sign in sign up
<<
Home , Howard Martin Temin

EUGENE GARFIELD INSTITUTE FOR SCIENTIFIC lNFORMATION~ 3501 MARKET ST., PHILADELPHIA, PA 19104

Ninety-one Citation Classics ~rosn the Jormsal of Experimental Medicine

Number 28 July 13, 1987

Since its inception as the Rockefeller In- of medicaI research. The Rockefeller Insti- stitute for Medical Research in 1901, The tute began with an initial gift of $200,0(MI Rockefeller University has played an import- to be distributed over 10 years. Guided by ant role in the advancement of medical re- a Board of Scientific Directors that includ- search in the US and throughout the world. ed some of the most distinguished US re- I am proud to be associated with this institu- search physicians of the time, the institute tion not only as a member of The Rockefel- initirdly awarded grants and scholarships to ler University Council but also because of US scientists working in medical research my respect and admiration for its president, laboratories at home and abroad. But as the . 1I also think that the uni- need to centralize medical research and de- versity represents the best in private medieal vote full-time efforts to laboratory work be- research in the service of humanity. came apparent, Rockefeller provided addi- From the 1850s to the turn of the century, tional funds to build the medical research the US was growing in wealth, the desire center. In 1905 the institute began publish- for education, and the need for scientists to ing the Jormud of Expen”mental Medicine communicate and develop ideas.z (p. 1-3),3 (JEM) and in 1906 opened its first labora- Private research laboratories existed tory buildktg.b Opened in 1910, the Rocke- throughout the US, but they suffered from feller Institute Hospital was the first clinical lack of financial support and public confi- research hospital in the US.T dence,4 and as a result many US scientists From this base the institute, hospital, and worked in small, inadequately equipped lab- journal grew to produce some of the most oratories, relying heavily on European in- enduring worldwide efforts to improve life, stitutions and publications for current infor- including the first isolation and successful mation.s With the successes of Louis Pas- tests of antibiotics, the development of pre- teur, , and other European pi- serving whole blood, and the first proof that oneers in bacteriology during the late can cause animal cancer. 1 Today, 1800s,4 the scientific community and the The Rockefeller University consists of 50 public began to realize the important rela- laboratories specializing in both basic and tionship between research and the treatment clinical research in the biomedical and re- of disease. The Rockefeller Institute was the lated behaviorrd and physical sciences. In first major foundation dedicated to support- addition to publishing JEIU, The Rockefeller ing medical research efforts in the US. University Press publishes four other med- John Davison Rockefeller, the magnate of ical research journals: the Journal of Clini- the Standard Oil Company, having decided cal Investigation, which was the subject of to donate some of his vast wealth to worthy a recent citation study,s the Journal of Gen- causes, agreed to finance the development eral , the Journal of Cell ,

179 and Biophysical Journal. Probably the best- Transforn@ Principle: Discovering hat known joumrd of The Rockefeller Univer- Genes Are Made of DNA. 13 He has tdso sity Press, however, is JEIU, the subject of written a Ciran”onClassic” commentary this study. about his work. 14 Nineteen other articles in JEIU began in 1896 with a $1,000 amual the Bibliography are also the subjects of contribution from Johns Hopkins Universi- Classics commentaries, as indicated by ty.9 (p. 243) The first editor was William asterisks. H. Welch (1850-1934), a renowned US With such a distinguished group of editots pathologist who revolutionized medical over the years, it is not surprising that JEM school education by combining course work, has continued to be one of the world’s most clinical duties, and laboratory work in the respected medical research journals. Ac- Johns Hopkins University curriculum. 10 cording to data from the 1985 .fournal Cita- The Johns Hopkins medical library is named tion Repotts@ section of the Science Cita- in his honor. (In a previous essay, I dis- tion Index@(SCP ), JEM has an impact fac- cussed how my work on the Welch Medi- tor of11 .2, placing it among the top 5 med- cal Library Indexing Project laid the foun- ical and immunology joumafs and 17th dation for my interest in citation indexing among the 4,072 journals ranked by impact and for the subsequent development of factor. [email protected]) Welch edited the journal for over five Classics from High-hnpact Journals years with great success; however, as the volume of research manuscripts submitted In the past few years we ‘ve published a increased and his involvement as chairman series of essays in which we identi& lists of the Rockefeller Institute’s Board of Sci- of classic papers from such high-impact entific Directors began to consume most of journals as the New England Journal of his time, the journal stopped being pub- Medicine (N!UM), 15the Lacer, lb the BriG lished. In 1905 Welch appointed fellow ish Medical Journal, 17 and the Journal of board member Simon Flexner as his succes- the Amen”can Medical Association. 18 In sor to the position of chief editor and Eu- these studies the citation threshold, the least gene L. Opie as assistant editor.g (p. 249) number of cites received by items in each Since then, the journal has continued to at- Bibliography, is between 158 and 270. tract accomplished scientists to serve on the However, as will be seen, the number of ar- editorial board. Previous editors have in- ticles in JEM at these thresholds is quite cluded Vincent P. Dole, Jr., Ren4 Dubos, high; therefore, we limited the analysis as Herbert S. Gasser, James Hirsch, Richard described below. It is not surprising that Krause, Henry Kunkel, and Peyton Rous. many of the papers listed in the Bibliogra- Its current edkors, Anthony Cerami, Zan- phy have also appeared in previous citation vil A. Cohn, and Maclyn McCarty, are also studies. I9-21 distinguished for their contributions to sci- To develop this Bibliography, we used the ence. Together with Oswald T. Avery and 1955-1985 SCI to identify the most-cited ar- Colin M. MacLeod at The Rockefeller Uni- ticles regardless of the year that they were versity, McCznty coauthored one of the most published in JEM. The 91 articles identified important papers in the history of science— are those cited over 420 times during the one that provided the first evidence that 3l-year pericd. The articles are listed alpha- DNA was responsible for transmitting betically by first author. The average num- hereditary information. la McCarty has re- ber of citations for the articles in the Bibli- ceived several awards for this research con- ography is 764. For the 50 papers that have tribution and has written a book entitled lhe not appeared in any of 1S1’sprevious cita-

