Annals of Medicine, 2013; 45: 532–538 © 2013 Informa UK, Ltd. ISSN 0785-3890 print/ISSN 1365-2060 online DOI: 10.3109/07853890.2013.850838

ORIGINAL ARTICLE

Bibliometric analysis of Nobelists’ awards and landmark papers in physiology or medicine during 1983–2012 Siqi Ye1, Rui Xing2, Jing Liu3 & Feiyue Xing1,4

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1Institute of Tissue Transplantation and Immunology, Department of Immunobiology, Jinan University, Guangzhou 510632, China, 2Life Sciences and Technology Base of Basic Science Grade 2011, Lanzhou University School of Life Sciences, Lanzhou 730000, China, 3Department of Stomatology, Jinan University School of Medicine, Guangzhou 510632, China, and 4Key Laboratory of Functional Protein

Research of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China

Abstract Aim. This study’s purpose was to determine if there was a relationship between Nobel Laureates’ awards and landmark papers and winning the Nobel Prize in Physiology or Medicine during 1983–2012. Methods. The 66 Nobelists’ awards and landmark papers in the period 1983–2012 were analyzed. Results. The results showed that the most Nobelists had won Gairdner, Lasker, Howitz or Wolf Award before they won Nobel Prize, indicating that Gairdner Award may be considered as a Nobel Prize’s wind vane. A small number of landmark papers were indeed published in low impact factor journals (10.5% below impact factor 5.0) and some of their citation were low (23.2% below 400 times). There were 61 of 76 landmark papers published in the journals of JCR partition 1, reaching 80%, but 2 of 76 landmark papers were even outside of JCR partition, demonstrating that JCR partition acts as a reciprocal supplement with impact factor and citation times. The test period of Nobel Prize was substantially between 10 to 30 years. There were 5 persons whose landmark papers were cited all above 6000 times to get Nobel Prize within the test period of ten years, suggesting that there is a trend of certain inverse ratio between the citation and the test period of Nobel Prize. Conclusion. These findings provide a new insight into the relationship among Nobel Laureates’ awards, landmark papers and Nobel Prize in Physiology or Medicine. Key words: Award, citation, impact factor, landmark papers, Nobel Prize, test period

Introduction Since 1901 when the first winners were named, Nobelists have become a generally recognized symbol of research excellence both by the scientific community and by the general public. Winning a Nobel Prize is the highest honor for scientists (1). A large number of journal papers have ‘Nobel’ or ‘Nobel

Key messages • The most cited papers published by some of Nobelists are not the ones for which they win the Nobel Prize. • The 5-year citation is of a comparatively evaluating merit, similar to the annual average citation. • The most cited papers for the Nobel Prize appear in a relatively short test period.

Prize’ in the title included in the data library (2). All of these prove the importance of the Nobel Prize and make it more attractive to us. The Nobel Prize in Physiology or Medicine is closely related to human diseases, for which it is paid more attention. In some cases, it may take a long time before the contribution gains consensus as Nobel-worthy, or its validity may need to be assessed through empirical verification or broad acceptance (3). In addition, no one has so far won the Nobel Prize in Physiology or Medicine twice in a lifetime. Some papers focus on the nationality, research institutions, age, and other aspects of Nobel Laureates, trying to find out the properties shared by Nobel Prize winners from multiple aspects (1–5). And after the promulgation of the Nobel Prize each year, there would be a lot of reviews about their prize-winning work. However, our interest involves Nobel Laureates’ awards and landmark papers. Our investigations focus on the Nobel Prize in Physiology or Medicine during the recent 30 years, 1983–2012. On the one hand, we conducted a statistical analysis on the prizes the Nobel Laureates had got before they won a Nobel Prize, so as to evaluate whether the Nobel Prize results could be predicted through the results of other major international awards. On the other hand, we examined impact factor frequency, citation and maximum citation frequency of the landmark papers published by Nobel Laureates, and time-span between international great awards and Nobel Prize or test period.

