Current Comments”EUGENE GARFIELDINSTITUTE FOR SCIENTIFIC INFORMATIOWJ3501 MARKET ST PHILAOELFHIA, PA 19104

The Most-Cited Papers of All Time,SCl 1945-1988. Part 4. The Papers

Ranked 301-4)0

Number 21 May 27, 1991

The fourth group of most-cited articles in the 1945-1988 Science Citation /nde.r@ is listed, togetherwith citation updates for 1989 and 1990. Eleven Nobel laureates appear as authors, bringing the total sofar to 45. The Journulof Biologica/ Chemistry published the most papers in this list ( 10), and leadsoverall with 53 of the top 400.

Through the four instrdlmcnts of this analysis covered to date, we have discussed the 3CCImost-citedpapers of at] time-looking at papers with instantaneous impacts, Nobel laureates as authors, the

journals in which the papers appeaed, delayed recognition, and perennial papers (those that have beenhighly cited year after year).

Introduction

I am often surprised to encounter readerswho are unaware that the Science Citationindex @ (SC/@) covers the literature from1945 to 1964, especially when you con-sider how important this period was to thedevelopment of science as we know ittoday. In this period, science conqueredpolio, took man into space, and developedthe field of molecular biology; computing,communications, and transportation tech-nologies brought the world closer to-gether; and, science began in earnest towrest the secrets of the physical universefrom the void. And, it is for this reasonthat, several years ago, we established aspecial project to produce citation indexesfor these years. 1,2 Knowledge from thisgolden age of science is extremely usefulin tracking the developments of ideas dur-ing this 20-yertr period and using them tobuild the science of tomorrow.

As a means to draw attention to the im-portance of these indexes, we compiled alist of the most-cited papers publishedfrom 1945 to 1988. From these efforts, wehave produced this series of essays forCurrent Contents.3-6

In the pages that follow, we have providedsome of the basic analyses characteristic of

these studies, such as the contributions ofNobel Prize winners, the impact of impor-tant journals, and the various paths papersmay take to end up among the most cited ofall time.

There is good reason to question whetheror not we should lump together materialcovering such a long period of time. Afterall, the number of papers published today is,probably, an order of magnitude greater thanit was in 1945. Therefore, we should expectthe number of citation superstars from theseearlier papers to be lower than that for morerecent papers. As a matter of fact, this ischaracteristic of much primordial work—tha{impottant papers suffer the fate of cita-tion obliteration. As I have discussed in pre-vious essays,7 citation obliteration is aphenomenon where a key development be-comes so standard within a field that re-searchers take it for granted and cease to citethe work.

Therefore, by way of commentary, ratherthan a pr6cis of selezted papers, we will con-centrate our efforts on updating the list andallow you, the reader, to interpret the signifi-cance in the context of your work,

79

Table 1. Bibkfgraphy of the fourth 100 moat-cited pape% SCI @ 1945-19%8. Papas arc arranged alpbabcticalIy.A= 1945-1988 cimions B=1945- 1988 rank. C=average nunrbcr of annual citations, 1945-1988. 33=1989 citationsE= 199Ucitations. An a.sttisk (*) indicates that tbe w waa the subject of a Cimtion Clossic @ commerrtaty. ‘lIreissue, year, and editinn of the commamuy follow tfrebibliographicmfcrcnce.

E BibfingcaPfdc Data

113 Ames B N. Aaaay of inorganic pboapbate. total pbnspbatc and pbos+hatases.144efhEnzymology&11 5-8, 1966.

45 ●AmfIIoff D. Mew for the quantitative estimation of N-acetylncununirtk =id

and tbeii application to hydmlyaates of sialomucoida. Biochcrn. J. 81:384-92,1%1 (26/80/Ls)

24 Avrarneaa S & ‘lixmynck T. The cmss-linldrrg of pmteina with glutamkiebydeand its uac fnr tbc prcpamtion of immunoadaortenta. Immundwrdstry6:53-66, 1969.

39 *kIW ‘f & Anderann P J. Hiwdmnicd mtis for acid Pk@StaSe usinghexazmiunr pamroaanifinas coupler, J. Histocherrt. Cytochem. 10741-53,1%2. (8/78)

323 *Barre-Sfnoussf F, Cbernmnn J-C, Rey F, Nugeyre M T, Chamaret S, GrueatJ, Datrguet ~ Axier.Bffn C, Vezinet-Brort F, Rooxiorrx C, Rozenbaunr W& Montagnfer L. kcdadnn of a T-lympbotmpic retmvims fmm a pseient atrisk foc acqukd immune deficiency syndmnrc (AfDS). .$cicnce 220%8-7 1,1983. (8J87t’f-S)

60 BeneaJ H A & Hfbfebrand J H. A spcctmphotometric investigatkm of theinterztion of iodine with arnmadc hydrocarbons. J. Arntv Cftrm Sk.71:2703-7, 1949.

67 Bkwk JW, DrurcarrWA M, Drrrant CJ, Ganef3in CR& Pamorts EM.Definiticm and antagonism of histamine HM-eceptom.Nuturr 236:385-90.1972.

