Oral communication at the International Society for Scientometrics and Informatrics Conference, held in Wuhan (China), 16-20 October, 2017.

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Sleeping Beauty awakened by self-citation of a review:
A case study of Judah Folkman hypothesis on angiogenesis.
16th Int. Conf. on Scientometrics & Informetrics
Philippe GORRY, MD-PhD., Asso. Prof.
Adil EL AICHOUCHI, MSc. PhD student
Wuhan University, June 29
Oct. 16-20th, 2017
Health Sciences College, Medical School & Dpt of Humanities & Social Sciences,
Research Unit in Theoritical & Applied Economics - CNRS UMR 5113

2. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
Introduction (1)
• Delayed recognition paper or Sleeping-beauty in science
• Definitions
• Delayed recognition, (Garfield, 1980), premature or resistant discoveries
(Burel, 2005; Braun, 2010), sleeping beauty (Van Raan (2004):
• “articles that go unnoticed (“sleeps”) for a long period of time and then,
suddenly, receives a lot of citations by a “prince” (another article).”
• Average-based criteria (Van Raan et al, 2014)
• depth of sleep: at most 1 citation/y (deep sleep) or between 1 & 2 citations/y
(less deep sleep)
• length of the sleep: between 5 & 10 years
• awakening intensity: 15 citations/y for 4 years
• Quartile-based criteria (Costas el al., 2010 & 2011)
• Parameter-free index: The Beauty coefficient (B)” (Ke et al, 2015)
• Others: K-value (teixera et al., 2017), Citation-angle (Yea le., 2017)

3. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
• Tumor angiogenesis
• Angiogenesis (the development of vessels) is essential
for tumor growth and metastasis,
• controlling tumor-associated angiogenesis is a promising tactic in
limiting cancer progression = Angiogenesis inhibitor
• Judah Folkman
• Father of tumor angiogenesis research
• developed new ground-breaking concepts and methodologies
• his laboratory trained numerous scientists
• received more the 150 awards and honours from 11 nations
• elected to the National Academy of Sciences, the Institute of
Medicine and to the President’s Cancer Advisory Board
• But his ideas were met with a lot of scepticism, criticism and
rejection
• Folkman liked to reflect on the resistance he faced by saying:
If your idea succeeds, everybody says you’re persistent,
if it doesn’t succeed you’re stubborn”
Introduction (2)

4. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
Aims & Objectives
• Aims
• Explanations for sleeping beauties is under explored
• Reasons for sleeping, explanations of awakening, role of the Prince …
• Identify new explanatory variables or control for (scientific field, time period,
journal, ...)
• Necessary to better understand scientific knowledge
• Objectives
• To what extend the phenomenon of delayed recognition have affected
Folkman’s
• analyze the scientific production of Folkman’s and the citation life of his
publications looking for sleeping beauties.
• If any SB, identify the relevant prince, and try to understand the reason for
delayed recognition and awakening mechanisms

5. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
Methods
• Quantitative approach = bibliometrics
• Literature search
• Databases: Scopus®
• Corpus (12/31/2015)
• 510 publications
• 116.703 citations
• Analysis
• Descriptive statistics: Built-in Scopus® functions & Excel®
• Co-publications network: VosViewer®
• Co-citations analysis: GEPHI ®
• RPYS analysis: CRExplorer® / RPYS online
- van Eck, N.J.&Waltman, L. (2010). Software survey:Vosviewer, a computer program for bibliometric mapping. Scientometrics, 84(2), 523–538.
- Bastian, M., et al., 2009. Gephi: an open source software for exploring and manipulating networks. In: International AAAI Conference on Weblogs
and Social Media, North America, March 2009 (ICWSM09).
- Thor, A., Marx, W., Leydesdorff, L., & Bornmann, L. (2016). Introducing CitedReferencesExplorer (CRExplorer): A program for reference
publication year spectroscopy with cited references standardization. Journal of Informetrics, 10(2), 503–515.
• Qualitative approach = historical analysis
• Literature review
• Judah Folkman biography
• History of Angiogenesis
• Interviews
• Researcher in tumor angiogenesis who met J. Folkman

6. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
0
5
10
15
20
25
0
20000
40000
60000
80000
100000
120000
1953
1956
1959
1962
1965
1968
1971
1974
1977
1980
1983
1986
1989
1992
1995
1998
2001
2004
2007
2010
2013
Publications
number
Citations
number
Results (1)
• Judah Folkman’s scientific production
• Folkman published his 1st paper in 1953
• He published 396 articles, 41 reviews, and some 76 monographs
• 9.658 papers/year with a maximum of 23 papers in 1998
• His work was rapidly recognized (675 total citations in 1970 for 26 publications);
• Until 2015, his work was cited more than 116,700 times
Folkman’s publications and citations

7. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
Results (2)
• Judah Folkman’s scientific production
• he published in various disciplines:
• multidisciplinary, medicine, surgery, oncology, pathology,
biochemistry
• in more than 160 different journals
Top journals where Folkman published the most.
Rank Source Title
Publications
number
SJR2015
1 Proc. Natl. Acad. Sci. USA 26 6.863
2 Cancer Research 21 5.372
3 Journal of The National Cancer Institute 17 6.192
4 Science 16 13.217
5 Journal of Pediatric Surgery 15 0.802
6 Nature 14 21.936
7 American Journal of Pathology 13 2.653
8 Annals of Surgery 12 4.503
9 New England Journal of Medicine 12 14.619

8. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
Results (3)
• Judah Folkman’s scientific production
• Folkman collaborated with a large number of researchers (n>160)
• His main collaborators were his fellows or technician:
• Yueng Shing, Evelyn Flynn, Robert D’Amato, and Michael O’Reilly.
Network of J. Folkman co-publications

9. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
Results (4)
• Calculation of the “Beauty coefficient”
• using equation
• for all of Folkman’s papers
!
"#$
"% Ctm − C0
tm
t + C0 − Ct
max 1, Ct
Top 5 Folkman delayed papers ranked by decreasing B index.
Authors Year Journal Citations B coefficient
Folkman J. 1971 New England Journal of Medicine 6279 1052,17
Folkman J.
1972 Annals of Surgery 838 175,04
Folkman J. Cole P. Zimmerman S.
1966 Annals of Surgery 167 141
Folkman J. Hochberg M.
1973 Journal of Experimental Medicine 449 137,22
Gimbrone Jr. M.A. Aster R.H. Cotran
R.S. Corkery J. Jandl J.H. Folkman J. 1969 Nature 138 121,59

10. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
Results (5)
• A single sleeping beauty (1)
• Only one top sleeping beauty
• Title : “Tumor Angiogenesis:
Therapeutic implications” ,
• Journal: New England Journal of
Medicine.
• Year of publication: 1971
• Type: review
• Beauty coefficient = 1052.17
• During its first 23 years, the paper
was cited 113 times (5 citations/year)
Total Citations Average per Year
6279 139,53

11. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
0
5
10
15
20
25
0
100
200
300
400
500
600
1953
1956
1959
1962
1965
1968
1971
1974
1977
1980
1983
1986
1989
1992
1995
1998
2001
2004
2007
2010
2013
Publications
dt=22.54
(tm=2012, Ctm=531)
Citations number
• A unique sleeping beauty (2)
• Citation history of Folkman’s sleeping beauty
Length of sleep
23 years
Depth of sleep
(4.7 citations/year)
Awakening intensity
(293.6 citations/y)
Results (6)

12. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
• Identifying the Prince and the kiss of life (1)
• Top publications citing Folkman’s main paper
• between 1993 and 1997
Results (7)
Rank Authors Source Year
Citations
number
Co-citations
with SB
Ratio
citations/co-
citations
1 Chen, C.S., et al. Science 1997 3127 6 0,001
2
O'Reilly, M.S., Holmgren,
L., Shing, Y., (...), Sage,
E.H., Folkman, J.
Cell 1994 2810 504 0,179
3 Folkman, J. N. E. J. M. 1995 1992 313 0,157
4
Holmgren, L., O'Reilly,
M.S., Folkman, J.
Nature
Med.
1995 1389 244 0,156
5 Isner, J.M., et al. Lancet 1996 792 91 0,114
6 Woodhouse, E.C., et al. Cancer 1997 587 0 0

13. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
• Identifying the Prince and the kiss of life (2)
• Co-citations network between Folkman landmark paper & the prince’ paper
Results (8)
Prince paper citations:
O’Reilly, M.S. et al., 1971
Sleeping-beauty paper
citations
Co-citations number:
504
GEPHI®

14. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
• Identifying the Prince and the kiss of life (3)
• Citations curves of the top 4 publications citing Folkman’s main paper
Results (9)
0
2000
4000
6000
8000
10000
12000
0
100
200
300
400
500
600
1970
1973
1976
1979
1982
1985
1988
1991
1994
1997
2000
2003
2006
2009
2012
2015
Publications numberCitations number
dt = 22.54
(tm=2012, Cm=531)

15. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
• Identifying the Prince and the kiss of life (4)
• Reference publication Year Spectroscopy.
• The prince is:
• M.S. O’Reilly (1st author, post-doc)
• J. Folkman (corresponding author)
• The kiss of life is:
• an experimental paper published in Cell
• about the discovery of noval angiogenesis inhibitor
• Folkman’s hypothesis confirm
Results (10)
RPYS online

16. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
• Discussion
• About Folkman’s research work recognition
• Folkman landmark paper suffered from delayed recognition.
• It was a theoritical paper, waiting for experimental proof of concept
• with the advance of molecular biology
• gene cloning technology was commercialized in 1976, the first human gene isolated was
the insulin gene in 1978 and the 1st human oncogene cancer in 1976
• Folkman has been the subjected of a science controversy
• About research contract sponsored by Monsanto
• which may have affected is academic credit
• Folkman kept citing his own paper after all those years demonstrates his
phenomenal persistence and belief in the importance of his theory
• Folkman’s SB is the paper that initiated the field of tumor angiogenesis r
• In general about sleeping-beauties
• Folkman SB does not fulfil Van Raan’s criteria
• Our results challenges the common practice
• of excluding review paper
• of excluding self-citations
• To distangle between Prince candidate papers with suggest as indicator
• ratio between co-citations between the Sb and the Prince
• and overall citations of Prince candidate paper
• Importance of 1st author vs corresponding author
Discussion

17. Ph. Gorry, 16th ISSI, Wuhan, Oct. 16-20th, 2017
• Acknowledgments
• In collaboration with
• Adil El El Aichouchi, MSc in History of Sciences, Bordeaux
• This work is supported by
• A grant from the Bordeaux Consortium on vascular ageing (ATT-VIVA).
• Contact
• Philippe GORRY, MD-PhD, Asso. Prof. 1,2*
• Research Group in Theoretical & Applied Economy UMR CNRS 5113,
Avenue Leon Duguit, University of Bordeaux, 33608 Pessac, FR
• Health College, University of Bordeaux, 33076 Bordeaux, FR
• * : philippe.gorry@u-bordeaux.fr
• Profile page:
• http://www.linkedin.com/in/philippegorry
• http://gretha.u-bordeaux.fr/fr/members/gorry-philippe
Thank you for your attention