Correspondence: Dr. Feiyue Xing, Dr. Jing Liu, Department of Immunobiology, Jinan University, Guangzhou 510632, China. Fax: ⫹ 86 20-85220723. E-mail: [email protected]; [email protected] (Received 2 July 2013; accepted 27 September 2013)

Bibliometrics of Nobelists’ awards and landmark papers 533

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Materials and methods The analyzed data for this paper were based on 66 Nobelists’ awards and landmark papers in the period 1983–2012. Within this period, Nobel Prizes in Physiology or Medicine were shared by two or more researchers. Thus, a total of 30 Prizes had been given to 66 scientists. The most reliable data on Nobel Laureates are displayed on the official web site of the Nobel Prize (http:// www.nobelprize.org/). Our data mainly came from it (2). Scientific publications seem to provide the best available basis for evaluating research output (6,7). It is important to analyze the relationship between Nobelists’ awards and landmark papers so as to find out its novel regularities and tendencies. At present, journals’ impact factor (IF), published by Journal Citation Reports (JCR), and JCR partition, issued by the Chinese Academy of Sciences, allow us to compare and evaluate the quality of journals (8). Based on journals’ IF, the JCR partition is divided into four areas. According to sequences of journal IF, the top 5% (including 5%) of the journals gets into partition 1, the top 5%–20% (including 20%) of the journals into partition 2, the top 20%–50% (including 50%) of the journals into partition 3, and the remaining 50% into partition 4. By using Google Scholar, we analyzed these papers’ cited frequencies from different points of view, including the citations within 5 years after the landmark papers were published, the average citations per year from the time of Nobelists’ publishing the papers to obtaining Nobel Prize, the total citations from the time of Nobelists’ publishing the papers to 10 March 2013, and the maximum citations during the period from the time of Nobelists’ publishing the papers to 10 March 2013. Therefore, we examined the impact factor and citation of the landmark papers which were associated with the prize-winning work done by Nobel Laureates. And all the data for 66 Nobel Prize winners in physiology or medicine from 1983 to 2012 were compared to explore the relationship between famous international awards won by Nobelists and Nobel Prize, and the correlation between the test period of the Nobel Prize and citation. There are many very influential scientific awards beside the Nobel Prize, such as the Gairdner Foundation International Award, the Lasker Awards, the Wolf Prizes, and the Louisa Gross Horwitz Prize. Through the statistical analysis of the prizes Nobelists got before winning the Nobel Prize, the predictability of Nobel Prize results on the basis of the four science awards were obtained. To ensure accuracy of the analyzed data, awards of Nobel Laureates were collected from the official website of the four international science awards.

Figure 1. Prize frequency distribution of Nobel Laureates in physiology or medicine, 1983–2012.

Impact factor of Nobelists’ landmark papers Our greater interest is in Nobel Laureates’ landmark papers that are the key basis for them to win the prize. The Nobel Committee usually cites the key papers on which the award was based in their press release each year. These papers are the ones that should be included as landmark papers. Alfred Nobel told in his suicide note that the Nobel Prize in Physiology or Medicine only rewards people who have made discoveries or inventions, which encourage the original innovation, rewarding a historic breakthrough from 0 to 1. Scientific research is an ongoing work, and every Nobelist made continuous contribution in their field. But only one or two or three key papers can represent the real breakthrough research (http://www.nobelprize.org/alfred_ nobel/will/). Therefore, we collected 82 landmark papers of the award-winning achievements written by 66 Nobel Laureates in Physiology or Medicine ranging from 1983 to 2012. According to the data, 66 Nobel Laureates had 82 landmark papers, but 6 of them had missing statistics due to some reasons such as publication closed down. Consequently, the number of analyzed landmark papers was 76. We analyzed these papers’ impact factor issued by JCR in 2011. The impact factor of all journals was the 5-year average impact factor from 2007 to 2011.

Results Statistical analysis of Nobelists’ awards As shown in Figure 1, in the period 1983–2012, 46 Nobel Laureates also won a Gairdner Award. And there were 38 Nobel Laureates who had won Lasker Awards. Almost 70% of the 66 Nobel Laureates had obtained the Gairdner Award before they won the Nobel Prize. The data draw more attention to the Gairdner Award. Thus we further collected data to see the time-span between winning a Gairdner Award and a Nobel Prize. There were 32 scientists who had won a Nobel Prize within 10 years after winning a Gairdner Award (Figure 2). This proportion was as high as 70%, sufficient to illustrate the predictability of Nobel Prize results based on results of a Gairdner Award. Most Nobel Prize winners once won the famous international awards for their outstanding work which had been highly recognized a few years before winning Nobel Prize.

