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Number 35
Essays of an Information Scientist, p254, 1979-80
Current Contents, #35, p.5-14, August 27, 1979
Moat-Cited
Biochemfsq
Number
35
Adck
and
of the 1%0s.
2.
~OkWf!Xr
Bicdogy
August 27, 1979
Recently
we listed the most-cited
physical sciences articles of the 1960s. 1
To continue
our discussion
of that
decade’s scientific literature we have
now compifed a list of the most-cited
biochemistry
and molecular
biology
papers.
These lists of most-cited articles are
selected by sorting and ranking the Science Citation Index@ (SCP) files for the
18-year period from 1%1 to 1978. Over
seventy-one
million citations to authored items are included in the SC1
data base for those years.z About 11
million of those citations are to papers
published during the 1960s. I estimate
that over 60,000 biochemistry papers
were published during that time.3 To
select a limited number of papers from
this massive volume of publication may
seem like a futife exercise. Nevertheless,
by identifying this sample I think we
learn quite a bit about the main directions and logistics of biochemical
research in the 60s.
I do not wish to suggest that these articles were the most “important” intellectual contributions to biochemistry
in that decade. Many of the papers
would qualify as such, but many authors
have indicated to us that they published
other papers that are more representative of their best work. Nevertheless, 1
find it hard to believe that it is a coincidence that these authors have so often
been recognized by their peers. Put it
this way—the authors of highly cited
papers also tend to publish other wellcited papers.
254
In providing the frequency of citation
I do not suggest that this is an indicator
of relative “value. ” In the case of a
theoretical
paper it may be an indication of impact or influence. For a widely
used method paper it may simply indicate just that. Citation data may be
the only convenient means of determining the impact of a new methodology.
Others might prefer to use the annual
sales of a particular biochemical reagent
or instrument.
If nothing else, citation frequency
does allow us to make comparisons between the kinds and amounts of activities symbolized by the articles involved. I hope that the alphabetical arrangement by first author under each
category will discourage invidious comparisons.
There are 101 articles listed in Figure
1 which follows this editorial. Originally, I intended to limit the study to 100
articles. Because both parts of Omura’s
work on liver microsomes appear on the
list, I decided to add one more paper.
Every paper on the list was cited more
than 564 times during the period
1%1-78. Thirty-nine were cited more
than 1000 times and 11 more than 2000
times. The average paper received 1294
citations. This means that it was cited at
least 72 times per year. You can better
appreciate
the significance
of this
number when you consider that the
average article published in a journal
covered by SCI during this period
received 3.28 citations. However, for
biochemistry papers one would expect
this figure to be doubled because the
average biochemistry paper now contains twice as many references as the
average SCI paper.
The papers were published in the 25
journals lis’ed in Table 1. Fifty-two
were publiihed in five journals: Journal
of Molecular Biology, Journal of Biological Chemistry, Proceedings of the National
Academy
of Sciences
US,
Biochemical
Journal. and Analytical
Biochemistry.
None of this will surprise
anyone familiar with the field.
Tnbta I: Journals that pubfisbed the most cited
1%0s articles fisted in Figure 1. according to
number of
articles.
No. 01 Ardcles
Joamal
J. M(,I Bid
14
J. JJiol. Chcm
12
Proc
Acad Sci. US
Nat
Biochmn
Anal.
9
9
J
n
Bmchem
JJwchemtsmy
h
Science
h
Arch.
B!ophys.
Acts
6
5
Biophys.
Rcs. Commun.
3
Ehochcm. Biophys.
Biochcm
5
Nature
Bwchem
3
J L,pid Res.
Ann.
NY Acad.
J titw?chem
AcIa Chem
Anal
Sci.
Cymchem.
Scartd
1
ZetI
I
Bt<q)hys. J
Eur
I
I
Chcrn
Biochcm.
2
2
I
1 Bncxhem
J Am
Chcm
J Am
Oil Chem.
Sex.
SW.
I
1
J Btochem —Tokyo
I
J. Cd
!
Bnd.
J Chromatography
J
M<)l
I
Pharr(w,col.