180 TabSe 1: Tbc SC/@ research fronta that include 10 or more 1985 citing dc+armentapublished in the Jourrwf of Erperimerrfal Medicine (f, .Exp. Med.). A= number of citing dncmnenta from J. ,!lrp.Med. for each research front, Following in parendreaes is the percent these drrcumentarepresent of the total nmrrberof citing documents. B= total number of citing dcarments. C =total number of core dncumenea. The research fronts are listed in de- scending order by the percent of citing documents that are from J, hp. Med.

Name A BC

85.3391 Characterization of T-cell populations and their selected activities in mice 11 (17,2) 642 85-4831 Effezta of mnnnclonal anehdies, anti-L3T4, and fA antigens on T-cell 13 (10,0) 130 3 activation and accessory cell pcpdation; arrdclonal analysis of expression arid recognition of T-cell receptor 85-7939 Major biatncompatibility wmplex-lirrked control of the murine immune 13 (9.0) 145 2 respnnae to myelin basic ; role of fa antigen mrd T-cell clones s~ific to myelin basic protein immunotbe~py 85-2050 Characterization of complement receptors for C3B, LFA-I, and related 20 (6.3) 320 17 anti8ens in the activation and fiurceion of cytc+mcic T-cells arrd macrophages 85-5994 Characterization, structural amdysis, and expression of class I and class IJ 21 (6.2) 337 13 genes from major bistocompatibility complexes in mice, hummrs, and other mammals 85-0178 Monoclorml antibody activation of T+elSs and arrtigen receptor gene 43 (5 ,8) 740 39 expression 85-1272 Antigen processing mrd presentation by macrophages, dendritic cells, and 25 (4.3) 578 23 B-cells; accessory cell heterogeneity and mechanisms of T-cell activation in the immune respnnst 85-3532 Characterization of anei-idiotypic antibodies and id[otypic regulation in 12 (4,3) 281 12 mice and humans 85-36% Effects of interleukin-2 and studies of its receptors on human T-cell 27 (3,7) 721 20 Iympbncytea 85-1129 Effects of interferon on the expression of class I and class U cell surface 13 (3.5) 374 13 antigens irrmononuclear cells 85-1728 T-cell subsets and actions in allograft rejection, arrtitumoractivity, and 10 (2.9) 346 16 aller8ic neuritis 85-CP381 Antigen expression, activity, and other aspects of natural killer cell 16 (2.8) 569 25 cytotoxicity in human Iymphncytes 85-0134 Hernato~ietic studies using human and murine bone-marrow cell cultures 11 (2,5) 436 25 85-0129 Antigens, differentiation, role of interfercms, and other aspects of B-cells 25 (2.2) 1,144 58 and T-cells in leukemia patients and other humans 85-1379 Biochemical characterization, biological activities, and cellular production 13 (2.1) 614 31 of intedeukin- I 85-2912 Isolation, purification, arrdcharacterization of and antigens from 48 (0.6) 7,571 4 various species using mormclonal mrtibdes and other metbnds 85-1406 Isolation, characterization, expression, and cloning of DNA and RNA 32 (0.5) 6,184 26 nucleotide sequences tion studies, the average number is 553. Full pared JEM with the Journal of Immunolo- bibliographic references for these articles are gy.zz “The analyses reveal an important given. For the remaining 41 a brief citation pointabout this journal [JEMl. It is probably is provided as well as references to the pre- badly named. No other journal seems to play vious studies. (For those readers who would as important a role today in the transfer of like full citations for ali papers in the Bibli- information on immunology.’ ’22Apparent- ography, you can contact me at 1S1.) ly its name has not impeded its continued By looking more closely at this list of impact. most-cited papers, it is obvious that immu- nology articles predominate. Approximately Reaenrch Fronts 37 of the 50 “new” articles in the Bibliog- raphy are related to this specialty-a fact Research-front analysis of JEM confirms noted in a previous citation study that com- its strong emphasis in the field of immunol- Figure 1: Year-by-year distribution of cisatiorrsreceived 25, of the articles in this front were pub- by three Irighly cited articles. Mid Lfne =Carrtor H. lished by JEM. Fifty-eight core papers were 141:1390-9, 1975 (878 cites). Broken Une= Roacn- thal A S. 138:1194-212, 1973 (S62 cites). Dotted identified, 11 of which are JEM articles. line= Zigmond S H. 137:387-410, 1973 (S45 cites). All the papers in the Bibliography are by definition Citation Classics, but 32 of them 130- are also core documents in current research 120 fronts. The 1975 pa~r (878 citations) by “\. Harvey Cantor, Harvard Medical School, 110 . Boston, and Fdward A. Boyse, Memorial ,> 100 Sloan-Kettering Cancer Center, New York, Ii ...., ..*... ..”’ ~ .h- ~,., ; ‘v” is the second of a two-part article describ- 90 h \~ ,, .“: rn ing the’ ‘Cooperation between subclasses of ~1‘\, / \ ~ 80 Ly + cells in the generation of killer activi- .-J ,,.!! ~, ~’” ~ JO ty. ” Part 1 turned up in our citation study \ >v./’”” ~ 60 of most-cited articles from 1961 to 1982. p ,J: Both parts are core to “Characterization of 50 T-cell differentiation, activities, and antigens ,1’ ,:” \ ,/”/ 40 ; .: in mice” (#85-3695). About 125 papers 30 /; were published on this topic in 1985. Another two-past study by Ahsn S. Rosen- ;: zignj~~~ s ~ . . 20 thrd and Ethan M. Shevach, National Insti- ;/,,,,, Rosenthal A S ---- 10 II . tute of Allergy and Infectious Diseases, Cantor H — Bethesda, Maryland, discusses the ‘‘Re- 75 80 85 quirement for histocompatible rnacrophages YEAR and lymphocytes” (Part 1) and the role of the microphage in controlling the immune response genetically (Part 2). The former ogy. We identified about 8,500 research part is 1 of 23 core papers that helped iden- fronts in 1985. Of these, 236 fronts involved tify the research front on antigen process- articles published in JEA4. Seventeen of ing and related mechanisms (#85- 1272). these topics contain 10 or more papers pub- Another paper in the Bibliography was au- lished in JEM (see Table 1). thored by two Rockefeller University re- The research-front topics are arranged by searchers, Sally H. Zigmond and former percentage of articles published in JEM. editor James G. Hirsch. We lament his re- Consequently, the first front listed, “Char- cent death on May 25, 1987. Their 1973 acterization of T-cell populations and their paper, ‘‘Leukoeyte locomotion and chemo- seleeted activities in mice” (#85-3391), is taxis, ” was cited 845 times and is 1 of 11 not the largest. Of the 64 articles published core papers on “Studies on neutrophil func- on this topic, however, over 17 percent (11) tion and polymosphonuclear leukoeyte che- were published in JEIU. Two reeent papers, motactic activity” (#85-3073). published in 1980 and 1981, constitute the Figure 1 shows the year-by-year citations “core” of this research front. In contrast, to each of the three papers noted above. As the 14th research front listed in Table 1, en- the graph shows, the Cantor paper received titled “Antigens, differentiation, role of in- its highest number of citations within the terferon, and other aspects of B-cells and first two years after its publication in 1975. T-cells in leukemia patients and other hu- In contrast, the Rosenthal and Zigmond pa- mans” (#85-0129), involved over 1,100 pers experienced a more gradual increase in published articles. Just over 2 percent, or citations.

