review article the most cited papers in osteoporosis and...

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Review Article The Most Cited Papers in Osteoporosis and Related Research Lukas A. Holzer, 1 Andreas Leithner, 1 and Gerold Holzer 2 1 Department of Orthopaedic Surgery, Medical University of Graz, 8036 Graz, Austria 2 Department of Orthopaedics, Medical University of Vienna, 1090 Vienna, Austria Correspondence should be addressed to Lukas A. Holzer; [email protected] Received 29 September 2014; Accepted 4 December 2014 Academic Editor: Manuel Diaz Curiel Copyright © 2015 Lukas A. Holzer et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Osteoporosis is a systemic disease of the bone that affects millions of people and causes burden for both the affected individual and health systems and societies worldwide. Since the 1970s much research has been done in the field of osteoporosis. e number of citations of a paper reflects its influence and importance to the field. omson ISI Web of Science database was searched to retrieve a list of the fiſty most cited articles related to osteoporosis and its research. e fiſty most cited articles in absolute numbers in the field of osteoporosis were cited from 877 to 3056 times (mean 1141 ± 537). Most papers were published in the basic science category ( = 23). 395 authors contributed; a single paper had between one and 62 authors (mean: 10.02 ± 9.9 authors). 12 authors (3.04%) contributed between 7 and 4 papers; 340 authors (86.1%) were at least named once. Corresponding authors were from eight countries with most contributions from the United States ( = 34, 68%). e majority of papers were published in the 1990s ( = 29). e list of 50 most cited papers presents citation classics in the field of osteoporosis and related research. 1. Introduction Osteoporosis is a systemic disease of the bone that affects millions of people and causes burdens for both the affected individual and health systems and societies worldwide [1]. Osteoporosis is a multidisciplinary disease and therefore relevant to different medical specialities, for example, general medicine, internal medicine, endocrinology, gynaecology, orthopaedic surgery, and traumatology, but also to preclinical and basic disciplines such as physiology, pathology, and biomechanics. Since the 1970s much research has been done in the field of osteoporosis. Research in osteoporosis poses a wide field and includes basic, clinical, and translational studies in the above mentioned specialities. Meanwhile several journals have been established that are dedicated to publishing articles related to the disease. A citation is a quotation or a reference of published scientific work in books, book chapters, or articles [2]. e number of citations of published scientific work has been used as a marker to evaluate the level of its influence and importance. However, the number of citations may not be the only factor in determining the importance of scientific work in the field, but allows defining “citations classics” that could be used, for example, for educational purposes. Furthermore, the number of citations directly influences the impact factor of a journal, a generally accepted factor that determines its quality and importance [2]. Analyses of most cited papers have been performed in various medical specialties including anaesthesiology, gynaecology, urology, orthopaedic surgery, plastic surgery, or subspecialties such as pain management, critical care medicine, hand surgery, shoulder surgery, or orthopaedic joint replacement [312]. Furthermore, such lists exist for var- ious pathologies or diseases such as pancreatitis, Parkinson’s disease, depression, sepsis, or epilepsy [1317]. However, no such study has been carried out in osteoporosis and related research. e purpose of the present study is to determine scientific articles in the field of osteoporosis and related research that have been cited most frequently by other authors and to establish a ranking of the fiſty most cited papers in the field by using the omson ISI Web of Science database. 2. Material and Methods 2.1. Search Strategy. In October 2013, omson ISI Web of Science database was searched for the following search terms: Hindawi Publishing Corporation Journal of Osteoporosis Volume 2015, Article ID 638934, 12 pages http://dx.doi.org/10.1155/2015/638934

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Page 1: Review Article The Most Cited Papers in Osteoporosis and ...downloads.hindawi.com/journals/jos/2015/638934.pdf · osteoporosis... Data Analyses. Eachofthe ymostcitedarticleswas reviewed

Review ArticleThe Most Cited Papers in Osteoporosis and Related Research

Lukas A. Holzer,1 Andreas Leithner,1 and Gerold Holzer2

1Department of Orthopaedic Surgery, Medical University of Graz, 8036 Graz, Austria2Department of Orthopaedics, Medical University of Vienna, 1090 Vienna, Austria

Correspondence should be addressed to Lukas A. Holzer; [email protected]

