100 Citation Classics in the Melanoma Literature: A Bibliometric Analysis Cormac W. Joyce, MB, BCh,* Conor M. Sugrue, MB, BCh,* Kenneth M. Joyce, MB, BCh,* Jack L. Kelly, FRCS (Plast),*† and Padraic J. Regan, FRCS (Plast)*†

BACKGROUND Modern immunologic therapies targeting genetic mutations have created a renewed interest in melanoma research, and this is reflected in the increasing number of published works. OBJECTIVE The purpose of this study was to identify the top 100 most cited articles in melanoma and to examine the characteristics of each individual article. METHODS Using an electronic database through the Web of Science, we were able to determine the 22 journals that contributed to the 100 most cited articles in melanoma. RESULTS Each article was examined individually looking at characteristics such as subject matter, article type, country of origin, institution, authorship, and year of publication. The New England Journal of Medicine contributed the most articles to the top 100 with 20 articles, whereas the most cited article originated from the Archives of Surgery and has been cited 2,384 times. The United States produced 74% of the top 100 articles, and the most prolific institution was the National Cancer Institute in Maryland with 18 articles. CONCLUSION This study has identified the most significant contributions to melanoma research over the past 63 years and identifies many important scientific breakthroughs and landmarks that have occurred during this time. The authors have indicated no significant interest with commercial supporters.

t is believed that melanoma was first described by Hippocrates of Cos in the fifth century BC as a “dark tumour,”1 but it was not until 1804 in Paris that Rene Laennec coined the term melanose when describing the disease.2,3 Much has been written historically about melanoma, and publications in the medical literature have continued to steadily increase over time. The relatively recent discovery of immunologic targets has created renewed interest in melanoma research. This has been reflected by improved survival rates despite an overall increase in disease prevalence. The most influential published works in melanoma research are scattered through a various number of high impact factor (IF) scientific journals, yet it is unknown which exact articles have been the most influential.

I

The pertinence of published article to a specific area is echoed in the amount of citations from peers it obtains. The reputation of an author is reflected in the number of citations that he or she receives. The number of citations is also hugely important for journals too, as the IF of a journal is reliant on the number of citations that its published articles receive. 4–6 The IF is a measure that reflects the average number of citations to recent articles published in the journal. Frequently, the IF is used as a proxy for the relative significance of an academic journal within its specialist field, with journals with a higher IF deemed more reputable and important than journals with a lower IF. Despite the IF factor system being recognizably and inherently flawed, it is still viewed as the leading method for assessing the merits of scientific journals. For a given

*Department of Plastic and Reconstructive Surgery, University Hospital Galway, Galway, Ireland; †National University of Ireland Galway, Galway, Ireland

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© 2014 by the American Society for Dermatologic Surgery, Inc. Published by Lippincott Williams & Wilkins ISSN: 1076-0512 Dermatol Surg 2014;40:1284–1298 DOI: 10.1097/DSS.0000000000000134

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year, the IF can be calculated by averaging the number of citations received per article published in that journal during the preceding 2 years. Numerous medical and surgical specialties have previously published on the most cited articles in their specialties and include general surgery,7 anesthesiology,8 orthopedics,9,10 otolaryngology,11 radiology,12 plastic surgery,13,14 dermatology,15 and critical care medicine.16 These publications have permitted greater understanding of characteristics required for a piece of research to attain the citation quotient necessary to attain status as a “classic” article. The purpose of our study was to identify and analyze the 100 most cited melanoma articles published in the peer-reviewed biomedical literature in the last 60 years.

Methods Sixty-four international journals were included in our search but only 22 of these actually contributed articles to the top 100 list (Table 1). The journals chosen by us were high IF scientific journals that are well regarded internationally. They included a mixture of well renowned scientific, medical, surgical, dermatology, and oncology journals. We chose the initial 64 journals because they were believed to be the most relevant and would also be the most likely to produce the most cited articles in melanoma research. The Web of Science, which is produced by the Institute of Scientific Information (ISI), provides Web access to the Science Citation Index,17 MEDLINE, and other citation indexes, which collectively index more than 12,000 journals worldwide. Using this on-line database, we were able to identify the most cited articles in melanoma research from 1945 until 2013 in our chosen journals. We searched for articles indexed by the terms “melanoma,” “melanomatous,” “melanocyte,” “melanocytic,” and “melanomatosis,” and we were able to identify the most frequently cited articles in melanoma from 1945 to 2013. Any articles not relevant to melanoma were excluded from our study. In addition to original research articles, we included editorials, correspondences, and review articles.

TABLE 1. Number of Articles Each Journal Contributed to the Top 100 Articles on Melanoma Number of Articles in Top 100

Journal New England Journal of Medicine

20

Journal of Clinical Oncology

19

Cancer Research

14

Annals of Surgery Cancer

10 6

Journal of the National Cancer Institute

4

International Journal of Cancer

4

Lancet

4

Archives of Surgery

2

Journal of the American Medical Association

2

Archives of Dermatology

2

Surgery

2

Oncogene

2

British Medical Journal

1

Cancer Cell

1

Journal of the American Academy of Dermatology

1

British Journal of Cancer

1

Annals of Internal Medicine

1

Nature Reviews Cancer

1

Melanoma Research

1

Lancet Oncology CA: A Cancer Journal for Clinicians

1 1

Advances in Cancer Research, American Journal of Dermatopathology, American Journal of Family Medicine, American Journal of Medicine, American Journal of Surgical Pathology, American Journal of Surgery, American Journal of Surgical Pathology, Annals of Medicine, Annals of Oncology, Biochimica et Biophysica Acta (BBA)—Reviews on Cancer, BioMed Central, British Journal of Dermatology, British Medical Bulletins, Canadian Medical Association Journal, Cancer Discovery, Cancer Epidemiology, Biomarkers and Prevention, Cancer Metastasis Review, Cancer Prevention Research, Cancer Treatment Review, Carcinogenesis, Clinical Cancer Research, Cochrane Database Systematic Reviews, European Journal of Cancer, European Journal of Surgical Oncology, Experimental Dermatology, Journal of the National Comprehensive Cancer Network, Journal of Cutaneous Pathology, Journal of Internal Medicine, Journal of Pathology, Journal of Surgical Oncology, Mayo Clinic Proceedings, Medicine, Molecular Cancer Therapy, Molecular Oncology, Neoplasia, Oncotarget, Pigment Cell and Melanoma Research, Pigment Cell Research, Plastic and Reconstructive Surgery, PLoS Medicine, Seminars in Cutaneous Medicine and Surgery, and Seminars in Cancer Biology were all included in the search but did not contribute any articles to the top 100.

We then selected the 100 most cited articles in melanoma for further study. We used the criteria previously described by Paladugu and colleagues7 to analyze

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100 CITATION CLASSICS IN THE MELANOMA LITERATURE

each article in turn looking for subject matter, article type, authorship, institution, level of evidence, institution, country of origin, and year of publication. The Oxford Centre for Evidence-based Medicine was used to source information relating to level of evidence.

the top 100 articles. The top article in the most cited list by Morton and colleagues received a citation index of 91.6, which ranked it 13th in terms of citation index (Table 3). Interestingly, only 4 of the top 10 articles from the list of most cited articles made it in to the top 10 in terms of citation index.