- Prcdcccwm
of Eur. j. JSiochcm,
However, thw is hinddght judgment.
If we consider that the fiit issue of the
Journal of Molecular Biology appeared
in 1959, and the fiit issue of Analytical
Biochemistry in 1960, it seems unusual
that they accounted for such a large
proportion of the most-cited papem of
the 1960s. I can well remember when
Kurt lacoby
and Roselle
Coviello
started A nalyticai
Biochemistry
for
Academic Press with the late Dr. Alvin
Nason as its founding editor.q I know
that he and Jim Barsky, who joined the
editorial board of Academic Press in
1%3, took special pride in the rapid success of this journal.
Dr. N.O. Kaplan of the University of
Caliiomia at San D~ego, co-chairman of
the editorial committee of Analytica{
Biochemistry,
attributes its success to
the fact that it concentrates solely on
publishing methodology
papers. Furthermore, the papers are reviewed quite
carefully, and only those describing
novel methods or developments are accepted. s I hasten to point out that its
impact factor is not SignKlcantly different from other high impact journals.
Therefore, most methodology papers it
published did not achieve such high use.
Methodology
papers
often
appear
among articles that are most-cited, but
not all methodology papers are heavily
cited.
Dr. S. Brenner of the Medcal Research Council of the UK was one of the
founding
editors of the Journal of
Molecular Biology. He says the succes+
of the journal can be accounted for
relatively simply. The number of leading figures in the field was not large in
1959. This made it possible for the
editors to contact most of them directly.
So, the journal was founded with the
support of most of the people who were
active and interested in the field. Subsequently, they all published in Journal of
Molecular Biology. 6 But one could say
this about many other less successful
journals. The widespread and rapid impact of molecular biology is also part of
the story. Certainly the Jouma! of
Molecular Biology was there at the right
time. But I’ve often wondered why it
took so long after the Watson-Crick
paper7 for this to occur.
Biochemistry,
published
by the
American Chemical Society, was started in 1%4. The six papers it contributed
are equivalent to nine or ten from a
journal established before 1960. This
journal, like most of the journals on this
list, is a high impact journal.
Seventy-three papers on the fist have
two or more authors. Forty-two have
two, 20 have three, and nine have four.
255
one paper has six authors and one has
eight. The total number of authors appearing on the list is 222. OnJy 28 papers
were written by one author. This is quite
a change from the situation in the forties.B Ail papers on the list are written in
English, except H. Wagner’s paper in
German on the separation of phosphofipids by chromatography.
Thk was
publiihed in Biochemische
Zeitschn~t,
the predecessor to the European Journal of Biochemistry.
Sixty-three
institutions
(shown
in
Table 2) are represented on the fist. Just
nine institutions account for 92 of the
222 authors. The list is dominated by
American laboratories, which account
for 39 of the 63 research institutions.
The United Kingdom follows with nine,
Sweden with six, and Australia and
Japan are represented by two institutions each. France, the Federal Republic of Germany, Italy, Switzerland, and
Taiwan are represented by one each.
Eighteen authors have two or more
papers on the list. B.N. Ames, P. Andrews, J.P. Changeux, W .W. Cleland,
P. Doty, A.D.
Hershey,
F. Jacob,
C.B. Lauren, S. Moore, M. Nirenberg,
T. Omura, K.A. Piez, R.A. Reisfeld,
R. Sate, and S. Spiegelman each wrote
two papers. R.J. Britten, J. Marmur,
and J. Monod each wrote three papers.
Thirteen
papers were authored
by
eleven Nobel laureates. E.L. Tatum was
awarded the prize for medicine in 1958
for his work on genes and heredity. The
1958 prize for chemistry
went to
F. Sanger for hk work on the chemical
composition
of insulin. M. F. Perutz
received the 1962 chemistry prize for
defining
the structure
of proteins.
F. Jacob and J. Monod shared the 1965
medicine prize for their study of cellular
mechanisms controlling enzymes and
virus synthesis.
The 1968 prize for
medicine was awarded to M.W. Nirenberg and R. W. Honey for their work on
the genetic code and enzymes. A. D.