Figure 2. Time-span of the winning of a Gairdner Award and a Nobel Prize frequency distribution of Nobel Laureates in physiology or medicine, 1983–2012.

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S. Ye et al. Table I. Frequency distribution of all Nobel Laureates’ landmark papers in physiology or medicine, 1983–2012.

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Name of journal

Figure 3. Landmark papers’ impact factor frequency distribution for Nobel Laureates in physiology or medicine, 1983–2012. 0: not included in SCI.

As shown in Figure 3, 45 landmark papers (60%) were published in journals whose impact factors were greater than 30. According to the JCR partition of the journals publishing landmark papers, there were 61 landmark papers (80%) published in JCR partition 1 (Figure 4). In addition, 6 of 76 papers were published in journals whose impact factors were below 5, and 2 of 61 papers were out of Science Citation Index (SCI), suggesting that some wonderful landmark papers may appear in journals with low impact factor. Altogether 82 landmark papers written by Nobelists were published in 24 different journals and one record of a meeting. According to the statistics in Table I, there were 23 papers published in Nature, 11 papers in Cell, 6 papers in Science, and, surprisingly, 6 papers in Journal of Biological Chemistry. Therefore, the landmark papers written by Nobelists are not always published in the most top-rank journals, of which Journal of Biological Chemistry can be taken as a typical paradigm to support this finding.

Citation of Nobel Laureates’ landmark papers There was a viewpoint that prizes in physiology or medicine seemed to depend more often on practical application and less on highly cited ‘discoveries’ than those in physics and chemistry. Citation data were even less predictive of Nobel Prizes in Physiology or Medicine than in physics and chemistry (7). For this reason, we further collected and analyzed citation frequencies of the landmark papers from different points of view below.

Figure 4. Landmark papers’ partition frequency distribution for Nobel Laureates in physiology or medicine, 1983–2012. 0: not included in SCI.

Cell Nature Science Proceedings of the National Academy of Sciences of the United States of America Lancet Journal of Biological Chemistry Journal of Experimental Medicine Genetics Developmental Biology Journal of Embryology & Experimental Morphology Journal of Physics C: Solid State Physics EMBO Journal Molecular and Cellular Biology Bacteriological Reviews Pharmacological Reviews Journal of Pharmacy and Pharmacology Journal of Cell Biology Journal of Cyclic Nucleotide Research Biochimica et Biophysica Acta New England Journal of Medicine Journal of the American Medical Association Cancer Research Biochemical Pharmacology Annales d’immunologie the 1951 Cold Spring Harbor Symposia on Quantitative Biology

Number of papers

Impact factor

11 23 6 10

34.929 35.241 31.769 10.591

4 6 2

32.489 5.498 15.7

2 2 1

4.311 4.42 Publication closed

1

Publication closed

1 1 1 1 1

9.369 6.381 Not included in SCI Not included in SCI 1.98

1 1

10.123 Publication closed

1 1

Publication closed 52.362

1

29.309

1 1 1 1

8.438 4.559 Publication closed N/A

The citation data were collected from the time of the landmark paper publication to 10 March 2013. The number of landmark papers in each cited frequency interval is shown in Figure 5A. Although the citations ranged widely, from 104 to 14320 times, they were mainly concentrated in two ranges, i.e. 2000–4000 and 200–800 times. The citation of only three landmark papers was above 10,000 times, but the citation of five papers fell below 200 times. Furthermore, to normalize the number of citations of landmark papers published at different times, citations of 82 landmark papers were collected for the 5-year citation within 5 years after they were published and the average citation per year from the time of their publication to the end of 10 March 2013. There were 58 articles cited less than 200 times (Figure 5B). Five-year citation data were selected to prove that the average citation data were reliable. Before collection of data, we thought that papers’ citation would reach a peak 5 years after they were published, but our data showed that the number of citations appeared in a relatively steady increase. Average citations per year of 82 papers from the time of publication to the winning of a Nobel Prize in Physiology or Medicine during 1983–2012 were statistically analyzed to find out whether there was any difference among the three citations. As a result, it was found that the tendency of the 5 years’ citation was relatively similar to the annual average citation. The annual average number of citations mainly was below 40 (Figure 5C). These results indicate that the normalized citation is more of a comparative merit, and that, compared to the annual average citation, the 5-year citation is of a similar evaluating merit, too.