The difference in time since publication among the top 100 articles may feature a bias because it is reported that older articles are more likely to have obtained more citations merely because of a longer citable period.14 To limit this bias, we evaluated the citation index of the 50 most cited articles in the top 100. To calculate the citation index for articles more than 10 year old, we calculated the total number of times they were cited per year until 10 years after publication and divided by 10. For articles that had been published within the last 10 years, the total number of citations since publication was divided by the number of years since publication. Ten years was chosen as the cutoff because it has been reported that articles are likely to receive most citations within the first 10 years of publication.18

In the top 100 articles, 81 were clinical and 19 were experimental. The clinical articles included 12 review articles, 2 updates to the American Joint Committee on Cancer (AJCC) melanoma staging system, and 1 case report (Table 2). The type of clinical study and level of evidence can be seen in Table 4.

Results The 100 most sited articles in melanoma are listed in Table 2 and are arranged in descending order, according to the number of times cited. The number of citations ranged from 2,384 to 293, and the mean number of citations per article was 526. The articles by Chapman and colleagues and Robert and colleagues were published in the same issue of the New England Journal of Medicine on June fifth 2011, and both of these articles are the most recent articles in the top 100. The oldest article, by Allen and Spitz, was published in Cancer in 1953, and the article details the clinicopathologic criteria for melanoma diagnosis and prognosis. The decade that contributed most articles to the top 100 was the 1990s with 41 articles. Twenty-six articles in the top 100 were published between 2000 and 2009, whereas the 1980s produced 17 articles. The 1950s contributed 1 solitary article, whereas the 1960s produced 3 articles. Four articles in the top 100 were published after 2010. The article with the highest citation index (563.3) was by Chapman and colleagues and was ranked ninth in

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Twenty-two journals contributed to the top 100 articles despite 64 journals initially being chosen for our study. These include high impact scientific journals and renowned medical and surgical journals. The New England Journal of Medicine contributed the most number of articles to the top 100 with 20 articles. This was followed by the Journal of Clinical Oncology with 19 articles (Table 1). Ten countries were responsible for producing all of the articles in the most cited list—United States, United Kingdom, Australia, Italy, Belgium, Austria, Denmark, France, Greece, and New Zealand. Seventy-four percent of articles came from the United States, whereas 6% came from the United Kingdom. The institution that produced the most number of articles was the National Cancer Institute in the United States with 18 articles. The University of Pennsylvania, MD Anderson in Texas, the John Wayne Institute in California, and the National Cancer Institute in Milan, Italy, also significantly contributed to the top 100. Of the 100 articles, 7 articles reported on sentinel node biopsy, 3 on the BRAF mutation, 2 on ipilimumab treatment, and 2 on the AJCC melanoma staging system. Ten authors were first-named authors on more than 1 article in the top 100 most cited articles. Balch wrote 7 articles, whereas Morton was first-named author on 5 articles (Table 5). Rosenberg was the lead author of 4 articles and Kirkwood, Clark Jr, and Veronesi wrote 3 articles each. Further 4 authors wrote 2 articles each.

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TABLE 2. Top 100 Most Cited Articles on Melanoma Rank

Article

Times Cited

1

Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK, Foshag LJ, Cochran AJ. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 1992;127:392–9

2,384

2

Clark WH Jr, From L, Bernardino EA, Mihm MC. The histogenesis and biologic behavior of primary human malignant melanomas of the skin. Cancer Res 1969;29:705–27

1,705

3

A Breslow. Thickness, cross-sectional areas and depth of invasion in the prognosis of cutaneous melanoma. Ann Surg 1970;172:902–8

1,554

4

Balch CM, Buzaid AC, Soong SJ, Atkins MB, Cascinelli N, Coit DG, Fleming ID, Gershenwald JE, Houghton A Jr, Kirkwood JM, McMasters KM, Mihm MF, Morton DL, Reintgen DS, Ross MI, Sober A, Thompson JA, Thompson JF. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol 2001;19:3635–48

1,476 (AJCC staging guidelines)

5

Rosenberg SA, Packard BS, Aebersold PM, Solomon D, Topalian SL, Toy ST, Simon P, Lotze MT, Yang JC, Seipp CA. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N Engl J Med 1988;319:1676–80

1,338

6

Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbe´ C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711–23

1,318

7

Kirkwood JM, Strawderman MH, Ernstoff MS, Smith TJ, Borden EC, Blum RH. Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J Clin Oncol 1996;14:7–17 Balch CM, Soong SJ, Gershenwald JE, Thompson JF, Reintgen DS, Cascinelli N, Urist M, McMasters KM, Ross MI, Kirkwood JM, Atkins MB, Thompson JA, Coit DG, Byrd D, Desmond R, Zhang Y, Liu PY, Lyman GH, Morabito A. Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer melanoma staging system. J Clin Oncol 2001;19:3622–34

1,164

8

1,126

9

Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, Hogg D, Lorigan P, Lebbe C, Jouary T, Schadendorf D, Ribas A, O’Day SJ, Sosman JA, Kirkwood JM, Eggermont AM, Dreno B, Nolop K, Li J, Nelson B, Hou J, Lee RJ, Flaherty KT, McArthur GA; BRIM-3 Study Group. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011;364:2507–16

1,067

10

Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, O’Dwyer PJ, Lee RJ, Grippo JF, Nolop K, Chapman PB. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010;363:809–19

1,014

11

Rosenberg SA, Aebersold P, Cornetta K, Kasid A, Morgan RA, Moen R, Karson EM, Lotze MT, Yang JC, Topalian SL, Merino MJ, Culver K, Miller AD, Blaese RM, Anderson WF. Gene transfer into humans—immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. N Engl J Med 1990;323:570–8

824

12

Curtin JA, Fridlyand J, Kageshita T, Patel HN, Busam KJ, Kutzner H, Cho KH, Aiba S, Bro¨cker EB, LeBoit PE, Pinkel D, Bastian BC. Distinct sets of genetic alterations in melanoma. N Engl J Med 2005;353:2135–47

796

13

Allen AC, Spitz S. Malignant melanoma; a clinicopathological analysis of the criteria for diagnosis and prognosis. Cancer 1953;6:1–45

778 (Review)

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100 CITATION CLASSICS IN THE MELANOMA LITERATURE

TABLE 2. (Continued ) Rank

Article

Times Cited

14

Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, Royal RE, Kammula U, White DE, Mavroukakis SA, Rogers LJ, Gracia GJ, Jones SA, Mangiameli DP, Pelletier MM, Gea-Banacloche J, Robinson MR, Berman DM, Filie AC, Abati A, Rosenberg SA. Adoptive cell transfer therapy following nonmyeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005;23:2346–57

770

15

Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, Buzaid AC, Cochran AJ, Coit DG, Ding S, Eggermont AM, Flaherty KT, Gimotty PA, Kirkwood JM, McMasters KM, Mihm MC Jr, Morton DL, Ross MI, Sober AJ, Sondak VK. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009;27:6199–206

709 (AJCC staging guidelines)