182 Table 2: Frequency distribution of publication dates for Table k Orographic areas represented by the institu- the 91 items in the Blbliograpby, 1955-1985 SCF. tional atlliations for all 91 enties in the Bibliography, listed in descending order according to the number of papers prnduccd. Publication Distribution of Date AU Articka Geographic Mation Dtatribution of of Institutions All Artklea 1930-1939 2 1940-1949 2 71 1950-1954 5 New York 32 1955-19s9 6 Massachusetts 11 1960-1964 17 California 10 1965-1969 21 Maryland 7 1970-1974 18 Colorado 4 1975-1979 17 Comccticut 4 1980-1985 3 Alabama 2 Minnesnta 2 New Jersey Pennsylvania Author and Institutional Information Flori& Illinois The number of Nobel laureates who have Missouri published in JEA4is significant. Five of them New Mexico Ohio appear in the Bibliography alone. Most have Texas associations with The Rockefeller Univer- Vermont sity. , current chairman of Washington Washin~tnn, DC 1 the Pathology Department, Hatvard MedicaJ United Kl~gdom 5 School, and former associate editor of JEM, Australia 7 Sweden 4 shared the award in 1980 with , Switzerland 1 University of Paris, and George D. Snell, Canada 2 , Bar Harbor, Maine, for Italy 2 Japan 1 work on the genetic control of immunolog- ical reactions. Astor Professor, -received the prize in 1972 , Salk Institute for Bio- with Rodney R. Porter, University of Ox- logical Studies, La Jolla, California, and for- ford, UK, for research on antibody struc- mer visiting professor at The Rockefeller ture. Huggins, University of Chicago, was University, was honored in 1975 with David honored in 1966 for his work on prostatic Baltimore, Massachusetts Institute of Tech- cancer treatments. nology and Rockefeller University alumnus, The institutional affiliations of other au- and Howard Martin Temin, University of thors in the Bibliography show that JEh4, Wisconsin, Madkon, for work on tumor vi- which originally began as an outlet for the ruses and cell . In 1974 George Emil Rockefeller Institute papers, “has always Palade, now a senior research scientist, Yale welcomed articles from outside and applied University School of Me&cine, and former the same criteria for judging their accept- professor at The Rockefeller University, ability as for those from inside the Insti- was awarded the Nobel for work on cell tute.”2 (p. 63) Fifty-nine institutions are structure and function. He shared the award represented in the Bibliography, with 39 ap- with , Catholic University of pearing only once. The Rockefeller Univer- Louvain, Belgium, and , sity appears most frequently (17 times), also of Rockefeller. Two other Nobelists, followed by Harvard University (10), Gerald Maurice Edelrnan and Charles Hug- Scripps Clinic and Research Foundation (7), gins, appear in the Bibliography. Edelman, and both the Memorial Sloan-Kettering a 1960 graduate of The Rockefeller Univer- Cancer Center and the National Institutes of sity who is also distinguished as a Vincent Health (6).