Hershey was awarded the f969 medicine
prize for his investigation of the genetic
structure of viruses. The 1972 prize for
chemistry was awarded to S. Moore,
W.H. Stein, and C.B. Anfinsen for their
work on enzymes.
In a study I did with Irv Sher in 1965
we showed that articles written by
Nobel laureates were highly cited long
before they received the prize.g That is
why we believed citation data had some
forecasting value. This is true for eight
of the eleven Nobel laureates on the list.
E.L. Tatum received the prize in 19S8.
He appeared on our fiit of most-cited
biomedicine papers of the 19-40s, years
before he was awarded the Nobel
Prize. 10 However, his most-cited paper
was published in 1%2. The same is true
of F. Sanger. He received the prize in
1958 and his most-cited paper was pubfished in 1965. Sanger appeared on our
list of most-cited biochemistry papers of
the 1940s.s Lastly, M.F. Perutz received the prize in 1%2. His most-cited
paper appeared in 1968. Thus, as Harriet Zuckermanl I has pointed out, many
Nobel laureates continue to make highly
cited contributions
to science in the
years before and after their award.
Ten of the articles listed have appeared as Citation Classics in Current
Contents@
(C@).
Since
most CC
readers are familiar wit h this feature, I
wifl not elaborate any further.
On the whole, methodology
papers
dominate the lit, accounting for 68 of
the 101 articles. Unquestionably,
methods are the backbone
of scientific
research. David Gillespie of the National Cancer Institute suggests two
reasons why a particular method paper
is highfy cited. He says, “The distinction
between a classic and a quickly outmoded method lies in the ability of the
investigators to see the uses to which the
method will be put... and, as importantly, to take heed of the little irregularities
that lead
to significant
improvemerits. ”lz
It is important to note that well-cited
methodology
papers are in a special
class. While most methodology papers
do not fare better than other papers,
the
most successful
ones are more heavily
256
Tabla 2. Insritu[ional affiliations of
most-cited
196CJSarticles.
according
authors
of the
to number
Mt. Sinai Hosp. INCW York,
of
4
NY I
Cell Res. Lab.
2
Dt+
2
authors.
Neuropath<d
Oak Ridge Nal, Lab.
(Oak
4
Ridge, TN)
Osaka [Iniw. (Osaka,
No.
lnsmu!e
Arthritis
01
National Heart Institute
National
2
MA I
II
3
Med.
2
Sch.
COU.CII.
[Inn
MRC.
(New York.
Washmgbm
IWashingmn,
TerresmialMagnetism
5
Dep!.
Gcnet
4
Harbor,
Cold Spring
Enaland I
Ph!sburgh
lPiusburgh.
PA I
(Cambridge.
Jowa (lOWa CIIY, IA)
2
Uni,.
Ken[ucky
2
Uni*.
Lund (Sweden)
2
Univ.
Southampton
2
ILexmaton.
Skxkholm.
Uppsala (Uppsala,
Virginia
Sch
(Charlottesville.
b
NY}
Microbiol.
4
Ophthalmol.
I
Howard
Dep.
Bmchem.
1
s
Last. Technol.
N. W
Columbta
Church
Lab. Chem.
lJmv. (New York.
Biol.
2
Dcpt
M#crobiol.
J
Wm..
Dept
Mcd
5
(Ithaca, NY)
4
Bmchem
5
5
Cahfomia
Davis. Dcpt
Food SCI. & Tech
3
Davis. Dept
Bic~h. & Biophy$
2
IL)
I Waltham.
MA)
Med
Dcpl
B],)phy,
1
Mcc’<>llum Pratt [ml
I
I
( Stmkh<,lm.
Rc$. (La.sanne,
Pharmaccut
(Sendai,
Cancer
Swiwerland I
Sch
Japan I
(Inw
Adelaide
(Austrabal
Ilniv
Colorado
Mcd
(Imv
M!ami
4
(Inii.
Rochester
Dentistry
Ctr
COI”
5
4
D.pl
ImI
Edinburgh
John* Hopkins
I Bab8m<,rc. Ml) I
Taiwan I
1
kxpenmcn!al
IFhlder,
4
Med.