16

Gershenwald JE, Thompson W, Mansfield PF, Lee JE, Colome MI, Tseng CH, Lee JJ, Balch CM, Reintgen DS, Ross MI. Multi-institutional melanoma lymphatic mapping experience: the prognostic value of sentinel lymph node status in 612 stage I or II melanoma patients. J Clin Oncol 1999;17:976–83

701

17

Morton DL, Thompson JF, Cochran AJ, Mozzillo N, Elashoff R, Essner R, Nieweg OE, Roses DF, Hoekstra HJ, Karakousis CP, Reintgen DS, Coventry BJ, Glass EC, Wang HJ; MSLT Group. Sentinel-node biopsy or nodal observation in melanoma. N Engl J Med 2006;355:1307–17

697

18

Clark WH Jr, Elder DE, Guerry D IV, Braitman LE, Trock BJ, Schultz D, Synnestvedt M, Halpern AC. Model predicting survival in stage I melanoma based on tumor progression. J Natl Cancer Inst 1989;81:1893–904

687

19

Albelda SM, Mette SA, Elder DE, Stewart R, Damjanovich L, Herlyn M, Buck CA. Integrin distribution in malignant melanoma: association of the beta 3 subunit with tumor progression. Cancer Res 1990;50:6757–64

679

20

Atkins MB, Lotze MT, Dutcher JP, Fisher RI, Weiss G, Margolin K, Abrams J, Sznol M, Parkinson D, Hawkins M, Paradise C, Kunkel L, Rosenberg SA. Highdose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J Clin Oncol 1999;17:2105–16

674

21

Rosenberg SA, Yang JC, Topalian SL, Schwartzentruber DJ, Weber JS, Parkinson DR, Seipp CA, Einhorn JH, White DE. Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high-dose bolus interleukin 2. JAMA 1994;271:907–13 Marchand M, van Baren N, Weynants P, Brichard V, Dre´no B, Tessier MH, Rankin E, Parmiani G, Arienti F, Humblet Y, Bourlond A, Vanwijck R, Lie´nard D, Beauduin M, Dietrich PY, Russo V, Kerger J, Masucci G, Ja¨ger E, De Greve J, Atzpodien J, Brasseur F, Coulie PG, van der Bruggen P, Boon T. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int J Cancer 1999;80:219–30

671

23

Banchereau J, Palucka AK, Dhodapkar M, Burkeholder S, Taquet N, Rolland A, Taquet S, Coquery S, Wittkowski KM, Bhardwaj N, Pineiro L, Steinman R, Fay J. Immune and clinical responses in patients with metastatic melanoma to CD34 (+) progenitor-derived dendritic cell vaccine. Cancer Res 2001;61:6451–8

573

24

Clark WH Jr, Reimer RR, Greene M, Ainsworth AM, Mastrangelo MJ. Origin of familial malignant melanomas from heritable melanocytic lesions. “The B-K mole syndrome.” Arch Dermatol 1978;114:732–8

570 (Review)

25

Middleton MR, Grob JJ, Aaronson N, Fierlbeck G, Tilgen W, Seiter S, Gore M, Aamdal S, Cebon J, Coates A, Dreno B, Henz M, Schadendorf D, Kapp A, Weiss J, Fraass U, Statkevich P, Muller M, Thatcher N. Randomized phase III study of temozolomide versus dacarbazine in the treatment of patients with advanced metastatic malignant melanoma. J Clin Oncol 2000;18:158–66

557

26

Smith B, Selby P, Southgate J, Pittman K, Bradley C, Blair GE. Detection of melanoma cells in peripheral blood by means of reverse transcriptase and polymerase chain reaction. Lancet 1991;338:1227–9

544

22

1288

605

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TABLE 2. (Continued ) Rank

Article

Times Cited

27

Brose MS, Volpe P, Feldman M, Kumar M, Rishi I, Gerrero R, Einhorn E, Herlyn M, Minna J, Nicholson A, Roth JA, Albelda SM, Davies H, Cox C, Brignell G, Stephens P, Futreal PA, Wooster R, Stratton MR, Weber BL. BRAF and RAS mutations in human lung cancer and melanoma. Cancer Res 2002;62:6997– 7000

536

28

Lienard D, Ewalenko P, Delmotte JJ, Renard N, Lejeune FJ. High-dose recombinant tumor necrosis factor alpha in combination with interferon gamma and melphalan in isolation perfusion of the limbs for melanoma and sarcoma. J Clin Oncol 1992;10:52–60

532

29

Rosenberg SA, Yannelli JR, Yang JC, Topalian SL, Schwartzentruber DJ, Weber JS, Parkinson DR, Seipp CA, Einhorn JH, White DE. Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2. J Natl Cancer Inst 1994;86:1159–66 Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S, Van Belle PA, Xu X, Elder DE, Herlyn M. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 2005;65:9328–37

517

31

Veronesi U, Adamus J, Bandiera DC, Brennhovd IO, Caceres E, Cascinelli N, Claudio F, Ikonopisov RL, Javorskj VV, Kirov S, Kulakowski A, Lacoub J, Lejeune F, Mechl Z, Morabito A, Rode´ I, Sergeev S, van Slooten E, Szcygiel K, Trapeznikov NN. Inefficacy of immediate node dissection in stage 1 melanoma of the limbs. N Engl J Med 1977;297:627–30

500

32

Reintgen D, Cruse CW, Wells K, Berman C, Fenske N, Glass F, Schroer K, Heller R, Ross M, Lyman G. The orderly progression of melanoma nodal metastases. Ann Surg 1994;220:759–67

498

33

Robert C, Thomas L, Bondarenko I, O’Day S, M D JW, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ, Davidson N, Richards J, Maio M, Hauschild A, Miller WH Jr, Gascon P, Lotem M, Harmankaya K, Ibrahim R, Francis S, Chen TT, Humphrey R, Hoos A, Wolchok JD. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011;364:2517–256

496

34

Morton D, Eilber FR, Malmgren RA, Wood WC. Immunological factors which influence response to immunotherapy in malignant melanoma. Surgery 1970;68:158–63

479

35

Morton DL, Thompson JF, Essner R, Elashoff R, Stern SL, Nieweg OE, Roses DF, Karakousis CP, Mozzillo N, Reintgen D, Wang HJ, Glass EC, Cochran AJ. Validation of the accuracy of intraoperative lymphatic mapping and sentinel lymphadenectomy for early-stage melanoma: a multicenter trial. Multicenter Selective Lymphadenectomy Trial Group. Ann Surg 1999;230:453–63

474

36

Curtin JA, Busam K, Pinkel D, Bastian BC. Somatic activation of KIT in distinct subtypes of melanoma. J Clin Oncol 2006;24:4340–6 Kirkwood JM, Ibrahim JG, Sosman JA, Sondak VK, Agarwala SS, Ernstoff MS, Rao U. High-dose interferon alfa-2b significantly prolongs relapse-free and overall survival compared with the GM2-KLH/QS-21 vaccine in patients with resected stage IIB-III melanoma: results of intergroup trial E1694/S9512/ C509801. J Clin Oncol 2001;19:2370–80