A

1,618

1,768

B

391

330

c

70

63

D

113

56

35

34

311

69

6

9

28

%

265

18

3

46

97

47

19

157

72

116

97

43

I.7@3 356 85

1,686 359 62

1,770 329 295

1,787 320 44

1.726 346 101

1,812

1,758

50

335

314

41

6 Boas N F. Methcd for the dctcnnination of hexoaamines in tissues. J. EirJLChcrm 2C4:55343, 1953.

[9 *~wd~ ~ H~l~n [ M,Jonm E R H & wan B C L. R_~s ~

acetylenic compamda. PaIII. The prepscation of acctylenic kdones byoxidatbn of =ctylenic carbinols and glycola. J. Chrm .%c. (London)1%3945. (2fh’i’9/PC&ES)

87 Braaeau P, Vale W, Brrrguaw Ling N, Butcher M, Rfvier J & GtdDemfn RHypntbrdamicfmlypcpti~ that inhibits the secretion of immunnreaceivepiNitary gmwtb hormone. Science 17%77-9, 1973,

27 I Breatbnach R & Chambnrt P. Organization and expression of eucaryodc splitgenes coding for proteins. AnruARrv. Biochern. 50:349-83, 1981.

20 Brecher G & Crwrkfte E P. Morphology ard enumemticmof bunran blcwdplatelets. J. Appl. Physiol. 3:365-77, 1950.

0 .Bwb I E. Met.ba of paper chromatography of stmids applicable to ~ studyof stcmids in mammafkn bbcd and tissues. Biochent. J. 50370-8, 1952.(3/84/LS)

48 *Char R F. Removal of fatty acida tiom acmnraburnhr by char’cod~nt.J. Biol. Chern. 242173-81, 1%7. (13/132TLS)

72 *Ch_g W Y. m@tn plays a pivottd role in CClhd= rcgufation. SCiefrce

207:19-27, 1980. (49/83/l.S)M *Cl~ti W W. k kiIIdCS of enzyme-catalyzed reactions with W Ormore

subsrmtes or prcducta. 1. Nomcnclarure aod rareequations. Biochim. Biophys.Acm 67:104-37, 1963. (2SJ77J

11 Clemerrtf E. Ab initio cumrrutstionsin atoms and molcculcs. iBM J. Res.

1,771 327 111

1,615

1,610

1,743

394

397

338

202

41

47

1,712

1,764

1,7M

353

332

319

7g

1%

69

1,718

1,772

1,771

349

326

327

72

118

87

Devt?fop.9:2-19, 1%5. “141 ClenrerrfiE & Roettf C. Roothaan-Hatmee-Fock atomic wavefonctiom.

At. Data Nucl. Dam Tables 14:177J$78, 1974.51 ●CleweU D B & Helbrakf D R, Su~coiled cirmdarDNA-pmrein complex in

Escherichia cofti puriticatica ~ induced convemicm to-an cqwncir~acDNA focnr.Proc. Nat Amd Sci. USA 62:1159-66,1969. (8/%3/3--S)

82 Cohen S N, Cbang A C Y & Hau L. Nonchmmoacmwdantibiotic rcsistame inbxteria genetic tmnafomrationof .&heri.chia coli by R-factcx DNA.Prwc. Nat. Aced .$ci. USA 6921104, 1972.

@ .Cde K S & CA R H. Dispemirm rrndabampticarin diekbica. I. Aft.emadng

CIUCWrtCbrXWtWiStiCS.J. Chem. Phys. 9341-51, 1941. (3==)22 *de Duve C & W’attiaux R Functinna of Iyaoaomcs. Annu Rrv. Physio/.

28:435-92, 1965. (7f85/LS)

1.824 311 107

1,658

1,817

375

313

38

79

80

ABCDE1,837 301 153 374 399

1,707 355 47 17 14

1,809 315 101 81 60

,661 374 66 49 47

,Wl 382 78 53 63

,711 354 78 52 43

,784 321 53 128 120

,632 387 37 12 16

,745 336 159 210 161

1,715 351 72 27 24

l,&i7 373 39 10 9

1,837 301 102 153 148

1,679

1,732

1,767

1,658

1,644

1,681

1,650

1,779

1,672

1.6438

1,612

1,617

1,675

1,628

1,633

365

344

331

375

380

363

379

324

370

399

396

392

369

389

386

70

64

74

38

38

140

49

71

119

50

58

62

168

37

102

Bibiiographk Data*Dewfer M J S & ‘TMelW. Grorrmlstates of molecules. 38. ‘IlreMNDO mctbnd.

Appmximationa and parameters,J. Amm Chem. SOC.95MLW9-907, 1977,(14/85/f3T&AS; 14/85/PC&fiS)

OLscheZ & Sbefflea L B. A specific color reaction of metbvlnentnaea and a. .spectmpbotnmetrk micronr&hndfor their detemrinadnn. J, BioL Chrm17s595-f503. 1948.

IMchffeId ~“fieltre W J & Popk J A. Self-consistent molecuktr-mlitslmedmds. IX, An exterr&d Gaussian-w basis for mnlecular-mbitid studies ofnrganic molecules. J. Chem Phys. 54724-8, 1971.

DftbnerJ C & later R L. A simple, spccitic spray for the detection ofphoapholipids on thin-layer cbromatngmrrmJ. Lipid Res, 5:12S7, 1964,

*Doyle PA & ‘Lhmer P S. Relativistic Hartrw-Fnck X-ray arrdelectronsurttdrg factors. Acts CrystrellogzA—Cryst. Phys. 2439G7, 1%8.(291fWET&AS)

*Deucferey ~ hmmnann ~ Ivarrkotic S & Schmahl D. OrgarrnempecarcirmgeneWkkmrgen bei 65 vemcbicdcnen N-Ni~VerbirArrrgen anBD-Ratten (Organnmpic carcinogenic effects of 65 different N-nieman-compourrdson BD-rats). Z Kmbsforsch 69:103-201, 1%7. (17/81/LS)

OrrnrrettC W. A multiple compariann prnmdwe for comparing severaltreatmentswith a contrnl, J. AmeK Stafirt, Arsn. 50 10%- 1121, 1955.