183 Figure 2: Graph of the cumulative citation-frequency distribution, 1955-1985 SC1’@,for articles with 50 or more citations and for those articles cited 50 or more times from the Ioumal of Experimental Medcine and two other comparable medical journals 100, : ‘b \\\:\ ‘?’\.“\\ ,. \. \*’ \ \<\ ●’\ \\.

10 - ● ,’\ \* \ \\ \\ \* ‘:> Q \ \ 1 - “\,\:\ \ . J. Exp. Med. ~.\\ I 1 \ \. Articles citecf~sf)

‘i \+\ In t he lg55-1985Sc/

~,1. Engl.’J. Med.

‘ Lance;

a , , , & 50 100 200 300 500 700 1000

CITATION THRESHOLD

Cmuufeted Number of Articie$ for the Journats, with the Cumulated Percent citation of Total in Parenthesm Threshold J. EXP. Med. Luncel N. Engl. J. Med. 1955-1%3s SCI

700 29 (0.9) io (0.2) 9 (0.2) 1,964 (0.5) 5C0 60 (1.8) 25 (0,6) 33 (0.9) 4,034 (1.)) 4011 103 (3.1) 54 (1.2) 66 (1,7) 6,470 (1.8) 300 208 (6.3) 119 (2.7) 125 (3.3) 11,851 (3.2) 250 326 (9.8) 193 (4.3) 220 (5.8) 17,380 (4,7) 200 487 (i4.7) 319 (7.2) 389 (10.2) 27,572 (7.5) 150 830 (25.0) 624 (14.0) 719 (18.8) 49,523 (13.4) 100 1,569 (47.3) 1,472 (33.1) 1,492 (39.0) 109,218 (29.5) 75 2,248 (67.8) 2,481 (55.8) 2,334 (61.0) 185,708 (50.2) 50 3,316 (icQ.o) 4,445 (ioo.o) 3,824 (100.0) 369,916 (100,0)

Age of papers and Geographic Affiitiosss oldest paper in the Bibliography, a 1933 Table 2 compares the number of articles methodology paper entitled’ ‘A serological published according to their publication differentiation of human and other groups dates from 1930 to 1985. Eighty percent of of hemolytic streptococci. ” In contrast, the articles in the Bibliography were pub- Tuomo Timonen and colleagues, National lished between 1960 and 1980. Rebecca C. Cancer Institute, Bethesda, wrote the most Lancefield, Hospital of the Rockefeller In- recent paper, a 1981 discussion of the stitute for Medical Research, authored the “Characteristics of human large granular

184 Table & Comparison of total items published with total consistently publish papers that are cited items cited 50 or more times for three medicsl jOur- above the average. For the 1955-1985 SCI, nals, 1955-1985 SCJ@. the total number of articles, regardless of journal, cited at least 50 times is about 370,000. JEM, the Lancet, and NEJM alone produced a significant proportion of these items—over 3 percent, or 11,585. For these journals Table 4 includes data

J, Exp, Med. 6,563 2,914 44.4 on articles published from 1955 to 1985 as L4ncet 88,158 4,198 4,8 well as articles cited over 50 times. JEM has N. Engl. J. Med. 41,594 3,694 8,9 a remarkable 30-year impact. Out of 6,500 articles published, over 2,900, or 44 per- lymphocytes and relationship to natural cent, were cited over 50 times. JEM has killer and K cells. ” published far fewer articles than the other The geographic distribution of authors ap journals; nevertheless, as the data demon- pearing in the Bibliography according to strate, it has been exceptionally influential. their institutional affiliations is listed in By comparison, while the btcet and Table 3. Eight countries are represented: NILfM have published over 88,000 and Australia, Canada. Italy, Japan, Sweden, 41,000 items, respectively, the Percentage Switzerland, the UK, and the US. Two pa- cited over 50 times was 4.8 and 8.9. pers are multinational collaborations. Ellis Figure 2 compares the citation-frequency L. Reinhesz, J.M. Breard, and S.F. Schloss- distribution of articles cited over 50 times man, all of the Sidney Farber Cancer Insti- for the three journals and a baseline average tute and Harvard Medical School, coau- for the 1955-1985 SCl articles cited 50 times thored a paper about human T lymphocyte or more. We used the tabular data listed subpopulations with L. Moretta, Universi- below the graph to plot each curve. Natural- ty of Oenoa, Italy, and M. Roper and M.D. ly, as the citation-frequency threshold in- Cooper, University of Alabama, Birming- creases, the percentage of articles decreases ham. The other collaborative article is by for all journals shown. Yet, as the graph Tomio Tada and Masaru Taniguchi, Chiba demonstrates, JEIU clearly has a huger per- University, Japan, and Chella S. David, centage of articles at the higher levels. For Wash@ton University School of Medicine, example, O.9 percent of JEM articles were St. Louis. cited over 700 times, while the comparable figure for the entire file cited over 50 times Citation-Frequency Distribution is 0.5. Believe it or not, the curve for the Another way to examine the output of a entire file presents a nearly perfect hyper- journal is to look at its citation-frequency bolic distribution. distribution, that is. the percentage of ar- JEM’s many contributions to medical re- ticles at or above a particular citation ievel. search over the years have clearly ranked We compiled citation-frequency distribution it as a valuable source of information. These data using the 1955-1985 SC1for three im- illustrations are one more indication that portant medical journals: JEIU, the Z.ancet, JEM is a journal extraordinaire. and NEJh4. The percentage and dktribution ***** of articles from these journals cited at least 50 times in the SCZare shown in Table 4 and Figure 2. My thanks to Carole Gun, Karen Prestigious medical journals, like the three Maguire, and Pat Taylor for their help in we have selected for graphic representation, the preparation of this essay. o,~7B1