473

38

Lewis MG, Ikonopisov RL, Nairn RC, Phillips TM, Hamilton-Fairley G, Bodenham DC, Alexander P. Tumour-specific antibodies in human malignant melanoma and their relationship to the extent of the disease. Br Med J 1969;3:547–52

448

39

Weeraratna AT, Jiang Y, Hostetter G, Rosenblatt K, Duray P, Bittner M, Trent JM. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 2002;1:279–88

449

40

Kirkwood JM, Ibrahim JG, Sondak VK, Richards J, Flaherty LE, Ernstoff MS, Smith TJ, Rao U, Steele M, Blum RH. High- and low-dose interferon alfa-2b in high-risk melanoma: first analysis of intergroup trial E1690/S9111/C9190. J Clin Oncol 2000;18:2444–58

448

30

37

516

473

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100 CITATION CLASSICS IN THE MELANOMA LITERATURE

TABLE 2. (Continued ) Rank

Article

Times Cited

41

Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U, Robbins PF, Huang J, Citrin DE, Leitman SF, Wunderlich J, Restifo NP, Thomasian A, Downey SG, Smith FO, Klapper J, Morton K, Laurencot C, White DE, Rosenberg SA. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 2008;26:5233–9

442

42

Balch CM, Murad TM, Soong SJ, Ingalls AL, Halpern NB, Maddox WA. A multifactorial analysis of melanoma: prognostic histopathological features comparing Clark’s and Breslow’s staging methods. Ann Surg 1978;188:732–42

442

43

Morton DL, Malmgren RA, Holmes EC, Ketcham AS. Demonstration of antibodies against human malignant melanoma by immunofluorescence. Surgery 1968;64:233–40

434

44

Fidler IJ. Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 1975;35:218–24

432

45

Breslow A. Tumor thickness, level of invasion and node dissection in stage I cutaneous melanoma. Ann Surg 1975;182:572–5

410

46

Balch CM, Soong SJ, Bartolucci AA, Urist MM, Karakousis CP, Smith TJ, Temple WJ, Ross MI, Jewell WR, Mihm MC, Barnhill RL, Wanebo HJ. Efficacy of an elective regional lymph node dissection of 1–4 mm thick melanomas for patients 60 years of age and younger. Ann Surg 1996;224:255–63

406

47

Clemente CG, Mihm MC Jr, Bufalino R, Zurrida S, Collini P, Cascinelli N. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 1996;77:1303–10

406

48

Soengas MS, Lowe SW. Apoptosis and melanoma chemoresistance. Oncogene 2003;22:3138–51

401 (Review)

49

Livingston PO, Wong GY, Adluri S, Tao Y, Padavan M, Parente R, Hanlon C, Calves MJ, Helling F, Ritter G. Improved survival in stage III melanoma patients with GM2 antibodies: a randomized trial of adjuvant vaccination with GM2 ganglioside. J Clin Oncol 1994;12:1036–44

393

50

Attia P, Phan GQ, Maker AV, Robinson MR, Quezado MM, Yang JC, Sherry RM, Topalian SL, Kammula US, Royal RE, Restifo NP, Haworth LR, Levy C, Mavroukakis SA, Nichol G, Yellin MJ, Rosenberg SA. Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anticytotoxic T-lymphocyte antigen-4. J Clin Oncol 2005;23:6043–53

391

51

Chang AE, Karnell LH, Menck HR. The National Cancer Data Base report on cutaneous and noncutaneous melanoma: a summary of 84,836 cases from the past decade. The American College of Surgeons Commission on Cancer and the American Cancer Society. Cancer 1998;83:1664–78

389

52

Jansen B, Wacheck V, Heere-Ress E, Schlagbauer-Wadl H, Hoeller C, Lucas T, Hoermann M, Hollenstein U, Wolff K, Pehamberger H. Chemosensitisation of malignant melanoma by BCL2 antisense therapy. Lancet 2000;356:1728–33

382

53

Lee JH, Miele ME, Hicks DJ, Phillips KK, Trent JM, Weissman BE, Welch DR. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer Inst 1996;88:1731–7 Miller AJ, Mihm MC Jr. Melanoma. N Engl J Med 2006;355:51–65

377

54 55

56

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Albertini JJ, Cruse CW, Rapaport D, Wells K, Ross M, DeConti R, Berman CG, Jared K, Messina J, Lyman G, Glass F, Fenske N, Reintgen DS. Intraoperative radio-lympho-scintigraphy improves sentinel lymph node identification for patients with melanoma. Ann Surg 1996;223:217–24 Gilchrest BA, Eller MS, Geller AC, Yaar M. The pathogenesis of melanoma induced by ultraviolet radiation. N Engl J Med 1999;340:1341–8

371 (Review) 370

369 (Review)

57

Koh HK. Cutaneous melanoma. N Engl J Med 1991;325:171–82

368 (Review)

58

Tsao H, Atkins MB, Sober AJ. Management of cutaneous melanoma. N Engl J Med 2004;351:998–1012

367 (Review)

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TABLE 2. (Continued ) Rank

Article

Times Cited

59

Guldberg P, thor Straten P, Birck A, Ahrenkiel V, Kirkin AF, Zeuthen J. Disruption of the MMAC1/PTEN gene by deletion or mutation is a frequent event in malignant melanoma. Cancer Res 1997;57:3660–3

363

60

Cascinelli N, Morabito A, Santinami M, MacKie RM, Belli F. Immediate or delayed dissection of regional nodes in patients with melanoma of the trunk: a randomised trial. WHO Melanoma Programme. Lancet 1998;351:793–6

361

61

Chapman PB, Einhorn LH, Meyers ML, Saxman S, Destro AN, Panageas KS, Begg CB, Agarwala SS, Schuchter LM, Ernstoff MS, Houghton AN, Kirkwood JM. Phase III multicenter randomized trial of the Dartmouth regimen versus dacarbazine in patients with metastatic melanoma. J Clin Oncol 1999;17:2745– 51

361

62

Elwood JM, Jopson J. Melanoma and sun exposure: an overview of published studies. Int J Cancer 1997;73:198–203

361 (Review)

63

Poste G, Doll J, Hart IR, Fidler IJ. In vitro selection of murine B16 melanoma variants with enhanced tissue-invasive properties. Cancer Res 1980;40:1636–44

358

64

Holly EA, Kelly JW, Shpall SN, Chiu SH. Number of melanocytic nevi as a major risk factor for malignant melanoma. J Am Acad Dermatol 1987;17:459–68

357

65

Goldstein AM, Fraser MC, Struewing JP, Hussussian CJ, Ranade K, Zametkin DP, Fontaine LS, Organic SM, Dracopoli NC, Clark WH Jr, Tucker MA. Increased risk of pancreatic cancer in melanoma-prone kindreds with p16INK4 mutations. N Engl J Med 1995;333:970–4

356

66

Elder DE, Goldman LI, Goldman SC, Greene MH, Clark WH Jr. Dysplastic nevus syndrome: a phenotypic association of sporadic cutaneous melanoma. Cancer 1980;46:1787–94

347

67

Jiang H, Lin JJ, Su ZZ, Goldstein NI, Fisher PB. Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 1995;11:2477–86