Elson L A & Morgan W T J, A calorimetric mctbnd fnr the rktcmrination ofglucnsarnine and Cbrmdmaamiele.Biachern J. 27:1824-8, 1933.

*EYP L, Prowae S J & Jrmkbt C R Ianladon of pure IgGi, IsOti ad IgGrLIimmurmglobrrhnstlom mouse acmm usiergprotein A-scpbrunse.Irrvnwrochemishy 15:429-36,1978. (12f89LS)

Fahey J L & McKelvey E M. Quantitative detemninatinnof serumirmmnmglobuhm in antibndy-agar plates. J, 6nrnrenoL9484-90, 1965.

Folhr O & Chralteu V. On tymaine and hyptopbane dctcrminatinnainpmteina. J, BioL Chem. 73:627-50,1927.

G-earYW J. Theuse of conductivity measurements in ormnic advents for tbcckteriaation of cnnrdirmtkmC-nmpauda. Cooni C~rrr. Rev 781-122,1971.

101 95 W2ehan E A. A genemlii Wdcoxnn test for comparing arbitrarilysingly-cenanred samples. Mrmefti 52:203-23, 1%5. (39/79/LS)

8 7 GeU-Marm M. Synrm@iea of baryons and mesons. Phys. Rru 125:1067-84,1%2.

64 73 Gfiea K W & Myers A. An improved diphenykarninemctbnd fnc the estimationof deoxyribmmckic acid. Natare 20693, 1965.

24 8 hod C A Kramer H & Somog@ M. The detmminatinn of glycogen. J. BioLChsm. 10f1485-91, 1933.

22 19 Gnndwln T W & Morton R A. TIE spccimpbotnmetric detenninatinn oftymine and tryptnpbarrin proteins. Biachem, J. 40628-32, 1946.

12E 137 Gordon T, CaatelLiW P, HjorOand M C, Karmef W B & Dawber T R. Highdensity lipoprotein aa a prntec!ive factnragainst cnmrraryhart dkeaae. ArnaJ. Med. 62:7LT7-14, 1977.

69 M *RUDIDOIKIG .S,4 correlation of reaction mtes. J. Arrw Chem Sot. 77:3M~,1955. (34/851ET&AS; 34/85fPC&ES)

i 1 *wnwm H P, Herman F, Lea J D & Skifhnan S. HF8 atomic WIttcringfactms. Acts Crystaflogz 17104CM, 1964. (3W77)

85 8 I *Heltim A & ShnOns K .%hrbih-mtionnf membranes by detergents. BIOChimBiophys. Acts 41%29-79, 1975. (22185ilS)

43 39 *Huggett A S G & Nfxon D A. Use nf glucose nxidase, peroxidaae, andwdianisidirre in determination of blocd and urinary glucose. L.uncst2368-70,1957. (21/81/CP)

i 2 Karrrovaky M J. SimpIe methods for ‘“stainingwith lead” at high pH inelectron micmscopy. J. Bioplrys. Biochem. C@ 1I:729-32, 1961.

61 47 Kat@trs NL Letter to editor. (Vicinal proton cnupling in nucleac magneticresonance.) J. Amen Chern. SW. 85:287@ 1, 1%3,

184 181 Kebabbtn J W & Cofne D B. Multiple receptors for dopamine. Nutrert?277:93-6,1979.

10 7 ~3f, J. Ilre calorimetric determination of @nspbnms. Biochem J. 26292-7,

184 147 *Kosterlitz J M & TlwuLew D J. O&ring, metmtability and pbasc transitionsin two-diiezraicnal systems, J. Phys. C—So/id Store Phys. 6118 I-203, 1973.(In press.)

81

ABCD1.835 306

1,617 392

1,773 325

1,782 323

1,737 340

1,734 342

1,641 382

1,717 350

1,678 367

1,835 306

1,821 312

1,627 390

1,721 348

1,668 372

1,836 305

1,642 381

1,681 363

1,688 358

1,833 308

1,636 384

1,652 377

1,832 309

1,6Cr3 398

1,837 301

1,678 366

1,761 334

1,764 332

1,800 317

1,671 371

44 52

74 85

104 114

52 69

40 27

% 55

57 4

115 71

153 287

46 23

59 68

78 64

215 201

46 184

131 95

37 58

120 87

73 25

73 40

68 78

45 33

76 200

89 63

54 10

80 39

84 211

71 99

41 62

46 35

E BibU~pbfc Data40 Kmdtz M. Crystalline soybean uypsitr inbibitar. II. Gencrsl prcprdes. J. Gerr.

f%)WiO~ 30291-310, 1947.79 ●~y p E & K@f~oWky M. Methud fur dre isukaticmof intact iSklS of

Langwhsns tlom dreratpsncmss. Diabetes 16:35-9. 1%7. (fU81/LS)w •La~II C.B. E-imuno m.wy, Scrmd.J. ClirL~. fnvsst.

29(SuPp. 124):21-37, 1972. (48/90CM; 48/9WLS)51 Lmnox E S. Transduction of linked genetic chamctem of the Irmt by

bsctcriupbage P1. Wtiogy 1:190-206, 195S,25 o~v 0 H & LOP J A. The determinsdun Of iIVWS~iCPbospbsk in ~

presence of labile phosphate esters. J. Biol. Chsm 162421-8, 1946.(3 U81/Ls)

46 MsisRl J V. Polyacrylumide gel electmpboresis of virsl proteins. .Meth.Wtiogy5:179-246, 1971.

1 MsrsdeU J D & Hershey A D. A fnwtionating column for snalysis of nucleicacids. AnaL Biochem. 1:66-77, 1960.

57 Msrcb S C, ParUdr 1 & Custremsas P. A simplified nreihcd furcysnogcnbrmnide activation of agamse fnc affinity cbmmstugmpby. Anaf. Biochem.W. 149-52, 1974,

255 MsrkweU M A L Ham S M+Bieb L L & Talk-t N E. A modification ofthe Lowry p+wedure to simpli~ protein dcterminatiun in membrsne andIipupmtein smnples. And Biodrsm, 87:2061O, 1978.