I
lcalyl
(Taipei.
NY)
(Inn
Ctty of Hupc Med. Ctr. IDuarce. CA I
Sch
I
Hosp
Blood C1r.
Med.
Tohoku
C,ty (d New York
Illinots (Ilrbana.
Nobel
SWISS lnsl
Public Health Res. Inst.
Brandms (km
BcaMy
Swedenl
I
Coil.
Univ.
(New York.
5
Unw.
Res.. Chesmr
Englandl
Taiwan
New York
Massachusetts Inst. Techno!
(Cambridge. MA I
[Inn
[nst. Cancer
Nat
I
Inst.
FL)
ISI. Rcgma Elena iR,,me,
5
Biihcm.
Cornell
Hughes Mcd.
I London,
3
NY}
Dqn.
2
1
Res. Inst., Royal Cancer
2
DIV. Bid
2
NY)
DepI.
{Miami.
2
2
CT)
Etnstein C<d!. Mcd
Dep(.
(Pasadena. CA}
Sweden)
Mcd
Chalmers Inst. Tcchmd
IGothe”bq.
Sweden)
Cdifomia
Inst
VA I
(New Haven.
(New York.
lNew York,
Wcnner-Gren
Sweden )
Univ.
Albert
KY I
kngiand I
[l”iv.
MI)
Sch. Med.
Glasgow {Glasguw,
Yale Univ.
Sco[lmdl
2
(Inm
7
b
Sta!c Umv.
lEasI Lansing,
Englandl
hb.
Biochcm.
7
3
Sch. Med.
2
Res.
Untv
Univ.
4
& Nutrit.
Rr$.
(1nit
Auwrabal
ISmckhcdm.
DCPI. Biochem
2
Cambridge
( !iouthampton.
NY
Inst. Pastcurl Pans. France)
NYU
9
DC)
Dept.
M,chigan
10
2
2
Cancer
Mcd
Sch. Med.
Dcpt
I
NY I
Camegielnst.
Ins!
Hosp
Physiol.
+@d
Swedenl
Englandl
(Melbourne.
Univ.
3
NC)
Dairytng
(London.
9
Harwcll,
3
PA I
{Stockholm.
S!. Vmccn!
[Ire..
Iu
UK
3
NY)
Mary’s
Cambridge,
England
Rockefeller
(Rye.
b
Cbcm.
Biol. Labs.
Re!
Inst
Sloan-Kettering
St
(Phda..
Ctr. (Durham.
Jnst. Res.
IShmficld.
2
MRC.
Med
Karobnska
& Inlcctkous
D]s.sasss
NY}
Res. Labs
NJ)
Pennsylvania
Namma[
un spcctfied
Haward Unm
(Cambridge.
Depl.
[Inn
Instimtc of
Allergy
2
I
Nat. Lab. (Ilpton.
Duke llIIN
4
lnsmute
Biochcm.
Stanford [Ini$. Sch. Med.
[1”,,. Munich (M””,ch,
FRGI
2
Cancer
Nahonal
Btochem.
4
WI I
I
Sharp & Dohmc
IRahway.
Instiru#c of
Dental Research
National
Dcpt
Merck
n
n
( Madison,
Lab. .& Depl.
Aarkcuhurc
Brookha$en
DISCascs
Unw.
W iscomi”
Biophys
& Metabolic
4
4
Agricdmre
Cdl.
2b
Institutes of Heabh
Natwnd
Med.
{ III),
Authon
Instlkulsm
National
I IS DcpI
of
Japan)
(M,ami.
Sch
NY I
TN)
I
I
E“gla”d)
H(,lc Marim
(W<)MIS H,de,
1
Med.
{Rochester.
(Bcckhenham,
I
FLI”
[lniv. Tennessee (Knon\dlc
wellc,,nw Rm, Labs
Woods
I
{Scotland)
B,,)l
I
Lab
MA9
. Sectmd afltl,ali,m
for a smgl.
e..th<,red paper
electrophoresis and the paper by Weber
and Osborn on gel electrophoresis,
among others, bring out certain points
about citation frequencies above the
564 threshold. It should be clear that no
greater intellectual significance should
be attributed to these papers than to
others on the list simply because they
were cited more than 9,0LXI times. Many
people have to be reminded of this lest
they take citation counts at face value.