346

68

Stern RS, Nichols KT, Va¨keva¨ LH. Malignant melanoma in patients treated for psoriasis with methoxsalen (psoralen) and ultraviolet A radiation (PUVA). The PUVA Follow-Up Study. N Engl J Med 1997;336:1041–45

345

69

Krag DN, Meijer SJ, Weaver DL, Loggie BW, Harlow SP, Tanabe KK, Laughlin EH, Alex JC. Minimal-access surgery for staging of malignant melanoma. Arch Surg 1995;130:654–8

344

70

Veronesi U, Adamus J, Bandiera DC, Brennhovd O, Caceres E, Cascinelli N, Claudio F, Ikonopisov RL, Javorski VV, Kirov S, Kulakowski A, Lacour J, Lejeune F, Mechl Z, Morabito A, Rode´ I, Sergeev S, van Slooten E, Szczygiel K, Trapeznikov NN, Wagner RI. Delayed regional lymph node dissection in stage I melanoma of the skin of the lower extremities. Cancer 1982;49:2420–30

344

71

Marchand M, van Baren N, Weynants P, Brichard V, Dre´no B, Tessier MH, Rankin E, Parmiani G, Arienti F, Humblet Y, Bourlond A, Vanwijck R, Lie´nard D, Beauduin M, Dietrich PY, Russo V, Kerger J, Masucci G, Ja¨ger E, De Greve J, Atzpodien J, Brasseur F, Coulie PG, van der Bruggen P, Boon T. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int J Cancer 1999;80:219–30

342

72

Gogas H, Ioannovich J, Dafni U, Stavropoulou-Giokas C, Frangia K, Tsoutsos D, Panagiotou P, Polyzos A, Papadopoulos O, Stratigos A, Markopoulos C, Bafaloukos D, Pectasides D, Fountzilas G, Kirkwood JM. Prognostic significance of autoimmunity during treatment of melanoma with interferon. N Engl J Med 2006;354:709–18

334

73

Eisen T, Ahmad T, Flaherty KT, Gore M, Kaye S, Marais R, Gibbens I, Hackett S, James M, Schuchter LM, Nathanson KL, Xia C, Simantov R, Schwartz B, PoulinCostello M, O’Dwyer PJ, Ratain MJ. Sorafenib in advanced melanoma: a Phase II randomised discontinuation trial analysis. Br J Cancer 2006;95:581–6

331

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100 CITATION CLASSICS IN THE MELANOMA LITERATURE

TABLE 2. (Continued ) Rank

Article

Times Cited

74

Greene MH, Clark WH Jr, Tucker MA, Kraemer KH, Elder DE, Fraser MC. High risk of malignant melanoma in melanoma-prone families with dysplastic nevi. Ann Intern Med 1985;102:458–65

331

75

Gershenwald JE, Colome MI, Lee JE, Mansfield PF, Tseng C, Lee JJ, Balch CM, Ross MI. Patterns of recurrence following a negative sentinel lymph node biopsy in 243 patients with stage I or II melanoma. J Clin Oncol 1998;16:2253– 60

330

76

Glass AG, Hoover RN. The emerging epidemic of melanoma and squamous cell skin cancer. JAMA 1989;262:2097–100 Schultz RM, Silberman S, Persky B, Bajkowski AS, Carmichael DF. Inhibition by human recombinant tissue inhibitor of metalloproteinases of human amnion invasion and lung colonization by murine B16-F10 melanoma cells. Cancer Res 1988;48:5539–45

330 (Review)

78

Bedikian AY, Millward M, Pehamberger H, Conry R, Gore M, Trefzer U, Pavlick AC, DeConti R, Hersh EM, Hersey P, Kirkwood JM, Haluska FG; Oblimersen Melanoma Study Group. Bcl-2 antisense (oblimersen sodium) plus dacarbazine in patients with advanced melanoma: the Oblimersen Melanoma Study Group. J Clin Oncol 2006;24:4738–45

328

79

Morton DL, Foshag LJ, Hoon DS, Nizze JA, Famatiga E, Wanek LA, Chang C, Davtyan DG, Gupta RK, Elashoff R. Prolongation of survival in metastatic melanoma after active specific immunotherapy with a new polyvalent melanoma vaccine. Ann Surg 1992;216:463–82 Claffey KP, Brown LF, del Aguila LF, Tognazzi K, Yeo KT, Manseau EJ, Dvorak HF. Expression of vascular permeability factor/vascular endothelial growth factor by melanoma cells increases tumor growth, angiogenesis, and experimental metastasis. Cancer Res 1996;56:172–81 Hendrix MJ, Seftor EA, Hess AR, Seftor RE. Vasculogenic mimicry and tumourcell plasticity: lessons from melanoma. Nat Rev Cancer 2003;3:411–21

328

77

80

81

1292

330

327

326 (Review)

82

Overgaard J, Gonzalez Gonzalez D, Hulshof MC, Arcangeli G, Dahl O, Mella O, Bentzen SM. Randomised trial of hyperthermia as adjuvant to radiotherapy for recurrent or metastatic malignant melanoma. European Society for Hyperthermic Oncology. Lancet 1995;345:540–3

323

83

Tahara H, Zeh HJ third, Storkus WJ, Pappo I, Watkins SC, Gubler U, Wolf SF, Robbins PD, Lotze MT. Fibroblasts genetically engineered to secrete interleukin 12 can suppress tumor growth and induce antitumor immunity to a murine melanoma in vivo. Cancer Res 1994;54:182–9

318

84

Balch CM, Soong SJ, Milton GW, Shaw HM, McGovern VJ, Murad TM, McCarthy WH, Maddox WA. A comparison of prognostic factors and surgical results in 1,786 patients with localized (stage I) melanoma treated in Alabama, USA, and New South Wales, Australia. Ann Surg 1982;196:677–84

316

85

Bale SJ, Dracopoli NC, Tucker MA, Clark WH Jr, Fraser MC, Stanger BZ, Green P, Donis-Keller H, Housman DE, Greene MH. Mapping the gene for hereditary cutaneous malignant melanoma-dysplastic nevus to chromosome 1p. N Engl J Med 1989;320:1367–72

315

86

Vile RG, Nelson JA, Castleden S, Chong H, Hart IR. Systemic gene therapy of murine melanoma using tissue specific expression of the HSVtk gene involves an immune component. Cancer Res 1994;54:6228–34

311

87

Balch CM, Soong SJ, Murad TM, Ingalls AL, Maddox WA. A multifactorial analysis of melanoma: III. Prognostic factors in melanoma patients with lymph node metastases (stage II). Ann Surg 1981;193:377–88

305

88

Kraemer KH, Lee MM, Andrews AD, Lambert WC. The role of sunlight and DNA repair in melanoma and nonmelanoma skin cancer. The xeroderma pigmentosum paradigm. Arch Dermatol 1994;130:1018–21

305

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TABLE 2. (Continued ) Rank

Article

Times Cited

89

Veronesi U, Cascinelli N, Adamus J, Balch C, Bandiera D, Barchuk A, Bufalino R, Craig P, De Marsillac J, Durand JC. Thin stage I primary cutaneous malignant melanoma. Comparison of excision with margins of 1 or 3 cm. N Engl J Med 1988;318:1159–62

