a prospective study Blood 2009;113(5412);19179464 349
95 Pasquali, S et al. Combination chemotherapy versus melphalan plus prednisone as treatment for multiple myeloma: An overview of 6,633 patients from 27 randomized trials Journal of Clinical Oncology 1998;16(3832);9850028 348
96 Fermand, JP et al. High-dose therapy and autologous peripheral blood stem cell transplantation in multiple myeloma: Up-front or rescue treatment? Results of a multicentre sequential randomized clinical trial Blood 1998;92(3131);9787148 342
97 Richardson, PG et al. A randomized phase 2 study of lenalidomide therapy for patients with relapsed or relapsed and refractory multiple myeloma Blood 2006;108(3458);16840727 340
98 Gupta, D et al. Adherence of multiple myeloma cells to bone marrow stromal cells upregulates vascular endothelial growth factor secretion: therapeutic applications Leukemia 2001;15(1950);11753617 340
99 Richardson, PG et al. Frequency, characteristics, and reversibility of peripheral neuropathy during treatment of advanced multiple myeloma with bortezomib Journal of Clinical Oncology 2006;24(3113);16754936 338
100 Dispenzieri, A et al. International Myeloma Working Group guidelines for serum-free light chain analysis in multiple myeloma and related disorders Leukemia 2009;23(215);19020545 336
 
Publication Year Number of Records
2007 10
2006 9
2003 9
2009 7
2002 7
2005 5
2004 5
2001 5
2011 4
1998 4
1997 4
2010 3
2008 3
2000 3
1999 3
1996 3
1975 3
2012 2
1995 2
1990 2
1994 1
1992 1
1989 1
1988 1
1984 1
1980 1
1969 1
 
Source Journals Impact Factor Number of Records
Blood 13.16 33
New England journal of medicine 72.406 20
Journal of Clinical Oncology 24.008 9
Leukemia 11.702 5
The LANCET 47.83 5
Cancer cell 27.4 4
Proceedings of The National Academy of Sciences of The United States of America 9.661 3
Nature reviews cancer 37.147 2
Nature 40.137 2
Mayo Clinic Proceedings 6.686 2
LANCET Oncology 33.9 2
Cancer 5.99 2
British Journal of Haematology 5.67 2
Cancer Research 9.122 1
Journal of Biological Chemistry 4.125 1
Cancer Journal 4.218 1
Cell 30.41 1
Journal of American Medical Association 44.405 1
Nature Genetics 27.959 1
Annals of Internal Medicine 17.202 1
Science 37.205 1
Oncogene 7.519 1
 
Countries Number of Records
USA 73
France 10
Italy 7
Germany 4
England 1
Spain 1
Netherlands 1
Austria 1
Japan 1
Greece 1
 
Institutions Number of Records
Dana Farber Cancer Institute 22
Mayo Clinic 13
University of Arkansas Medical Sciences 9
UTMD Anderson Cancer Center 5
University of California Los Angeles 4
Chu de Toulouse 4
Chu de Nantes 3
NIH national cancer institute (NCI) 3
University of Turin 2
University of Bari Bari 2
University of Arizona 2
John Hopkins University 1
Eli & Etdythe l. Broad Institute, Seven Cambridge Centers 1
University of Munich 1
Cancer Institute Medical Group 1
Adult division of The South West Cancer Chemotherapy Study Group 1
University of Miami Miller School of Medicine 1
University of South Carolina 1
Hiroshima University 1
Whitehead Institute Biomedical Research, Nine Cambridge Center 1
Bethesda Naval Hospital, Center Cancer Research 1
University of Leeds 1
International Myeloma Working Group 1
University of Athens School of Medicine 1
National Institute of Health 1
Chu Lille 1
University of Salamanca 1
University of Bologna 1
Sapienza University Rome 1
Erasmus University Rotterdam 1
Cedars Sinai Outpatient Cancer Center 1
University of Wurzburg 1
University of Muenster 1
Washington University 1
St Louis Hospital 1
University of North Carolina 1
University of Vienna 1
Institute of Molecular Genetics 1
Roswell Park Center Institute 1
University of Leipzig 1
Joan Karnell Cancer Center 1
Arcispedale Santa Maria Nuova 1
 
Category Number of Studies
Management 51
Pathogenesis 33
Staging 3
Review Articles    4
 

Regarding authors with the highest number of publications, Hideshima T and Mitsiades CS ranked first with six publications each, followed by Barlogie B, Kyle RA, and Richardson PG with five publications each, and Attal M with four publications (Table 7). Anderson KC was the top author with 26 publications as co-author. Most of the articles were categorized under the title of Hematology (40%) followed by General Internal Medicine (29%), and Oncology (27%), respectively.

Author Name Number of Records
Hideshima T 6
Mitsiades CS 6
Richardson PG 5
Kyle RA 5
Barlogie B 5
Attal M 4
Durie BGM 2
Chauhan D 2
Rajkumar SV 2
Palumbo A 2
Rosen LS 2
Bernson JR 2
Vacca A 2
Weber DM 2
Singhal S 1
 

A subgroup analysis was performed to capture the development and progress of MM therapy during the last five years. It demonstrated that the most cited article received 441 citations while the least cited article received only 70 citations. Forty-four of the 100 articles were published in 2012, 26 in 2013, and 20 in 2014. The top three journals targeted by authors were Blood (35%), Journal of Clinical Oncology (11%), and NEJM (11%). The author with the most publications as the first author was Palumbo A with five publications, whereas the second position was shared by San-Miguel J, Kumar S, and Richardson PG with four publications each. The country with the highest output in last five years was the US (79%). The top three research areas focused by authors were Hematology (50%), Oncology (38%), and General Internal Medicine (14%).