185 REFERENCES

1. GarfJeld E. Joshua Lederberg-multidisciplirrmian rxtraordinaow. .%a.w of an mformarion scierrdsl. Philadelphia: 1S1 Press, 1977, Vol. 1. p, 81-2. 2 Comer G W. A history of the Rockefeller Institute IX)] -1953: ongitcs and grow~h. New York: Rockefeller Institute Press, 1%5. 635 p. 3. Berliner H S. A system of sck?ntijic medicine: philanthropic foundations in the Flr.rner era. New York: Tavistnck, 1985, 190 p. 4, Blake J B. scientific institutions since the Renaissance: their role in medkzd research. Proc. Arrwr. Phil. Sot. 101:31-62, i957. 5. Wekh W H. 7?reJournal of E.rperimenral Medicine. Introduction. J. Ezp. Med. 1:1-3, 18%. 6. Holt L E. A sketch of the development of the Rockefeller Institute for Mrdical Research (Address delivered at the opening of the Iaburmories in New York City, 11 May 1906). Studies from The Rockefeller Institute for Medical Research. Vol. 6. Lancaster, PA: New Era, 1907. p. 17-25. 7. ‘J’heRockefeller University. New York Rockefeller University, 1986. 1 p. (Bruchure. ) 8. Garfield E. Fifty classics from the Jourrwd of Clinical Irrvesrigation: over 60 years of Nobel-class rexearch, Current Corrrems (8):3-11, 23 February 1987. 9. FJexner S & Ffexrrer J T. William Henry Welch arrd the heroic age of American medicine. New York: Viking Press, 1941.539 p. 10. Welch, William Henry. Encyc@xrecfia Britannica, Chicago, IL: Encyclopedia Britannica, 1985. vol. 12. p. 566, 11. Garfield E. Origins of Current Contcvrfs, 1S1, and computer-aided information retrieval. How it all began at the Welch Medical Library Indexing Proy?ct. E$says of an infomrarion sctenrisl: ghostwrirlng and other essays. Philadelphia: 1S1 Press, 1986. Vol. 8. p. 320-6. 12. Avery O T, MacLeod C M & McCarty M. Studies on the chemical nature of the substance inducing transformation of pnemuocnccaJ types: induction of transformation by a deoxyribonucleic acid fraction isolated from pneumoceccus Type IJf. J. Exp. Med. 79:137-58, 1944. 13. McCarty M. 7he trcms~ornrin8principle: discovering rhaI 8enes are made of DNA. New York: W.W. Norton, 1985.252 p. 14. ------Citation Classic. Commentary on J. &p. Med. 79:137-58, 1944. Currenl Conterus/Life Sciences 28(50):26, 16 December 1985. 15. Gartield E. 100 classics from the New England Journal of Medicine. Essays of an information scientist: /he awardr of science and oiher essays. Philadelphia: 1S1 Press, 1985. Vol. 7. p. 186-93. 16. ------100 classics from lle Lancer. Ihd. p. 295-305. 17, ------The 101 most-cited pcrpers from the British Medical Journal highlight the important role of epidemiology in medcine. Curreru Contents (7):3-12, 16 February 1987. 18. ----—---- 100 Citation Classics from 71reJournal of the American Medical Association. J~A–J. Am. Med. A.m. 257(1):52-9, 1987. 19. ------Most-cited articles of the 19WS. Parr 4. Clinical research, Emays of m information mientiw, Philadelphia: 1S1 Press, 1981. Vol. 4, p. 379-88. 20. ------Tbe 1983 articles most cited in 1983 and 1984. 1. Life sciences. f6id., 1986. Vol. 8. p, 444-59. 21, ------, The 1,(KiUarticles most cited in 1961-1982. IO. Another 100 Citation Classics cap the millenary. Current Contents (16):3-14, 2 I April 1986. 22. ------Journal citation studies. III. Jorcrrud of Erperimenral Medicine compared with Journal of lmrnunolog.v; or. how much of a clinician is the mununologist? Essays of w infornuuton sc:encist. Philadelphia: 1S1 Press, 1977. Vol. 1. p. 326-9.

Bibliography: The most-cited articles from the Journal of Experimental Meaiciae, 1955-1985 SCP. Articles are listed in alphaixtic order by first author. Full bibliographic information is provided for ordy those papers that have not appeared previously in a Current Contents@ (CCW ) study. For papers that have appeared in past studies, a brief reference to the previnus strrdyis provided. See key at end of table for full essay references. Asterisks (*) indicate articles with Cifation Ckrssic@ commentaries. The issue number, year, and edition of CC in which these commentaries appeared are in psrentheacs.