However, the economic and policy implications of such widespread use of a
new technique does tell science administrators how to make research more
efficient. I should think that any future
discovery that would d~place
these
methods could have enormous impact.
The paper by Weber and Osbom is in
fact the most-cited
on the list. “The
reliability of molecular
weight determinations by dodecyl sulfate-polyacryIamide gel electrophoresis”
was cited
9,509” times in just ten years since its
publication in 1%9. The authors experimentally confirm that electrophoresis can accurately determine the molecular weights of polypeptide protein
chains. There are in fact only a smalf
number of papers or books in the entire
history of science cited more than 2,000
times. The classic example is the Lowry
method
for protein
determination.
What is not clear here is why people
continue to cite those methods explicitly and not cite others.
Seventeen papers d~cuss one or more
aspect of chromatography. Clearly large
numbers of scientists need to estimate
the molecular weights of proteins, and
many use the sephadex gel-filtration
method described by Andrews.
Five papers deal with centrifugation/sedimentation
techniques
which
are instrumental
in studies of protein
synthesis, where RNA molecules of different size and weight must be distinguished.
The remaining 20 papers cover miscellaneous
topics
and methods
including
quantitative
estimations
of
cited than theoretical papers. Thus it
would be expected that they would
dominate a list that represents about
one out of every six hundred published
in biochemistry during the 60s.3
As you can see, the list has been
divided into several categories-nucleic
acids, protein structure, enzymology,
electrophoresis,
chromatography,
centrifugation/sedimentation,
and miscellaneous. These categories are not meant
to be definitive. A simple arrangement
by journal might have been equally
useful.
The titles of most papers provide a
better capsule description than I could
provide in the space available. The
rapid growth of molecular
biology is
reflected in the first group of 25 papers
on the nucleic acids, DNA, and RNA.
Seven deal with the gene’s role in protein and RNA synthesis. The Jacob and
Monod paper is a good example of a
review article that contains new and important ideas not apparent
in the
sources under review. ”rn this paper they
suggested the now familiar concept of a
messenger
RNA. For this Jacob and
Monod were awarded the Nobel prize in
1965.
Considering
that seven papers are
concerned
with proteins one wonders
why there is not a journal named Protein.
Included in this group are three
papers on protein structure and three
on their binding properties.
Eleven papers are on enzymes, specialized proteins that accelerate or inhibit biochemical reactions. Five papers
describe the preparation and properties
of a variety of enzymes. Two discuss enzyme kinetics and rate equations. TWO
more papers discuss allostenc enzymes
in bacterial metabolism.
The emphasis
on methodology
is
reflected in the large number of papers
on electrophoresis,
chromatography,
centrifugation,
and other techniques for
separating large molecules. There are 16
papers
on electrophoresis
alone!
The
papers by Davis and Omstein on disc
258
bbchemical
substances
in tissue or
fluids. Three papers d~uss
various
aspects of human and animal hemogl~
bin. One paper details the electron
transport system in the outer membrane
of liver mitt ~hondria. Other areas dealt
with include the incorporation
of radb
active amino acids into proterns,
the
determination
of cystine as cysteic acid,
that
and
a scintillation
machine
measures
the amount
of radioactive
materiaf in blologictd fluids.
In the near future I will provide an additional list of life science papers of the
1%0s. These will cover all aspects of
biomedical research except biochemistry. Following that I hope to cover clinical papers.
I’m sure you can understand the frustration I experience
in having to cut
these MS off at an arbitrary
point,
knowing there are many additional important papers that should be listed.
Science is such big business these days
that even a listing of 1,000 papers would
leave out many key people. So there
must be an arbitrary cut-off point. Current Contents can’t provide unlimited
space for this information.
That is why I
look forward to our Atlas of Science. 13
In it we expect to identify almost every
signf]cant
paper for each field and
period studied. Since it has been four
years since I first mentioned this project
I should add that we hope to complete
that project during the next year.
ems Ial
REFERENCES
1.