20 M-J B & My D M. Determination of inmgrmic pbrrspbate.Anal. Chem21:%5-7, 1949.

60 McFsrfsne A S. EBiciesrttmce-kbcling of prnteins witlriodine.Ncuwe 182:53,

61

164

238

84

47

85

38

46

61

27

169

67

5

37

290

102

79

12

19S8,McMUfan W L. Tmnsitiun temperatureof strrrng-coopledsuprcnnductws.

Ptlys. Rev 167:331-44, 1968,●Mewing J, Crea R & Seebrrrg P H. A system for sbatgun DNA 5equencin8.

Nucl. Acid Res, 9:309-21, 1981, (In press.)Metrapofls N, Rosenbfutfr A W, Rnsenbhrtfs M N, TeUerA H & TefferE.

Equatio. of state calculations by fsst computing machines. J. Chsm. Phw.21:1087-92,1953.

*Mfdrefl R FLInositol pbcapbolipids and ceO surface rczcpkrrfunctinn.Binc/rirn. Biophys. Acts 415:81-147, 1975. (5W38/CM)

*MUes A A, Mfsra S S & Irwin J O. ‘fhe estimation of tlw bactakidsl puwer ofthe blcmd.J. Hyg. 3&73249, 1938. (37/791LS)

●MiUer G J & Mffler N E. Plesma-highdensity -lipapm+ein cnncermation snddevelopment of iscbaemic hcmtdisease. I@tcer 1:16-9, 1975, (15/81/LS)

*MitcheU P. Chemiosmotic ccmpling in oxidative and pbotusyntbkphospbotylatiun. Bio/. Rev Cambridge PhiL SK 41:445-502, 1966. ( ltV78)

●MoUenbauer H H. Plastic emWn8 mixtmw fcwusc in elcctmn micmsmpy.Sfain Teclmof 39111-4, 1964. (27/87/LS)

Mod lL Tmnspurt, collective nrc4imI,snd Brnwnian mtiion. Prog. 77WOZPhys.#@to 33:423-55, 1%5.

MtdffkerrR S. Molecular compmmds and their spectra. IL J. Anw CIwrn. SOC.74811-24, 1952.

*Ne4der J A & Mead R A simplex method for fimctiun minimizstiun.CompLU.J. 7308-13, 1%5. (lW9/ET&AS)

Nevifle D M. Molecuhu weight determinatiurrof pruteindodecyl suffatecomplexes by gel ekctrnphcsis in a discortMuaas buffer system. J. Bid.Chem. 246:6328-34, 1971.

Nffssun S G. Binding states of individual mrcleons in suungly deformed ncdei,Mat. Fys. Medd Dan. W Sefsk 29:3-68,1955.

*Niswender G D, MIdgley A ~ Monrae S E & ReJchert L E. Rafioimm@assay fw mt luteiniring hmrnune with arrdavineLH scmm and wine LH-’3’I.Pnx SW. tip. BioI. .Med 128:807-11, 1%8. (44NM.S)

North ACT, PtsUUPSD C & hktheWS F S. A semi-empirical methud ofawn COITCCtiOn.Acts CrystaUogz A--CrySt. Phys. 24351-9, 196s.

Omurs T & Satn R The cabcm mmmxiddrinding pigment of livermicmsmnes. II. Solubilizaticm, pmilication, and pmperdes. J, BioL Chart2392379-85,1964.

Onsager L. Elecoic muments bf molecules in liquids. J. Arner Ckmr. SK.58 M86-93, 1936.

Ouchterltmy O. Antigen-antibmly mactiom in gels. Acts Pdnl. A4icrobiof.Scond 32:23140, i953.

82

A1,742

1,694

342

1,615

1,686

1,805

1,635

1.784

1,7451,685

1,727

1,608

1,713

1,685

1,837

1,793

1,735

1,676

1,629

B339

357

54

394

359

316

385

321

336362

345

CDE124 105 92

47 32 47

202016

77 65 62

169 124 121

201 330 281

65 140 144

4686

40 25 295641

144 186 197

399 73 76 76

352 156 193 214

361 99 71 68

301 102 65 65

318 47 41 36

341 193 354 356

368 99 42 35

388 44 65 40

Bibfiogmpfrfc DataPalade G. fntncelhrlar rtsprctsof the pmcssof protein synthesis. Science

189347-58, 1975.Pople J A. Elomcm intendrm in urrsaturatedIrydrrxarbons.Tronr. Fara&zy

sm. 491375-85, 1953.*Pmdik M D. Starch gel in ekmophomsis in a discontinuous system of buffers.

Nafrme1801477-9, 1957. (15/84/LS)Refd R V. Localpbermmcrmlogicatnuclecar-nuclenrrpotentials. tin, F’frys.N. Y

5&41 1-48,1968.Rosenkerg M & Cmrrt D. Regulatory sequerrres involved in the prumotion

amf terminatia of RNA trmrscriptirm.AnJM Rev Gerret.13:319-53, 1979.Sarrger F, CouLvon A& Barrefl BG, %rdthAJH&RoeBA. C3orrirrgin

single-stranded bacter@bage as an aid to rapid DNA sequencing. J. Mol.BioL 143:161-78, 1980.