Discussion

Bibliometric analysis has been used in the past to identify frontiers in specific fields and to evaluate the contribution of authors, institutions, and nations. The total number of citations received by an article represents its overall contribution to the clinical world.

Our study demonstrates that over the years, the focus of research has shifted from diagnosis, staging, and pathogenesis to better treatment outcomes in patients with MM (51 publications). The timeline for the evolution of MM therapy has progressed starting with melphalan-prednisone in 1960’s which was the standard of care for about 30 years. During the next 30 years, therapy further evolved when drugs such as vincristine, doxorubicin, and dexamethasone (VAD), alkylating agents such as Carmustine (VBAD), cyclophosphamide and melphalan (VCMP) were introduced. However, these therapeutic agents did not significantly improve the outcomes. High-dose melphalan followed by autologous stem cell transplant (ASCT) was a step towards favorable clinical outcomes. The armamentarium against MM was revolutionized by the development of ground-breaking agents such as immunomodulators (thalidomide and lenalidomide) and the proteasome inhibitor (bortezomib).

After better treatment outcomes, the most frequently encompassed category was disease pathogenesis (29 publications). Over the years, a thorough understanding of aetiological factors and relation of genetic aberrations to pathogenesis has laid the foundation for significant improvement in disease management and prognostication. Two of the top ten most cited articles were aimed at the staging of disease. The first being the Clinical Staging System proposed by Durie BGM et al., although the most cited article in our list is no longer the primary staging system. Modern-day physicians rely on the International Staging System (eighth most cited article) and cytogenetics to classify MM.

The findings of this analysis demonstrated that 32 of 100 articles were published in general medical journals, for which there may be several reasons. Firstly, general medicine journals capture a wide range of population compared to speciality journals. Secondly, patients with MM are usually co-managed by internists and oncologists which would make the general medicine audience more interested in advancements in MM. Lastly, the novel therapeutic options have different mechanisms of actions and extensive side effect profiles. It is very important for the general internist to be aware of these side effects to effectively manage these patients in both inpatient and outpatient settings.

The authors of these studies targeted high impact factor journals which is evidenced by the fact that most of the articles were published in journals with impact factors greater than 20. This suggests that MM researchers tend to publish in prestigious and well-respected journals that capture a wide range of the population. We noted diversity amongst the authors, as only a total of 12 articles were contributed by the top two publishers as first authors. These findings suggest a diverse group of researchers involved in the MM field.

Among the top 100 cited articles, only seven studies were focused on bortezomib-containing regimens, whereas none of them included carfilzomib or ixazomib based novel therapeutic regimens. This shows that articles with a high frequency of citations consisted mostly of early-published articles. Therefore, one limitation of such articles is that they favour older studies. Among the top 100 list, only two articles from 2012 were included and the articles published after 2012 did not have enough citations to be included in top 100 list. Therefore, we conducted a subgroup analysis of top 100 articles published after 2011. A bibliographic analysis of top cited articles published in the last five years (2012-2017) showed different results from our original search. Only two studies from the sub group analysis were included in the primary analysis due to a lower number of total citations received. Studies 2012, and onwards were focused on latest developments in the field of MM including therapeutic agents such as novel proteasome inhibitors (carfilzomib, ixazomib), monoclonal antibodies (daratumumab, elotuzumab), and chimeric antigen receptor T cell therapy [7-11].

Our primary limitation was conducting the search in the “title mode”. Therefore, articles that did not contain MM in the title were not retrieved or included in our study. Secondly, our search was limited to the WOS database which excludes citations of textbooks and other databases which are weaker at tracking older publications. Finally, articles published in languages other than English were excluded.

Conclusions

This bibliographic analysis provides a list of the 100 top-cited articles in MM along with the captivating comprehension of the history and development in various aspects of disease processes. The landscape of MM is rapidly evolving, and bibliometric studies such as the one we present provides a valuable tool that can highlight important transitions in the field. As new evidence continues to emerge, these types of analyses can provide a quantitative instrument to guide the researchers and funding agencies to assess the overall direction of the field with limited health care resources.


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Review article
peer-reviewed

Disease Milestones through Bibliometric Analysis of the Top 100 Cited Articles in Multiple Myeloma


Author Information

Azka Latif

Hematology and Oncology, University of Arizona, Tucson, USA

Vikas Kapoor

Hematology and Oncology, University of Arizona, Tucson, USA

Qurat ul ain riaz Sipra

Department of Internal Medicine, University of Arizona, Tucson, USA

Saad Ullah Malik

Hematology and Oncology, University of Arizona, Tucson, USA

Jawad Bilal Corresponding Author

Medicine, University of Arizona, Tucson, USA

Irbaz Bin Riaz

Hematology and Oncology, Mayo Clinic and Foundation, Rochester, MN, USA

Faiz Anwer

Hematology and Oncology, The University of Arizona, Tucson, USA


Ethics Statement and Conflict of Interest Disclosures

Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.

Acknowledgements

We thank Ms. Marsha A Halajian for editing and final proofing of the manuscript.


Review article
peer-reviewed

Disease Milestones through Bibliometric Analysis of the Top 100 Cited Articles in Multiple Myeloma


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