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Bibliometrics of Nobelists’ awards and landmark papers 535

Figure 5. Citation frequency distribution of the landmark papers from Nobel Laureates in physiology or medicine, 1983–2012. (A) Total citation frequency distribution of the landmark papers from Nobel Laureates in physiology or medicine, 1983–2012. (B) Five years’ citation frequency distribution of the landmark papers from Nobel Laureates in physiology or medicine, 1983–2012. (C) Average citation frequency distribution per year of the landmark papers from Nobel Laureates in physiology or medicine, 1983–2012.

We also analyzed the maximum citation of Nobelists’ landmark papers and the journals carrying these papers. It should be pointed out that three of the journals had closed down. Of the 66 laureates, there were 25 persons whose maximum cited articles were just their landmark papers winning the Nobel Prize. But it was noted that the most cited papers written by 44 of 66 (62%) Nobelists were not the ones for which they won Nobel Prize (Table II). The number of the papers’ maximum citation was mainly distributed in the 1000–4000 times category (Figure 6). As shown in Figure 7, nearly 70% of the landmark papers were published in the journals with impact factors greater than 30. But the journals with low impact factors also contained highly cited papers.

many years earlier. After the required test time, their achievements eventually gained affirmation. We call this test time ‘test period’. The data showed that one Laureate had completed his research more than four decades before winning his Nobel Prize. There were a few laureates who got the Nobel Prize within a very short period. For example, Shinya Yamanaka just took 6 years to do so. But for about 80% of Nobelists it took 10 to 30 years. Less than 8% win a Nobel Prize within 10 years of completing their researches (Figure 8). Our results indicate that the test period of the Nobel Prize is generally between 10 to 30 years.

Test period of Nobel Prize

According to the data from Figure 8, we wanted to study further whether the citation times were associated with the length of the test period. From Figure 9A, it was noted that more scatter was concentrated on the period of 10 to 30 years, with 500 to 3000 cita-

As is known to all, it may take a long test time to win the Nobel Prize in Physiology or Medicine. Great discovery needs time to be tested. Generally, the Nobel Laureates’ research was mostly done

Association between the test period of Nobel Prize and citation

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Table II. Citation and journal of landmark papers winning Nobel Prizes, and most cited papers in physiology or medicine, 1983–2012.