SaVitzky A & GofayM J E. SmnnrMngand differentiruinnof data bysimplified least squares procedures. Anaf. Chem 36:1627-39, 1964

ScfrnefrferW C & Hogebrmrn G IL Irrtnwelkrlardisoihution enzymes, V,Furtherstudies on the distribution of cytochrome c in rat liver b+xrrogenates.J. Mol. C/rem. 183:123-8, 1950.

Slater J C. Atomic shielding constants, Phys. Rev 3657-64, 1930,Srnitfdss O. An improvd pucedure for starch-gel ekctmphorcsis; tirrtber

variations in the serum proteins of rrorrmdindividuals. Bicxfrem J. 71:585-7,1959.

*SnkoloffL, Rehic%w KermedyC, Des ItwdersM ~ PatkskC S+PeMgmvK D, Sakumfa O & ShfrrohmnM. The [’4CkJeoxyglumse rrrethndfor themeasurement of local cerebral glucose udti.mtion: dreory,pmxdure, andrrorrrralvalues in the conscious arrdarrdredzed dbhro rat.J, Neumrhem28:897-916, 1977. (271891CM; 27189LS)

SottncswaG L, KrryfenstiermB, Ermter L & BergstrandA. Anelectron-transport system associated with the ouw membrane of livermitochcmdria.J. Celf BioL 32:415-38, 1%7.

Spitzer R 1+EndicottJ & Robins R. Researchdiagnmticcriteria.Arch.GerLP~hiat. 35:773-82, 1978.

Weiner AL, ParkerC W & KiprdsD M. Radioirnnmrmassayforcyclicrmcleaides.1,Pqwatirm of arrtibndicsand icdinared cyclic rruclentkk.J. BioL Chem. 247:11 WI-13, 1972. (38B5A-S)

UngerstedtU. Stereotaxicmapping of the rnorroamirrepathways io the ratbrain.Acts Physid Scud (Supp. 367):148, 1971.

*Us4nff H H & Zm’rrhrr3L Active trenspmt of srrdiumm the source nf electriccurrent in the short-circuited isolated tlog skin. Acts Physiof. Scund211W27, 1951. (35/81iLS)

Wallemtehr S, Zucker C L & Ffelss J L. Smrrestatistical methods useful incirctdatkm research. Circ. Res. 471-9, 1980.

WebarK, PrirrgleJ R & Dshom M. Measrrrmnentofmolecutar weigbtv byelmtropboresis on SDS-acrylami& gel. Mesh..Eiuyrrrology2&3-27, 1972.

WestphalO, LrrderftzO & Bfster F.Uher die Exrraktiorrvon BakterierrmitPhenolr’t%ser (Extmctiorrof bacteria with phermlfwater).Z NaosrforschSect B 7:148-55, 1952.

1,724 347 78 14 15 *w~ K R & Wang K-T. Separation of dansyl-arnino acids by PoIYarnide

layer chromatography. Biorhim Biophys. Acsa 133:369-70, 1%7. (35/84R.S)1,651 378 49 31 25 YenrrrrE W & Cor3drrgE C. Tbs determination of amino-acids with rrirrhydrin.

Anafyst 80209-14, 1955.1,832 310 51 37 51 *ZIWI& A, N B & Boyle AJ. A ncw merbcd for the direct d-nation of

semnr chotesreml. J. .Lz6. Clin Med. 41:486-92, 1953. ( 12/81/LS)

Most-Cited Papers: The “Fourth 100” citations 1945 to 1988, and 1989 and 1990citations, respectively.

Table 1 lists the papers ranked from 301 The authors of 38 of these 100 papersto 400, based on citation totals from 1945 have written Citation Classic@ commen-to 1988, in alphabetical order by the pri- hmies on the listed works. These are indi-mary author’s last name. The columns that cated by asterisks. The Current Contents ~precede the bibliographic data include total (CC @) reference for each commentary fol-citations 1945-1988, rank, average annual lows in parentheses. Inclusive of this in-

83

Tabte2. Ctsrunrdogimtdktrttrutionof tbe fourth 100mmkited papers fmm the SC] @-’,194S-1988. Data inparentheses sre cmrndated through the top 400 most+ited psper-sidentified to date.

Average AverageNmrsber of Cltaticms 1988

Decade Paps Total Cites Per Year Ctics

1920s1930s1940S1950s1960s1970s1980s

Total

I (4)6 (15)8 (37)

20 (86)33 (142)26 (91)

6 (25)

100 (403)

1,667 (23,9’26)10,105 (48,330)13,961 (119,353)34,440 (470,895)56,151 (460,113)45,106 (358,309)10,410 (62,898)

171,840 ( 1,543,924)

38 (136)38 (79)42 (76)49 (162)72 (132)

119 (268)214 (376)

82 (175)

6 (102)29 (57)39 (92)47 (236)68 (123)

142 (446)285 (663)

88 (246)

stallment, I73 of the 400 most-cited papershave been featured as Citation Classics.

Table 2 provides a chronological distri-bution of the fourth 100 most-cited papersand, in parentheses, the data accumulatedthrough the top 400, inclusive. The decadewith the most papers and largest numberof accumulated citations is the 1960s. Notsurprisingly, since they have climbed thelist in so few years, papers published inthe 1980s have the highest annual citationaverage as well as 1990 citedness. So faramong the 400 papers, not one was pub-lished in 1942, and only three from 1941and two from 1943 made the list. Whetherthis reflects an overall decline in publica-tions in wartime is not certain.