1955-1985 SCI Citntksrra Blbfiugraphk Data

693 Aiiiann A C, Harington J S & Birheek M. An examination of the cytotoxic effects of sihca on macrophages, f. &p. Med. 124:141-54, 1966. 614 *Avery O T. J. E@ Med. 79:137-57, 1944. %= Vol. 8, p. 43. (50/851LS) 580 ●Baaten A. J. Exp. Med. 135:610-26, 1972. Sce Vol. 2, p. 475. (32 R4tLS) 551 Becken A & Berracerraf B. Properties of antihudies cytophfk for cnacrophages. J. &p. Med. 123:119-44, 1966.

186 1955-1985 SCI citations Biblirr/@pftkc Dirts

491 Sewn M J. The major histncompatibllity complex determines susceptibility to cytotoxic T cells directed againat minor histccompatibility antigens, J. hp. Med. 142:1349-64, 1975. 1,465 *Bianeo C. J. E@ Med. 132:702-20, 1970. See Vol. 7, p. 271, (20181/LS) 432 Bfrta H & Wigaell H. Shared idiotypic determinants on B and T lymphmytea reactive against the mr-neantigenic determinants. 1. Demonstration of similar or identical idiotypes on lgG molecules and T-cell receptors with specificity for the same aklnarrtigens.J. Exp. Med. 142:197-211, 1975. 1,919 Boyden S V. J. E@. Med. 93:107-20, 1951, See Vol. 8, p. 44. 1,029 Boyden S. J. Esp. Med. 115:453-66, 1962. See Vol. 8, p, 189, 1,137 Cantor H. J. Exp. Med. 141:1376-89, 1975, See Vol. 8, p. 134. 878 Cantor H & Bnyse E A. Functional subclasses of T lymphocytes bearing different Ly antigens. 11. Cooperation between subclasaea of Ly + cells in the generation of killer activity. J. Erp. Med. 141:1390-9, 1975. 436 Cerotiid J-c, Engera H D, MacDrmald H R & Brunner K T. Generation of cytotoxic T Iymplrocytes in vitro. L Responac of normal and immune mouse spleen cells in mixed leukocyte cultures. J. &p, Med. 140:703-17, 1974, 815 Cohn Z A. J. Exp. Med. 112:983-1004, 1960. See. Vol. 4, p. 374. 582 Cohn Z A & Benson B. The differentiation of mononuclear phagccytes: morphology, cytnchemistry, and biochemistry. J. Erp. Med. 121:153-70, 1965. 463 Cohn Z A & Wiener E. The particulate hydrolaaes of macrophages. 1, Comparative enzymology, isolation, and properties, J, Ekp. Med. 118:991- [008, 1963. 2,CQ3 “Corms A H. J, Exp,d-fed, 91:1-13, 1950. See Vol. 8, p. 44, (6/81/LS) [,168 Curers A H. J. Exp. Med. 102:49-59, 1955. SW Vol. 8, p. 189. 626 Cooper M D. J. Erp. Med. 123:75-102, 1966. See Vol. 3, p. 702. 864 “Dickier H B. J. Exp. Med. 136:1914, 1972. Sce Vol. 8, p. 313. (14/84/LS) 706 Dixon F J, Fe]rjrrranJ D & VetsqrreaJ J. Expsrimerrtal glomerulonephritis: the pathogemsis of a laboratory mudel resembling the spectrum of human glomemlonephrh is, J. Exp. Med. 113:899-920, 1%1. 460 Djord]evic B & Szybalsfd W. Genetics of human cell lines. III. Incorporation of 5-bromo- and 5.iod@froxyuridine into the dccxyribnnucleic acid of human cells and its effeet on radiation sensitivity. J, E,rp.Med. 112:509-31, 19(KI. 3,314 Drdbecco R. J. Erp. Med. 99:167-82, 1954. See Vol. 8, p. 44. 465 Enrdfey D D. J. Exp. Med. 147:1106-15, 1978. See Vol. 4, p. 691. 461 Edefman G M. J. Exp. Med. 113:861-84, 1961. Sce Vol. 3, p. 690. 446 Erb P & Fehfnmrru M. The role of macrophsges in the generation of T-helper cells. 11. The genetic cmrtrol of the microphage-T-cell interaction for helper cell induction with soluble antigens. J. Exp.Med. 142:460-72, 1975, 496 Farqufrrrr M G, Wissig S L & Pafade G E. GIomendar permeability. I. Ferritin transfer across the normal gkomendar capillary wall. J. Exp. Med. 113:47-66, 1961. 569 ●FBftmmr M. Antibdy formation in vitro. J, Ecp, Med. 114:837-56, 1%1. (52/83/LS) 425 Folkmrur J, Merler E, Abernathy C & Williams G. Iwrlation of a tumor factor responsible fOr angiogenesis. J. Esp. Med. 133:275-88, 197 i. 745 Friend C. Cell-frez transmission in adult Swiss mice of a disease having the character of a leukemia. J. Erp. Med. 105:307-18, 1957. 786 Gery I, Gerzhon R K & Waksmnn B H, Potentiation of the T-lymphocyte response to mitogens. Parts 1 & U. J. Erp. Med. 136:128-55, 1972. 1,144 Gold P. J. J%Xp.Med. 121:439-62, 1965. See Vol. 7, p. 328. 1,166 “Gold P. J. E-q). Med. 122:467-81, 1965. See vol. 7, p, 32g. (48/80/CP) 917 Goldblatt H. J. Exp. Med. 59:347-79, 1934. See CC (8):3-12, 24 February 1986. 448 Good R A. J. Erp. Med. 116:773-%, 1%2. See Vol. 3, p. 702. 499 Goodwin J S, Bankhurzt A D & Meazner R P. Suppression of human T-cell mitogenesis by prostaglandirr: existence of a prostaglardh-producing suppressor cell. J. E.Tp. Med. 146:1719-34, 1977. 451 Gordon R D, Sipaotr E & .%melzort L E. in vitro cell-mediated immune responses to the male specific (H-Y) antigen in mice. J. Esp. Med. 142:1108-20, 1975. 515 * O & Muffer-Eberhard H J. The C3-activator system: an alternate pathway of complement activation. J. Exp. Med. 134 :S90- 108, 1971, 422 Huggfna C, Brfziareffi G & Sutton H. Rapid induction of mammary carcinoma in the rat and the influence of hormones on the tumors, J. Erp. Med. 109:25-42, 1959. 2,970 “Jondaf M. J. Erp. Med. 136:207-15, 1972. See Vol. 7, p. 178. (24/85/LS) 549 Jorrdaf M & Kfeirr G. Snrface markerz on human B and T lymphocytes. II. presence of Epstein- Barr receptors on B Iymphucytes. J, Erp. l-fed, 138:1365-78, 1973.