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Year

Name

2011

RM Steinman

2010

RG Edwards

2009 2009 2009 2008

EH Blackburn JW Szostak CW Greider H Zur Hausen

2008 2007

F Barré-Sinoussi MR Capecchi

2007

O Smithies

2003

P Mansfield

2002

JE Sulston

2002

HR Horvitz

2001 2001

T Hunt LH Hartwell

2001

PM Nurse

2000

A Carlsson

2000 2000 1999

P Greengard ER Kandel G Blobel

1998 1998

LJ Ignarro RF Furchgott, LJ Ignarro

1998 1996

F Murad PC Doherty

1996

RM Zinkernagel

1994 1994

M Rodbell AG Gilman

1993 1993 1992

RJ Roberts PA Sharp EH Fischer

1992

EG Krebs

1991 1991 1990 1989 1989 1988

E Neher B Sakmann ED Thomas HE Varmus JM Bishop GH Hitchings

1988

GB Elion

1988

JW Black

Journal of landmark papers winning Nobel Prize Journal of Experimental Medicine Journal of Experimental Medicine PNAS Nature Nature Lancet Lancet Cell Cell Cell PNAS EMBO Journal Science Molecular and Cellular Biology Cell Cell Nature Nature Journal of Physics C: Solid State Physicsa Developmental Biology Developmental Biology Developmental Biology Cell Nature Cell Genetics Bacteriological Reviewsb Cell Nature Nature Science Pharmacological Reviewsb Journal of Pharmacy and Pharmacology Nature Nature PNAS Journal of Cell Biology PNAS Nature At the meeting in Rochester, Minnesota, USA, in 1986, they reported their results independently: what is the chemical structure of EDRF is nitric oxide Journal of Cyclic Nucleotide Researcha Nature Nature Nature Nature Journal of Biological Chemistry Journal of Biological Chemistry PNAS Cell PNAS Journal of Biological Chemistry Journal of Biological Chemistry Biochimica et Biophysica Actaa Journal of Biological Chemistry Journal of Biological Chemistry Biochimica et Biophysica Actaa Nature Nature New England Journal of Medicine Nature Nature Cancer Research Biochemical Pharmacology Cancer Research Biochemical Pharmacology Lancet Nature

Citation 1608 383 599 364 194 257 1307 420 420 2111 1599 1107 941 364 451 1917 719 566 441 2110 2257 2257 1267 736 1090 529 682 405 900 776 512 609 154 260 800 394 2643 1238 10643

755 1687 666 1687 666 356 209 166 680 822 332 104 287 332 104 287 1706 1706 505 946 946 140 221 140 221 375 2171

Journal of most cited papers

Maximum citation

Nature

11082

Nature

632

Nature Nature Nature Nature Reviews Cancer

2478 3700 3716 2007

Science Cell

6058 1917

Nucleic Acids Research

13415

Journal of Physics C: Solid State Physicsa Nature

1296

Nature

4080

Cell Science

1470 2358

Methods in Enzymology

2532

Acta Pharmacologica et Toxicologicab

1808

Nature Medicine Science Signaling Journal of Cell Biology

1248 1772 2463

PNAS

3958

PNAS Advances in Immunology

1067 1931

Advances in Immunology

1931

Analytical Biochemistry Annual Review of Biochemistry

3653 5435

Science Cell Science

10454 2679 846

FASEB Journal

2858

Pflugers Archiv: European Journal of Physiology Pflugers Archiv: European Journal of Physiology New England Journal of Medicine Science Molecular and Cellular Biology Journal of Biological Chemistry

15891 15891 2490 1543 2366 426

PNAS

1370

Nature

2171

5174

(Continued)

Bibliometrics of Nobelists’ awards and landmark papers 537 Table II. Continued Year

Name

1987 1986 1986

S Tonegawa S Cohen R LeviMontalcini MS Brown

PNAS Journal of Biological Chemistry PNAS

Citation 480 1922 310

Journal of most cited papers Nature Psychological Bulletin Science

PNAS 286 Science Journal of Biological Chemistry 1141 1985 JL Goldstein PNAS 286 Science Journal of Biological Chemistry 1141 1984 NK Jerne PNAS 634 Annales d’immunologiea Science 2438 4031 Annales d’immunologiea 1983 B McClintock the 1951 Cold Spring Harbor Symposia 997 Science on Quantitative Biology PNAS ⫽ Proceedings of the National Academy of Sciences of the United States of America. aPublication closed. bNot included in Science Citation Index. Ann Med Downloaded from informahealthcare.com by Universitat Autonoma Barcelona on 10/27/14 For personal use only.

1985

Journal of landmark papers winning Nobel Prize

tion times. And the more the citation times, the shorter the tested period. There were five persons to get a Nobel Prize in 10 years whose landmark papers were cited above 6000 times. The highly

Maximum citation 3401 7205 2565 4459 4459 4031 1275

cited papers were widely accepted and became a hot topic, foretelling greater innovation, significance, and value. The data show that the highly cited papers for the Nobel Prize appear indeed in a rela-

Figure 6. Papers’ maximum citation frequency distribution of Nobel Laureates in physiology or medicine, 1983–2012.

Figure 7. Impact factor of the journals containing the papers with maximum citation frequency published by Nobel Laureates in physiology or medicine, 1983–2012. 0: not included in SCI.

Figure 8. Test period of the Nobel Prize in Physiology or Medicine, 1983–2012.