Papers from the 1980s: “Bullets”

Keep in mind that if our starting databasewere 1945 to 1990, instead of 1945 to1988, there would be many changes inranking, especially with the papers from re-cent years. Only six papers in Table 1 werepublished in the 1980s, each averaging 200or more citations per year-the only ones inthis list to do so. Even among those papersranked 201-300, only papers published inthe 1980s were cited at this rate. However,65 of the pre-1980 papers in the top 200 av-eraged more than 200 cites per year.

If you add columns D and E to column A,the transient nature of these rankings be-comes apparent. Consider, for example, thepapers by B.N. Ames, E. Clementi, andM.J.S. Dewar-over the last two years, all

have been cited far above their listedaverages.

“Bullets” typically start off strong andquickly accelerate. A good example is themost recently published paper in the table.It also is the first AIDS paper to make ourmost-cited listing. The citations to this1983 article from the Montagnier group inParis concerned the isolation of a T-lymphotropic retrovirus from a patient atrisk for AIDS. Coauthored by FrancoiseBarre-Sinoussi and colleagues, Pasteur In-stitute, citations to this paper jumped from27 in 1983 to 146 in 1984. Between 1983and 1988, the paper was cited 1,770 times,averaging nearly 300 per year, with a highpoint of 435 in 1987 (see Figure 1).

As they noted in their Citation Classiccommentary:

[The] idea that our viral isolate was anew retrovirus that might tx the cause ofthe disease was not very well accepteduntil it was confined one year later byother laboratories .. . Thus, this paper ishighly cited because it provided evidencefor the role of a new hurnarr retrovims inAIDS.8

This paper is one of four 1980s articles inTable 1 that have been highlighted in previ-ous essays identifying papers highly citedwithin two years of publication.g, 10 Othersinclude a description of multicellular split-gene coding for proteins (R. Breathnach),lla method for “shotgun” DNA sequencing(J. Messing),l I and a review of calmodulinin cellular regulation (W.Y. Cheung). 12Fig-ure 1 illustrates the citation records of the1980s publications from this study.

84

lkbte 3. Nobd Prize winners wfth pspem ranked between 301 and 400 in tie SC1@,1945-19%3A.Nobelists,listed afphabeticaly. B=year snd @e. C=affiliation.

A BJames W. Btack 1988fiysiology m MedicineSrantey N. Cohen 198&Physiology or MedicineChristian & Duve 1974Physiology or MedicineMurrayGeU-Marm l%9iPtrysicsRoger Guillemin 1977/Pbysiotogy or MedicineAttkd D. Hembey 1969iPbysiology or MedicinePeter Mitchell 1978K!hemistryR&err S. Muffiken 1966KXremishyLass Orrsager 1968KhemistryGemge E. Pslade 1974Ptrysio@y or MedicineFmfaick Ssnga 1958 & 1980/Chemisrsy

We should note here that one of the mostcited of the other pioneering AIDS papers,by Robert Gallo and colleagues, 13also thesubject of a Citation Chssic commentary, 1dhad beat cited 1,496 times through the endof 1988, falling just short of the cutoff forthe top 400.

In his Cfassic commentary on this 1984paper, Gallo discussed the detection of theHTLV-111 virus and the subsequent citationimpact of the papers published by his group.

The fust published detection of thevirus was from a patient with lymph-node

enlargement, but tests of sera origirrall yshowed less tharr 20 percent of AIDS pa-tients had antibodies to LAV. No doubtthis was due to insufficient virus produc-tion. We found and descritnxi 48 isolatesof H’lZV-Iff (now generically HIV) from

cSmith, KhIK snd French LaboratoriesStanford University School of MedicineRockefeller UniversityCalifornia Institute of TechnologySalk InstituteCarnegie fnstirurionof WashingtonGlynn Research LaboratoryUniversity of ChicagoYale UniversityYale UniversityMedical Rewsrch could Laboratory of

Molecular Biology

patients with AIDS and at risk; none ofthe 115 nonrisk healthy people yieldedsuch isolates. We think the 1984 Sciencepapers are frequently cited because it wasthe first time anyone stated that theyknew the cause of ADS. 14

An article in the New Scientist,ls by Ali-son Rawling, Sydney University, Australia,analyzes the citation trends for the Galloand the Barre-Sinoussi papers. She notesthat, after the very public contest for prior-ity in the discovery of the AIDS virus be-tween the two groups, the scientific com-munity has increasingly cited theBarre-Sinoussi paper as the primordialpaper on HIV. Without drawing a directconclusion, she indicates that this may be aconscious choice by the scientific commu-nity to disregard the formal settlement of

Ngrsrw 1. Citation records for 19fJs3spstpess rsudsed between 301 and 400.

450

400

350

300

250

200

150

100

50

0

-- ._. . Sarre-Slnoud F.-.=. - .-

walknswtn s

M@8sliw J

-WV

’80 ’81 ’82 ’83 ’84 ’85 ’86 ’67 ’66

Year

85

Tsbte 4. The ]oumaJs that pubfkhed the fourth

mm of nmsl-dti SC{@ papees! 1945-1988.A=title, with fust year of pablicarion in parenthe-ses. B=numberof most-citedardclca appearinginthe journal