304

90

Zhang XD, Franco A, Myers K, Gray C, Nguyen T, Hersey P. Relation of TNFrelated apoptosis-inducing ligand (TRAIL) receptor and FLICE-inhibitory protein expression to TRAIL-induced apoptosis of melanoma. Cancer Res 1999;59:2747–53

304

91

Friedman RJ, Rigel DS, Kopf AW. Early detection of malignant melanoma: the role of physician examination and self-examination of the skin. CA Cancer J Clin 1985;35:130–51

304

92

Holman CD, Armstrong BK. Pigmentary traits, ethnic origin, benign nevi, and family history as risk factors for cutaneous malignant melanoma. J Natl Cancer Inst 1984;72:257–66

303

93

McGovern VJ, Mihm MC Jr, Bailly C, Booth JC, Clark WH Jr, Cochran AJ, Hardy EG, Hicks JD, Levene A, Lewis MG, Little JH, Milton GW. The classification of malignant melanoma and its histologic reporting. Cancer 1973;32:1446–57

301 (Review)

94

Hunder NN, Wallen H, Cao J, Hendricks DW, Reilly JZ, Rodmyre R, Jungbluth A, Gnjatic S, Thompson JA, Yee C. Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. N Engl J Med 2008;358:2698–703

300 (Case report)

95

Kittler H, Pehamberger H, Wolff K, Binder M. Diagnostic accuracy of dermoscopy. Lancet Oncol 2002;3:159–65

298

96

Bennett DC, Cooper PJ, Hart IR. A line of non-tumorigenic mouse melanocytes, syngeneic with the B16 melanoma and requiring a tumour promoter for growth. Int J Cancer 1987;39:414–8

297

97

Singh RK, Gutman M, Radinsky R, Bucana CD, Fidler IJ. Expression of interleukin 8 correlates with the metastatic potential of human melanoma cells in nude mice. Cancer Res 1994;54:3242–7

296

98

Greene MH, Clark WH Jr, Tucker MA, Elder DE, Kraemer KH, Guerry D IV, Witmer WK, Thompson J, Matozzo I, Fraser MC. Acquired precursors of cutaneous malignant melanoma. The familial dysplastic nevus syndrome. N Engl J Med 1985;312:91–7

294 (Review)

99

Thompson JF, McCarthy WH, Bosch CM, O’Brien CJ, Quinn MJ, Paramaesvaran S, Crotty K, McCarthy SW, Uren RF, Howman-Giles R. Sentinel lymph node status as an indicator of the presence of metastatic melanoma in regional lymph nodes. Melanoma Res 1995;5:255–60

293

100

Hoon DS, Wang Y, Dale PS, Conrad AJ, Schmid P, Garrison D, Kuo C, Foshag LJ, Nizze AJ, Morton DL. Detection of occult melanoma cells in blood with a multiple-marker polymerase chain reaction assay. J Clin Oncol 1995;13:2109–16

293

The most cited article in the top 100 was by Morton and colleagues, and it describes the early use of sentinel node mapping in malignant melanoma. This article was published in 1992 in the Archives of Surgery and was cited 2,384 times. The second most cited article was the 1969 article by Clark and colleagues published in Cancer Research. It details the histologic behavior of melanoma and has been cited 1,705 times. Breslow’s seminal article from 1970 on tumor depth was at number 3, and has been cited 1,554 times to date. The 2001 AJCC melanoma staging system was at number 4 with 1,339 citations, and the 2010 article from Flaherty and colleagues describing

improved survival rates with ipilimumab was at number 6 with 1,318 citations. The results of the Eastern Cooperative Oncology Groups Trials was cited 1,126 times and was number 8 in the most cited list. This was followed by number 9 by the seminal article on the BRAF inhibitor, vemurafenib, from the New England Journal of Medicine from 2011. This article has been cited 1,067 times. The article by Morton and colleagues featured at number 17 in the top 100, in which they focused on the difference in the outcome of sentinel node biopsy versus

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100 CITATION CLASSICS IN THE MELANOMA LITERATURE

TABLE 3. Top 50 Most Cited Articles With Their Citation Index Rank

Author

No. Citations Citation Index Rank

No. Citations Citation Index

1 2

Morton (1992)

2,384

91.6

26

Smith (1991)

544

Clark (1969)

1,705

22.6

27

Brose (2002)

536

56.5

3

Breslow (1970)

1,554

8.3

28

Lienard (1992)

532

30.6

4

Balch (2001)

1,476

5

Rosenberg (1988)

1,338

6

Hodi (2010)

1,318

7

Kirkwood (1996)

1,164

8

Balch (2001)

9 10

Chapman (2011) Flaherty (2010)

11

Rosenberg (1990)

12

Curtin (2005)

13

Allen (1953)

778

8.7

38

Lewis (1969)

448

28

14

Dudley (2005)

770

115.6

39

Weeraratna (2002)

449

47.6

15

Balch (2009)

709

287.5

40

Kirkwood (2000)

448

48.1

16

Gershenwald (1999)

701

68.9

41

Dudley (2008)

442

98.8

17 18

Morton (2006) Clark (1989)

697 687

126.3 18.8

42 43

Balch (1978) Morton (1968)

442 434

15 26.8

19

Albelda (1990)

679

35.3

44

Fidler (1975)

432

11.2

20

Atkins (1999)

674

38.7

45

Breslow (1975)

410

17.6

21

Rosenberg (1994)

671

38.6

46

Balch (1996)

406

42.4

22

Marchand (1999)

605

69

47

Clemente (1996)

406

17.7

23

Banchereau (2001)

573

72.7

48

Soengas (2003)

406

49.7

24

Clark (1978)

570

17.3

49

Livingston (1994)

393

27.8

25

Middleton (2000)

557

44.3

50

Attia (2005)

391

51.6

170

29

Rosenberg (1994)

517

31.7

Fang (2005)

516

89.6

535

31

Veronesi (1977)

500

10.7

95

32

Reintgen (1994)

498

37.7

1,126

123

33

Robert (2011)

496

271.7

1,067 1,014

563.3 362.5

34 35

Morton (1970) Morton (1999)

479 474

25.5 50.8

824

54.1

36

Curtin (2006)

473

86

796

125.6

37

Kirkwood (2001)

473

57.4

TABLE 4. Type and Level of Evidence of the Clinical Studies (n = 67) in the Top 100 Clinical Study Type

27.1

30

76.7

nodal observation, has been cited 297 times to date. An early report on the BRAF mutation in melanoma was described by Brose and colleagues at number 27. At 29, Rosenberg and colleagues report on the use of tumor

1294

Author

Number of Studies

Therapeutic

36

Level 1

13

Level 2

8

Level 3 Level 4

3 12

Diagnostic

8

Level 1

1

Level 2

5

Level 3

2

Prognostic

23

Level 1

2

Level 2 Level 3

19 2

necrosis factor alpha with interferon gamma and melphalan for isolated limb perfusion in melanoma. The article by Albertini and colleagues, detailing the use of radiolymphoscintigraphy in sentinel node biopsy was at 55 in the top 100 list. The prolongation of survival in metastatic melanoma by using the melanoma vaccine was described by Morton and colleagues at 79, and the article on adequate margins for melanoma excision by Veronesi and colleagues was at 89. Discussion Melanoma treatment has evolved significantly over the past 60 years, and this is reflected in the scientific literature. Better understanding of disease progression coupled with targeted immunologic therapies has given rise to improved survival rates. The top 100 articles in melanoma echoes the trends that have occurred in melanoma research over the past 60 years and also demonstrates the significant advances in research that have taken place.