2.
3.
4.
5,
6.
7,
8.
9.
Gatffakt E. Most-cited articles of the 1960s. 1. Physical sciences.
Currem Contents (21):S-IS. 21 May 1979.
Science Cit.fion Index 1978 Guide. Philadelphk: 1S1Press, 1979. 150p.
Gnsflafd E. Trends in bkrchemical literature.
Trend$ Biochem. .$ci. (In press. 1979).
Barsky L Telephone communication. 7 June 1979.
Kapfan N O. Telephone communication. 16 May 1979.
Ifrenner S. Telephone communication. 16 May 1979.
Watqon J D & Crfck F H C. A structure for deoxyribose nucleic acid. Namra 171:737-8, 1953.
Garffekt E. Highly cited articles. 35. Biochemistry papers published in the 194%.
Current Contents (8):5-1 1, 21 February 1977.
Garfkfd E & StsarI. New tds for improving and evaluating the effectiveness of research. (Yovits M C.
Gilford D M, WIICOX
R H, Stavely E & Lemer H D, eds.) Research prwgmm ef~ecfiveness. Pmreed.
mgs of the conference sponsored by Office of Na val Research.
New York: Gordon & Breach, 1966. Chapter 7. p. 135-46.
Washing/on,
DC, July 27-29, 1%5.
10. Garlfefd E. Highly cited articles. 37. Biomedical articles pubfished in the 1940s.
Currenf Cwrferm (13):5-12. 28 March 1977.
II. Zssckermrm H. Scientific eltte. Nobel laureates in the United State.r
New York: Free Press. 1977. 335p.
12. G2Uaqde D. Cmrfion Classics A quantitative assay for DNA-RNA hybrids with DNA immobilimd on
a membrane. Current Conterm [11): 14, 14 March 1977.
13. Garfiefd E. lSf “sAt/as of Science may help sfudents in choice of career in science.
Curwnr flmrmnls (29):S-11. 21 July 1975.(Reprinted in: Garffald E. E.way.rtI/ an informaoon
.wienml Philadelphia: 1S1Press. 1977. Vol. 2. p. 311-2. )
F@lm
~:
!wn.
10t mml.cllco
ff m amcle
amc!es of [he 1960s in biochemistry
has appeared as a CtmmwI Clasm-.
and molecular
a reference
biology.
follows the amhor
Authors’ affiliations follow each cita
affiliations,
Total
Clmtforss
1%1-197s
Bfblfogsapbk Data
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I(YJS AmesB N
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Ml
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Chem
R Ii ~ osvfdms E Hz. Gene
I I I Carnegie
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121Rockefeller
1441
llnw.,
Erf[tea R f & Kohne
Washington,
DcpI
New York,
regulatmn
DepI
NY
m the newralizatimr
NfAMDD.
Ten
Srtbesda,
Magnet
of bacteriophage
for higher celfs: a theory. .bence
Magne!..
DNA.
20014
I bS:349-57.
1969
Washi”gf on, DC 20015
llH321
D E. Repeated sequences in DNA,
TcrI
MD
W ashmgmn.
259
Screnu
DC 20315
16 I: 529-Kf,
l%t!.
Carmgic
Imt
of
142
_
920
CkQszLmfin
RR.
A Qm~h~
J. L601. Chem. 244:61607.
M ● Lfers ?. DNAd#recwd
PtKIC. Nal
,4cad
Slmford,
71KI
J%&
f.r the iWEe =de
Ptilcxlio.
of E c.h DNA-dc~ndcnl
1%9. Harvard Llniv.. Biol. Lab., Cambndgc, MA 02138
syn[hews of RNA
.$./. LJS 4L3:81-94, 1962 S!anford
by an emyme
~Jmv Sch
Med
1513
polym.rasc
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Bmchc,n
CA 90J5
A k Mmra
H N. The precision of ullmviolct
absorptm.
measurements t. lhc Schrn#dt-
Tfmnnfmu$cr procedure for nuclelc .ctd cstimstson. Bmchtm
hi”
GJassow, J3CJX Btahcm.
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724
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RNA
Bmphy.
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