AJ. Biol.Cbem. (1905)Biocbem.J. (1935)J. Amer. Cbem. SIX. (1879)Nature (1869)Biocbim. Biopbys. Acts (1947)Science (1880)Amd. Biocbem. ( 1960)J. Cl-em, Fhys. (1931)Phys. Rev. (1893)Am Crystallogr. A-Cryst. Phys. (1968).-@a Physiol. Stand. (1940)Amt. Cbem. (1929)Immm-mhemimy (1964)tit (1823)Meth. Enzymology (1955)Pmt. Nat. Acad. Sci. USA (1915)Acts Crystdlo.gr. (1948)Acts Patbol. Micmb]ol. Stand. (1924)Amer. J. Med. (1946)Analyst (1877)Am, Phys. N. Y. (1957)Annu. Rev, Biwbem, (1932)Amm. Rev. Genet. (1967)Amm. Rev, Physiol. ( 1939)Arch. Gen, Paychiat. ( 1959)At. Data Nucl. Data Tables ( 1969)Biol. Rev. Cambridge Phil. SIX. ( 1936)Biomeuika (1901)Circ Res. (1953)Comput. J. ( 1958)Cccl. Cbem. Rev. (1%6)Diabem (1952)IBM J. Res. Develop. (1957)J. Amer.Stadst.Aa.sn.(1888)J. Appl. Pbysiol. (1948)J. Biophya Biocbem. Cytol. (1955)J. Cell Biol. (1%2)J. Cbem. $x. (London) (1849)J. Gen. Pbysinl. (1918)J. Histcchem. Cytcchem. ( 1953)J. Hyg. (1901)J. Jmmmml. (1916)J. Lab. Clin. Med. (1915)J. Lipid Res. (1959)J. Mol. Biol. ( 1959)J. Neumcbem. (1956)J, Phys, C--solid State Pbys. (1968)MaL Fys. Medd. Dan, Vld. Selak. ( 1917)MedI. Viilogy (1967)Nuc1. Acid. Res. (1974)F’mc.Sm. Exp. Biol. Med. (1903)Pm& Them. Phys. (1946).Smnd. J. CJii. Lab. Invest. (1949)Stain Tectmol. ( 1926)Tnma.Faraday SW. (1905)Vrology ( 1955)Z, Rrebaforsch. ( 1903)Z, Narurforach.Sect. B. (1947)

B

1066544333222222211111I11II11111II11111I111I1111II111111111

the dispute—a settlement which states thatthe two groups jointly share the digcovery.

Nobel Laureates

Eleven Nobel laureates authored papersin Table 1, bringing our total to 45Nobelists who have authored 66 of the top400 papers. Table 3 lists the 11 laureateswith papers ranked between 301 and 400,the years and categories in which they re-ceived their awards, and their aftliations,as listed on their papers.

Journals of the SC] Top 400

Table 4 presents the 58 journals that pub-lished the papers covered in this segment ofthe series. As expected, the Journal of Bio-Iogical Chernis~ry (JfJC) leads with 10 pa-pers, bringing its cumulative total to 53.And for the third time, the second highesttotal comes from the Bwchemicai Journal,which has 6 articles here and 24 overall.

Among the 400 most-cited articles listedto date, three were published in French andfive in German. In the previous three lists,review journals did not show up. In thislisting, the Annual Reviews series-in Bio-chemistry, Genetics, and Physiology-ap-pear for the fmt time.

Journals publishing at least five articlesamong the SCI Top 400 are shown in Table5. These 19 journals account for 237 papers,or 59 percent of the total. Interestingly, fiveof them-Natum, Journal of the AmericanChemical Society, Science, Physical Re-view, and Journal of Experimental Medi-cine—were first published in the 19th cen-tury. In contrast, three started in 1960 orlater.

“Shooting Stars” and Obliteration

Eleven papers in Table 1 can be classifiedas shooting stars. These papers accumulatecitations quickly and, often, just as quickly,drop off with long citation “tails.” For ex-ample, a typical case history is the 1959methods paper on a procedure for determin-

86

ing serum proteins in normal individurds,by O. Smithies, Connaught Medical Re-search Laboratories, Toronto, Ontario, Can-ada. In 1%6, seven years after publicationin the Biochemical Journal, amual cita-tions to the reticle peaked at 286 then de-clined to double digits three years later.From 1979 on, it has fewer than 16 cites an-nually, with only a single citation in 1990.Cumulative through 1988, the paper has1,685 citations, with an annual average of56. Figure 2 gives a graphic representationof this paper’s history.

In a recent conversation with CC, Smith-ies characterized this as an evolution of thistype of paper-highly cited when it was thefiist, best method and, eventually, replacedby papers detailing newer, often simplermethods. In this case, Smithies 1959 paperwas replaced by the work of U.K.Laemndi16 and B.J. Davis, 17 numbers twoandseven in this series. 3.4

The fact that this paper was su~rseded

by subsequent procedures does not in anyway dim the importance of this work. Inrecognition of his efforts in gel electropho-resis, Smithies received the 1990 GairdnerFoundation award.

Most of the shooting star papers parallelthe Smithies publication history. They aver-age from 47 to 96 citations a year then falloff within two to seven years after theirhigh points.

Tabfe5. Jommalstit pubtishwl five or more ofthe top 400 most.cited SCI @ fm~ 194S.1988. A=titJe,withfirstyearof publicationin pa-rentheses. B=number of most-cited pspem sp-pearing in thejommd.

A

J. Biol. Chem. ( 1905)Biochem. J. (1906)Nanuz ( 1869)AA. Biochem. ( 1960)J. Chem. %YS. (1931)J. Mol. Biol. (1959)Rec. Nat. Acad. Sci. USA (1915)J. Amer. Chem. SW. (1879)Science (1880)Phys. Rev. (1893)J. Cell Biol. (1%2)J. Histoshem. Cytochem. ( 1953)Me!h. Enzynmlogy ( 1955)AA Chem. (1929)Biocbim. Biophys. Ada (1947)J. Exp. Med. (18%)Acts (lystdloby. (1948)Acts CrystsdtOgr.A-Cryst. ~yS. (] %8)J. fnunursi. (1916)

B

5324!81414131311109888766555

‘IWO of the papers me from the 1950s,eight from the 1960s, and one from the1970s. Whether we can attach any signifi-cance to the high percentage of shooting starpapers from the 1960s is doubtful. However,Leon M. Lederman, winner of the 1988Nobel Prize for physics, characterized thisas the golden age of science. His 1962 paperexemplifies how primordial referenceseventually decline and are absorbed into thecommon wisdom. This paper, coauthoredwith, among others, Melvin Schwartz and

Figure 2. Citation Mstory of O. Smlthtes %hooJJngStaF’ paper.