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TABLE 5. Authors Who Contributed 3 or More Articles to the Top 100 Articles in Melanoma Author Kirkwood JM Balch CM

No. Citation Classics 10

Position on Author List First author-3, tenth-2 eleventh-1, fourteenth-1, nineteenth-1, last-2

9

First author-7, seventh-1, eighth-1

Clark WH Jr

9

First author-3, second-2, fourth-1, fifth-1, last-2

Morton DL

8

First author-5, thirteenth-1, seventeenth-1, last-1

Rosenberg SA

8

First author-4, last-4

Cascinelli N

7

First author-1, second-1, fifth-1, sixth-3, last-1

Reintgen DS

7

First author-1, fifth-1, ninth-1, tenth-1 eleventh-1, fourteenth-1, last-1

Soong SJ

7

Second author-4, third-3

Yang JC Elder DE

7 6

Second author-2, third-2, sixth-1, ninth-2 First author-1, second-1, third-1, fourth-1, fifth-1, ninth-1

Mihm MC Jr

6

Second author-2, tenth-1, sixteenth-1, last-2

Ross MI

6

Eighth author-1, ninth-1, fifteenth-1, seventeenth-1, last-2

Thompson JF

6

First author-1, second-2, fourth-2, eighteenth-1

Topalian SL

6

Third author-1, fourth-1, fifth-2, eighth-1, last-1

Atkins MB

5

First author-1, second-1, fourth-1, fifth-1, eleventh-1

Cochran AJ,

5

Third author-1, sixth-1, eighth-1, last-2

Flaherty KT Gershenwald JE

5 5

First author-1, third-1, fifth-1, twelfth-1, twenty-seventh-1 First author-2, second-1, third-1, eighth-1

Dre´no B

4

Fifth author-1, fifth-1, eleventh-1, last-1

Ernstoff MS

4

Third author-1, sixth-2, tenth-1

Fraser MC

4

Second author-1, fifth-1, last-2

Morabito A

4

Second author-1, fifteenth-2, last-1

Lotze MT

4

Second author-1, eighth-2, last-1

Restifo NP

4

Sixth author-1, eleventh-1, twelfth-2

Sosman JA White DE

4 4

Third author-1, fifth-1, sixth-1, eighteenth-1 Ninth author-1, nineteenth-1, last-2

Adamus J

3

Second author-2, third-1

Bandiera DC

3

Third author-2, fifth-1

Chapman PB

3

First author-2, last-1

Coit DG

3

Sixth author-1, ninth-1, thirteenth-1

Elashoff R

3

Fourth author-1, fifth-1, last-1

Fidler IJ

3

First author-1, last-2

Foshag LJ Gore M

3 3

Second author-1, seventh-1, eighth-1 Fourth author-1, fifth-1, seventh-1

Hart IR

3

Third author-1, last-2

Herlyn M

3

Sixth author-1, eighth-1, last-1

Ikonopisov RL

3

Second author-1, eighth-2

Kammula US

3

Sixth author-1, eighth-1, ninth-1

Karakousis CP

3

Fifth author-1, eighth-1, tenth-1

Kraemer KH

3

First author-1, fourth-1, fifth-1

Lebbe C Lejeune F

3 3

Seventh author-1, thirteenth-1, nineteenth-1 Thirteenth author-2, last-1

Lie´nard D

3

First author-1, thirteenth-2

Lyman GH

3

Tenth author-1, eighteenth-1, last-1

Maddox WA

3

Last author-3

Murad TM

3

Second author-1, second-1, sixth-1

O’Day SJ

3

Second author-1, fourth-1, seventh-1

Parkinson DR

3

Sixth author-1, seventh-1, ninth-1

Pehamberger H

3

Second author-1, third-1, last-1

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100 CITATION CLASSICS IN THE MELANOMA LITERATURE

TABLE 5. (Continued ) Author

No. Citation Classics

Position on Author List

Robert C

3

First author-1, third-1, eighth-1

Schadendorf D

3

Ninth author-1, thirteenth-1, fifteenth-1

Seipp CA

3

Seventh author-1, eighth-1, last-1

Sherry RM

3

Third author-1, fourth-1, seventh-1

Smith TJ

3

Fourth author-1, sixth-1, seventh-1

Sondak VK

3

Third author-1, fourth-1, last-1

Thompson JA

3

Ninth author-1, twelfth-1, seventeenth-1

Tucker MA Veronesi U

3 3

Third author-3 First author-3

Weber JS

3

Fifth author-1, sixth-1, twenty-fourth-1

Many important articles on melanoma have failed to make it to the top 100 however. No articles from Pigment Cell and Melanoma Research contributed to the top 100 despite publishing high-quality articles that focus on melanoma research. Melanoma Research had 1 solitary article in the top 100 most cited list. The reason that many seemingly landmark articles have failed to make it to the top 100 may be due to a phenomenon called “obliteration by incorporation.”6 This occurs, as over time, when many classic articles have become such common knowledge that it is not deemed appropriate to cite them. This would indicate that the number of citations that an article receives is not reflective of its overall importance to the scientific community. An important article on melanoma that failed to make it to the top 100 is the 1979 article by Balch and colleagues19 in which they looked at tumor thickness as a guide to the surgical management of stage I disease. This article has received 292 citations to date and just narrowly missed out on being included in the top 100. Another much cited article that just missed out was the 2005 Lancet review article entitled “Cutaneous melanoma” by Thompson and colleagues,20 which was cited 291 times. Seven articles in the top 100 report on the sentinel node biopsy for melanoma, which was first described by Morton and colleagues in 1992 for patients with melanoma. All 7 of these articles were published from 1992 to 2006, and this further highlights the significance of the sentinel node biopsy as a prognostic tool, in that all the citations were received in just 14 years.