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Figure 9. Association between the test period and citation of Nobelists’ papers in physiology or medicine, 1983–2012. (A) Relationship between the test period and total citations from the time of Nobelists’ publishing the papers, for which Nobel Prizes in Physiology or Medicine during 1983–2012 were obtained, to 10 March 2013. (B) Relationship between the test period and citation within 5 years from the time of Nobelists’ publishing papers before obtaining the Nobel Prize in Physiology or Medicine, 1983–2012.

tively short test period. We also analyzed the relationship between the test period and citation within 5 years of the time of Nobelists’ publishing papers before obtaining a Nobel Prize. As shown in Figure 9B, the distribution of the test period based on the total citation was very similar to that of the 5 years’ citation. Most of the papers were cited below 500 times. The higher the citation of the papers, the shorter the test period for winning a Nobel Prize.

Discussion The Nobel Prize in Physiology or Medicine is highly recognized due to its objective and well-grounded prize-awarding system (2). The Nobel Prize is awarded for an outstanding contribution carried out by scientists in a particular field of scientific activities which will have an everlasting impact and create altogether new fields for research (6). Therefore, we analyzed Nobel Prize winners in physiology or medicine from 1983 to 2012 in multiple aspects. Several novel associations and tendencies can be drawn from this paper. Firstly, the progression of Gairdner Award to Nobel Prize has a certain predictability. Over the past 30 years, almost 70% of the 66 Nobelists had won the Gairdner Award before they won the Nobel Prize. There were nearly 70% of Nobelists having won the Nobel Prize within 10 years of winning the Gairdner Award. The Gairdner Award can represent the trend of the Nobel Prize. The Lasker Awards is also very prescient, but not as much as the Gairdner Award. Secondly, the data reviewed here indicate that citation ranking and impact factor are not absolutely positive correlations to winning a Nobel Prize. Although the impact factor of some journals is not high, their influence is great, such as Journal of Biological Chemistry. Furthermore, the most cited papers written by some the Nobelists are not the ones for which they won the Nobel Prize. Thus, we should not blindly believe the articles published in the top magazines, but rather find valuable articles. The 5-year citation is of a comparatively evaluating merit, similar to the annual average citation. Thirdly, we looked at the test period of the Nobel Prize and analyzed the relationship between the test period and citation.

The data show that the highly cited papers for the Nobel Prize appear indeed within a relatively short test period, and less cited ones may require a longer time to be tested. Additionally, JCR partition acts as a reciprocal supplement with impact factor and citation. Our results reveal relationships among Nobel Laureates’ awards, landmark papers, and the Nobel Prize in Physiology or Medicine. We hope that this study can give some inspiration to those researchers having the potential to become Laureates in the future. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. This work was supported by the National Natural Science Foundation of China (No. 81172824, No. 30971465, and No. 30471635) and ‘211’ project grant.

References 1. Garfield E, Welljams-Dorof A. Of Nobel class: a citation perspective on high impact research authors. Theor Med. 1992;13:117–35. 2. Karazija R, Momkauskait A. The Nobel Prize in physics—regularities and tendencies. Scientometrics. 2004;61:191–205. 3. Baffes J, Vamvakidis A. Are you too young for the Nobel Prize? Res Policy. 2011;40:1345–53. 4. Charlton BG. Scientometric identification of elite ‘revolutionary science’ research institutions by analysis of trends in Nobel prizes 1947–2006. Med Hypotheses. 2007;68:931–4. 5. Stephan PE, Levin SG. Age and the Nobel Prize revisited. Scientometrics. 1993;28:387–99. 6. Kademani BS, Kalyane VL, Kumar V, Mohan L. Nobel laureates: their publication productivity, collaboration and authorship status. Scientometrics. 2005;62:261–8. 7. Gingras Y, Wallace ML. Why it has become more difficult to predict Nobel Prize winners: a bibliometric analysis of nominees and winners of the chemistry and physics prizes (1901–2007). Scientometrics. 2010;82:401–12. 8. Dorta-Gonzalez P, Dorta-Gonzalez M. Comparing journals from different fields of science and social science through a JCR subject categories normalized impact factor. Scientometrics. 2013;95: 645–72.

Bibliometric analysis of Nobelists' awards and landmark papers in physiology or medicine during 1983-2012.

This study's purpose was to determine if there was a relationship between Nobel Laureates' awards and landmark papers and winning the Nobel Prize in P...
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