187 1955-198s SCI Clfatfons Bibliographic Data

464 Klebanoff S J. Iodhrrrtionof bacteria: a bactericidal mechanism. J. Exp. Med. 126:1063-78, 1%7. 660 “Koffler D. J. EKp. Med. 126:&37-24, 1%7. See Vol. 4, p. 385. (36/80/CP) 513 Lambert P H & Dixon F J. Pathogenesis of the glomertdonepkltis of NZB/W mice. J. Exp. Med. 127:507-22, 1968. 589 LnstcefleldR C. J. .Ezp. Med. 57:571-95, 1933. See Vol. 2, p. 615. 715 “Lay W H & Nuasmtweig V. Receptorsfor complement on leukocytes. J. Erp. Med. 128:991 -KW7, 1%8. (42/84/LS) 542 Ledbetter J A. J. Exp. Med. 153:310-23, 1981. See Vol. 6, p. 304. 453 lamer R A, Glaasock R J & Dixon F J. The role of asrti-glomerular basement membrane rmtibudy in the pathogenesis of human glomerrdonephritis. J. Exp. Med. 126:989-1004, 1%7. 689 Lichterrateha L M. J. Erp. Med. 120:507-30, 1964. See Vol. 4, p. 388. 599 Mackaness G B. Cellular resistance to infection. J. Exp. Med. 116:381-406, 1%2. 506 Mackmreaa G B. The immunological basis of acquired cellular resistance. J. Erp. Med. 120:105-20, 1964. 722 Mackanesa G B. The influence of immunologically committed lymphoid celfs on microphage activity in vivo. J. Eqr, Med. 129:973-92, !%9. 486 MUler J F A P & MItehell G F. Cell to cell interaction in the immune reapnnse. 1. Hemolysin- forming cells in neonatally thymectomizcd mice reconatieuted with thymus or thoracic duct lymphocytes. J. Erp. Med. 128:80-20, 1968, 832 “Miller L L. J. Exp. Med. 94:431-53, 1951. See CC (16):3-14, 21 AprO 1986. (13/fUI/LS) 2,110 Miahell R I. J. Exp. Med. 126:423-42, 1%7. see Vol. 7, p. 221. 569 “Mitchell G F. J. fip. Med. 126821-37, 1%8. See Vol. 3, p. 703. (25/84/LS) 553 ● MoUer G. Demonstration of mouse isoantigens at the cellular level by the fluorescent antibody technique. J. Erp. Med. 114:415-34, 1%1. (27/84il,S) 1,335 *Moretta L. J. Exp. Med. 146: 184-2~, 1977. Scc Vol. 7, p. 329. (50/85/LS) 477 Nathan C F, Karnovsky M L & David J R. Alterations of rmrcrrrphagefimctimrs by mediators from Lymphocytes. J. @r. Med. 133:1356-76, 1971. 889 *fMserrmm E F. J. Erp.Med. 124:921-52, 1966. k Vol. 8, p. 314, (521841LS; 381851CP) 3,117 Pedade G E. J. .Exp. Med. 95:285-98, 1952. Srx Vol. 8, p. 47. 513 Parrott D M V, de Sorraa M A B & East J. Thymusdependent areas in the Iymphoid organs of nearatally thymectomizcd mice. J. E&p.Med. 123:191-204, 1966. 674 “Pernfa B. J. Exp. Med. 132:1001-18, 1970. See Vol. 1, p. 522. (27/83/LS) 462 Pope J H & Rowe W P. Detection of specific antigen in SV40-transformed celts by immunofluorescence. J. -Erp. Med. 120:121-8, 1964. 959 ●PuckT T. J. E.rp. Med. 103:273-83, 1956. See CC (16):3-14, 21 April 1986. (3/83/LS) 773 Puck T T & MarcrIs P I. Action of x-rays on mammalian cells. J. hp. Med. 103:653-66, 1956. 584 Puck T T, CiWirua S J & RoMrraemA. Genetics of smnatic mammalian cells. III. Long-term cultivation of euploid cells from human and animal subjects. J. Erp, Med. 108:945-55, 1958. 650 Rnbellbro E. J. Erp. Med. 133:156-67, 1971. See Vol. 3, p. 703. 1,042 “Reif A E. J. Exp. Med. 120:413-33, 1964. See Vol. 8, p. 136. (5/83/LS) 482 Reirrttera EL, Krmg P C, Peaando J M, Ritz J, Goldstein G & 8chtoass SF. 1a determinants on human T-cell subsets detirted by monoclon.d antihwfy: activation stimuli required for expression. J. .Ex.rr.Med. 1501472-82, 1979. 452 ReJnhera E L. J. ExP Med. 151:969-74, 1980. See Vol. 6, p. 65. 862 Rmerrthaf A S & Shevaclr E M. Function of macrophages in antigen recognition by guinea pig T Iymphncytes. L Requirement for histocompstible macrophages and lymphocytes. J. Ezp. Med. 138:1194-212, 1973. 469 ●SeU S & GeU P G H. Studies on rabbit lymphocytes in w“tro. 1. Sdrrndation of blast transformation with an amiallotype serum. J. Exp. Med. 122:423-40, 1%5. (14/84/LS) 521 Shearer G M, Rehrr T G & Garborfno C A. Cell-mediated Iympbolysis of trinitropbenyl- mmiiticd autologous lymphocytes. J. Erp. Med. 141:1348-64, 1975. 444 Shevrmh E M & Rmenthaf A S. Function of macruphages in antigen recognition by guinea pig T lymphocytes. 33. Role of the microphage in the regulation of genetic control of the immune respnnse. J. Exp. Med. 138:1213-29, 1973. 544 Shou L, Schwartz S A & Gnod R A. Suppressor celf activity after concarrrrvafinA treatment of lymphocytes from normal donnrs. J. Exp, Med. 143:1100-10, 1976. 456 ShoweU H J, Freer R J, Zlgrrmnd S H, ScfrifPmarmE, AmvarrffmmarS, Corm= B & Betker E L. The stmcture-activity relations of synthetic peptides as chernotactic factors and inducers of Iyaosomal secretion for rreutrophils. J, Exp. Med. 143:1154-69, 1976, 568 Swift H F, WUson A T & Larrcefield R C. Typing grmrp A hemolytic streptococci by M precipitin reactions in capillary pipettes. J. Exp. Med. 78:127-33, 1943. 188 1955-1985 Sc[ citations Biblfograpbic Data