300 T

250.

200- -

150 -

1oo- -

50- -

0.’58 ’60 ’62 *64 *66 *68 *7O *72 ’74 ’76 ’78 ’80 ’82 ’64 ’86 ’88

Year

87

Figurs 3. Citation reeords of papsrs showing delayed rtxognkion.

250

200[

#’: MSW@S N

150- -g

j IIJO -

//

50 -- ,/ ~--- ./

This [synthesis of acetylenic ketones]proved to be an elegant method and gaverise to the term “the Jones reagent” whenit was found applicable to the oxidationof a variety of compounds.zo

The 1953 paper, in the Journal of Chemi-cal Physics, on calculations by fast comput-ing machines, deserves to be singled out.published by Nicholas Metropolis and col-leagues, Los Alamos Scientific Laboratory,New Mexico, and the University of Chi-cago, this publication, through 1988, hasgarnered nearly 1,700 citations, an averageof 46 per year. Three interesting points: thepaper has not yet peaked (its highest annualcitation count was 238 in 1990); one of thecoauthors is Edward Teller—at the Univer-sity of Chicago when the paper was writ-ten—who, along with mathematicianStanislaw Ulam, developed the thermonu-clear hydrogen bomb; and, one of the LosAlamos coauthors was Teller’s wife, Au-gusta H. Teller.

More than 25 papers from the late 1920sthrough the 1960s have been referencedfairly steadily through the decades. We callthese papers “perennials.” The oldest paperlisted is the classic by Otto Folin andVintila Ciocaltetr, Harvard Medical School,Boston, Massachusetts. It was published in1927 in the JBC. This is the fifth JBC paperthat dates from the 1920s or early 1930s.The citation record of this methods paperindicates that, between 1945 and 1960, itaveraged 34 citations annually. In 1961, itreached a peak of 69. Since then, the num-ber of works citing it gradually declined,with only nine in 1990. Other perennialshave similar citation “biographies.” Figure4 illustrates this paper’s year-by-year cita-tion record.

Metheds papers also characterize thegroup of1930s perennials. These cover thedetermination of glucosanine and chon-drasarnine (L.A. Elson), glycogen (C.A.Good), phosphorus (E.J. King), elec-

tric moments of molecules in liquids(L. Onsager), atomic shielding constants(J.C. Slater), and the estimation of the bac-tericidal power of blood (A.A. Miles).

A Classic commentary on this last paper,by Ashley A. Miles, London Hospitrd Med-ical College, England, touches on the rea-sons for the paper’s longevity.

I suspect, from the references I havecome across, that the paper is most com-monly cited for the description of the sur-face-viable count for bacteria .... From thescientific literature I have subsequent yread, the bactericidal method and the sta-tistical consi&rations in determining thesignificance of differences in killing rates

appear, like the mule, to have nothing toshow in the way of offspring; though asfar as my own work is concerned, theyare coming home to roost in some currentwork on the bactericidal power of micro-phage populations. ‘fhe surface-viablecount evidentl y—and gratifyingly-liveson.2 I

The 1940s-vintage publications highlightspectrophotometry: for the determination ofmethylpentoses (Z. Dische) and the interac-tion of iodine with hydrocarbons (H.A,Benesi). Other topics include descriptionsof the general properties of soybean trypsininhibitor (M. Kunitz), dispersion and ab-sorption of dielectrics (nonconductors ofelectrical current) when exposed to alterna-ting current (K.S. Cole), and the determina-tion of inorganic phosphate in the presenceof unstable phosphate esters (0.H. Lowry).

The largest number of perennials in Table1 was published in the 1950s. These 12 pa-pers represent a wide range of topics studieson amino acids (E. W. Yemm), proteins (A.S.McFadane), bacteria extraction (O.Westphal), the distribution of enzymes(W.C. Schneider), molecular compounds(R.S. Mulliken), genetic linkage (E.S.Lennox), electron interaction in h@mcar-bons (J. A. Pople), the transport of sodium inepithelial tissue (H.H. Ussing), determinat-ion of hexosamines in tissues (N.F. Boas),chemical reaction rates (G.S. Hammond),blood in urinary glucose (A.S.G. Huggett),and, finally, blood platelet counts (G.Brecher).

89

conclusion

There are trends that stand out in these es-says. Among them: Nobel Prize winnershave participated as authors on one out ofevery six of the top 400 papers; high-im-pact journals dominate the publication ofthese most-cited papers, with 13 journalsaccounting for more than half of these pa-pers (203 of 400); and, while the “shootingstars” of the group are the papers from the1980s, having an impact immediate enoughto make thk listing, there continue to be

“perennial” papens that have been citedsteadily for decades.

Obviously, the essays describing the top400 papers, 1945 to 1988, are really a “snapshot” of the SC1 data at the end of 1988. Youcan see by the 1989 and 1990 data in Table 1that the rankings of many of these papershave been dramatically altered already. Thisis a reflection of both the rapidly changingdynamics of science and the exrraordinrwygrowth of the literature and exemplifieswhat is so exciting about science.

01%1 L9

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