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The recent discovery of BRAF mutations and the survival benefit of ipilimumab therapy are recognized milestones in melanoma research. The 2 ipilimumab articles in the top 100 have been cited 1,814 times in just 3 years, whereas the 3 articles on BRAF have been cited 2,617 times in 11 years. We found that in our top 100, 78% of the articles were more than 10 years old, whereas 36% were more than 20 years old. The reason that almost two-thirds of articles in the top 100 were relatively recently published may be explained by the overall increase in published articles and the widespread internet use for literature searches within the past 20 years.12 It has been proposed that the most important seminal articles in melanoma may be located in the reference list of the most cited articles.7,21 However, it has been argued that the older articles actually are, the greater their likelihood of attaining more citations based on the fact that they have had a longer citable period.9 By and large, scientific articles are not cited for up to 2 years after publication and typically reach a maximum after 3 to 10 years, after which they continue to be cited but at a lesser rate.18 To overcome this potential bias for older articles, we calculated the citation index of the top 50 articles in the list of 100 most cited articles. This is the number of citations divided by the number of years since publication and is often used instead of the total number of citations.14 The article with the highest citation index was by Chapman and colleagues and was only published in 2011. In fact, the top 10 articles in terms of citation

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index were all published since 2001 (Table 3). This would indicate that the citation index is more favorable to recent articles rather than older ones. The amount of published works increases annually, and recent research articles are more likely to cite other recent articles in their work instead of older ones, which may have been obliterated by incorporation. This in turn may skew the citation index in favor of more recent articles. The top 10 articles in the citation index list contained articles from just 2 journals—the New England Journal of Medicine and the Journal of Clinical Oncology. Regarding the article type, we found that 85% of articles were original research articles. This is similar to other studies looking at the top 100 citation classics in different fields.7,14 All of the 12 reviews in the top 100 originated from the United States and 5 of these were more than 24 year old. Fifteen articles in the top 100 originated in countries where English is not the primary language (Italy, Belgium, Austria, Denmark, France, and Greece). The remaining 85 articles came from English-speaking countries (United States, United Kingdom, Australia, and New Zealand). The top 100 most cited articles in melanoma research provide a fascinating understanding of the history and development of trends in current melanoma management. The most influential articles have been identified, and these are the articles that have had the most impressive impact on the field of melanoma research. The United States provided the majority of the articles in the top 100, yet this is not surprising considering that they lead the rankings in all 20 of the scientific disciplines according to the ISI.9,17 Also, American authors have a tendency to cite local articles instead of international articles,12 but this has also shown to be the case with articles originating from the United Kingdom.22 It has been reported that stringency and consistency of the peer-review process varies considerably between journals.23 Some studies have found that journals favor authors located in the same country as the journal with some revealing a seemingly strong degree of preferential attachment to the United States.24,25 This American bias may be

anecdotal as the peer-review process is typically blinded. The United States does actually produce the greatest amount of articles in the English language, therefore it is not surprising that the majority of published works originate here because of the sheer volume of articles. In our study, we observed that 74% of articles originated from the United States, and this highlights the impact that this country has made on the field of melanoma research. This is in part due to the sheer number of large well-funded cancer centers that produce highquality research. Several limitations do exist with a study of this nature. The number of citations an article receives relies not only on the quality of the work but also on several other factors.26 Other intrinsic biases can interfere with the creation of any list of top 100 most cited articles. These include journal bias, language bias toward English, in-house bias, self-citation, and omission bias by purposely failing to cite important articles by competitors.8 “Incomplete citing” is often performed to persuade the reader instead of giving credit to those who were most influential on their body of work. To the best of our knowledge, this has been the first report of a citation analysis of the melanoma literature. The top 100 list generated from our analysis not only identifies the landmark articles that have had the most influence on melanoma research but also acknowledges the most prolific authors and institutions that have contributed articles to the list. The most cited list also provides information to aspiring authors as to what it takes to write a classic article. To produce such a body of work, a novel innovation, idea, or observation must be found that has an enduring effect on melanoma treatment. The measurement of scientific quality is certainly not based on the number of citations. However, the more times an article has been referenced is a measure of its influence on the scientific community as a whole. Every article in the top 100 most cited articles has had a significant impact on melanoma research, and these are the articles that will most likely be remembered the most.

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100 CITATION CLASSICS IN THE MELANOMA LITERATURE

References 1. Urteaga O, Pack G. On the antiquity of melanoma. Cancer 1966;19: 607–10. 2. Laennec RTH. Extrait au memoire de M Laennec, sur les melanoses. Vol. 1. Bull L’Ecole Societie de Medicine: Paris, 1812; p. 24.

15. Dubin D, Häfner AW, Arndt KA. Citation classics in clinical dermatologic journals: citation analysis, biomedical journals, and landmark articles, 1945-1990. Arch Dermatol 1993;129:1121–9.

3. Roguin A. Rene Theophile Hyacinthe Laennec: the man behind the stethoscope. Clin Med Res 2006;4:230–5.

16. Baltussen A, Kindler CH. Citation classics in critical care medicine. Intensive Care Med 2004;30:902–10.

4. Garfield E. The impact factor and its rightful use [in German]. Anaesthesist 1998;47:439–40.

17. Institute for Scientific Information. Science citation index expanded 1946–2006. Available at: http://www.wokinfo.com. Accessed November 1, 2013.

5. Garfield E. Journal impact factor: a brief review. Can Med Assoc J 1999; 161:979–80. 6. Garfield E. 100 citation classics from the Journal of the American Medical Association. J Am Med Assoc 1987;2:52–9. 7. Paladugu R, Schein M, Gardezi S, Wise L. One hundred citation classics in general surgical journals. World J Surg 2002;26: 1099–105. 8. Baltussen A, Kindler CH. Citation classics in anesthetic journals. Anesth Analg 2004;98:443–51. 9. Kelly JC, Glynn RW, O’Briain DE, Felle P, et al. The 100 classic papers of orthopaedic surgery: a bibliometric analysis. J Bone Joint Surg Br 2010;92:1338–43. 10. Bosker BH, Verheyen CC. The international rank order of publications in major clinical orthopaedic journals from 2000 to 2004. J Bone Joint Surg 2006;88-B:156–8. 11. Fenton JE, Roy D, Hughes JP, Jones AS. A century of citation classics in otolaryngology-head and neck surgery journals. J Laryngol Otol 2002; 116:494–8. 12. Yoon DY, Yun EJ, Ku YJ, Baek S, et al. Citation classics in radiology journals: the 100 top-cited articles, 1945-2012. AJR Am J Roentgenol 2013;201:471–81. 13. Loonen MP, Hage JJ, Kon M. Value of citation numbers and impact factors for analysis of plastic surgery research. Plast Reconstr Surg 2007; 120:2082.

1298

14. Loonen MP, Hage JJ, Kon M. Plastic surgery classics: characteristics of 50 top cited articles in four plastic surgery journals since 1946. Plast Reconstr Surg 2008;121:320–7.

18. Bohannon RW, Roberts D. Core journals of rehabilitation: identification through index analysis. Int J Rehabil Res 1991;14:333–6. 19. Balch CM, Murad TM, Soong SJ, Ingalls AL, et al. Tumor thickness as a guide to surgical management of clinical stage I melanoma patients. Cancer 1979;43:883–8. 20. Thompson JF, Scolyer RA, Kefford RF. Cutaneous melanoma. Lancet 2005;365:687–701. 21. Picknett T, Davis K. The 100 most-cited articles from JMB. J Mol Biol 1999;293:171–6. 22. Campbell FM. National bias: a comparison of citation practices by health professionals. Bull Med Libr Assoc 1990;78:376–82. 23. Mabe M. The growth and number of journals. Serials 2003;16:191–7. 24. Ernst E, Kienbacher T. Chauvinism. Nature 1991;352:560. 25. Link AM. US and non-US submissions: an analysis of reviewer bias. JAMA 1998;280:246–7. 26. Weale AR, Bailey M, Lear PA. The level of noncitation of articles within a journal as a measure of quality: a comparison to the impact factor. BMC Med Res Methodol 2004;4:14.

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