446 Tada T. J. Exp. Med. i44:713-25, i976. k Voi. 4, p, 94. 5oi Timonen T. J. Exp. Med. 153:569-82, 198i. See Vol. 6, p. 306, 863 “Tomasi T B. J, E.zp. Med. i2i: iO1-24, i%5. See Vol. 8, p, 192. (47/80/LS) 494 Trinehlerf G. J, &p. Med. 147:1314-33, 1978. See Voi. 4, p, 691. 431 Uhr J W. J. E@ Med. 117:457-77, 1963. See Vol. 3, p. 704. 666 Unkelesa J C, Tobia A, (kaowskl L, Qulgiey J P, Rkfkbt D B & Reich E. An enzymatic timction associated with transformation of tibroblasts by oncogenic vimses, 1. Chick embryo fibroblast mdNres transformed by avian RNA tumor viruses. J, Exp, Med. 137:85-111, 1973. 535 Unkeleas J C, Gordon S & Reich E. Secretion of plaaminogen activator by stimulated macmphages. J. Exp. Med. 139:834-50, 1974. 470 van Furth R & Cobo Z A. The origin and kinetics of mononuclear pha8ncytea. J. Erp. Med. 128:415-3S, 1968. 428 Ward P A, Coehrone C G & Muller-Ebarhard H J. The role of serum complement in chemotaxis of leukocytes in w’tro. J. Exp. Med. 122:32746, i965. 422 Weiaanmrt G. J. Exp. Med. 116:433-50, 1962, See Vol. 3, p. 707. 451 Wu T T & Kabat E A. An anaiysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains aml their implications for antibndy complementarily J. Erp. Med. 132:21 1-X), 1970, 845 Zigenond S H & Hirsch J G, Leukmyte locomotion and chemotar.is: new methods for evaluation, and demonstration of a cellderived cbemotsctic factor. J. Exp. Med. I37:387-41O, 1973. 538 Zinkernngel R M & Doherty P C. H-2 compatibility requirement for T-ceil-mediated lysis of target cells infezted with Iymphccytic choriomeningitis virus. J. Exp. Med. 141: i427-36, 1975. 506 Zlnkernagei R M. J, Exp. Med. i47:882.%, i978. See Vol. 4, p, 691.

REY

Abbreviated bibliographic information for the eight volumes of Essays of am Information Scientist and twn 1986 Cument Conren@ essays cited in the Bibliography abnve.

GarfieldE. .Essays of on information scientisr. Philadelphia: 1S1 Press, 1977-1986. Vols. i-8. ------The articles most cited in the SCI, i%l -i982. 9. More contemporary classics of science. Current Contents (8):3-12, 24 February 1986. ------The 1,OCQarticles most cited in i%] -1982. 10. Another iOO Citation Classics caps the milienary. Current Conterrts(16):3-14, 2 I April i986.

189