Received 29 September 2014; Accepted 4 December 2014

Academic Editor: Manuel Diaz Curiel

Copyright © 2015 Lukas A. Holzer et al.This is an open access article distributed under theCreative CommonsAttribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Osteoporosis is a systemic disease of the bone that affects millions of people and causes burden for both the affected individual andhealth systems and societies worldwide. Since the 1970s much research has been done in the field of osteoporosis. The number ofcitations of a paper reflects its influence and importance to the field.Thomson ISIWeb of Science database was searched to retrievea list of the fifty most cited articles related to osteoporosis and its research. The fifty most cited articles in absolute numbers inthe field of osteoporosis were cited from 877 to 3056 times (mean 1141 ± 537). Most papers were published in the basic sciencecategory (𝑛 = 23). 395 authors contributed; a single paper had between one and 62 authors (mean: 10.02 ± 9.9 authors). 12 authors(3.04%) contributed between 7 and 4 papers; 340 authors (86.1%) were at least named once. Corresponding authors were fromeight countries with most contributions from the United States (𝑛 = 34, 68%). The majority of papers were published in the 1990s(𝑛 = 29). The list of 50 most cited papers presents citation classics in the field of osteoporosis and related research.

1. Introduction

Osteoporosis is a systemic disease of the bone that affectsmillions of people and causes burdens for both the affectedindividual and health systems and societies worldwide [1].Osteoporosis is a multidisciplinary disease and thereforerelevant to different medical specialities, for example, generalmedicine, internal medicine, endocrinology, gynaecology,orthopaedic surgery, and traumatology, but also to preclinicaland basic disciplines such as physiology, pathology, andbiomechanics.

Since the 1970s much research has been done in thefield of osteoporosis. Research in osteoporosis poses a widefield and includes basic, clinical, and translational studies inthe abovementioned specialities. Meanwhile several journalshave been established that are dedicated to publishing articlesrelated to the disease.

A citation is a quotation or a reference of publishedscientific work in books, book chapters, or articles [2]. Thenumber of citations of published scientific work has beenused as a marker to evaluate the level of its influence andimportance. However, the number of citationsmay not be theonly factor in determining the importance of scientific workin the field, but allows defining “citations classics” that could

be used, for example, for educational purposes. Furthermore,the number of citations directly influences the impact factorof a journal, a generally accepted factor that determines itsquality and importance [2].

Analyses of most cited papers have been performedin various medical specialties including anaesthesiology,gynaecology, urology, orthopaedic surgery, plastic surgery,or subspecialties such as pain management, critical caremedicine, hand surgery, shoulder surgery, or orthopaedicjoint replacement [3–12]. Furthermore, such lists exist for var-ious pathologies or diseases such as pancreatitis, Parkinson’sdisease, depression, sepsis, or epilepsy [13–17]. However, nosuch study has been carried out in osteoporosis and relatedresearch.

The purpose of the present study is to determine scientificarticles in the field of osteoporosis and related research thathave been cited most frequently by other authors and toestablish a ranking of the fifty most cited papers in the fieldby using theThomson ISI Web of Science database.

2. Material and Methods

2.1. Search Strategy. In October 2013, Thomson ISI Web ofScience database was searched for the following search terms:

Hindawi Publishing CorporationJournal of OsteoporosisVolume 2015, Article ID 638934, 12 pageshttp://dx.doi.org/10.1155/2015/638934

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2 Journal of Osteoporosis

“osteoporosis,” “fracture,” “bone mineral density,” “bone den-sity,” “bone mass,” “BMD,” “dual energy X-ray absorptiom-etry,” “DXA,” “DEXA,” “osteoclast,” “osteoblast,” “osteocyte,”“bone formation,” “bone resorption,” “hormone replacementtherapy,” “estrogen replacement therapy,” “bisphosphonate,”“teriparatide,” “denosumab,” and “SERMs.”

All papers with the main focus of their research onosteoporosis and related basic, clinical and translationalresearch were included in this study. Papers including theabove used terms, but focusing on other research areas wereexcluded. The search output was then recorded and rankedaccording to the absolute number of highest citations. In caseswith an identical absolute number of citations, the papers thathad a higher citation density (see below) were ranked higher.A list of the fifty most cited articles was established.

Searches and analyses were done by individuals with along-time experience in both basic and clinical research inosteoporosis.

2.2. Data Analyses. Each of the fifty most cited articles wasreviewed and the following data was extracted: numberof citations, authors, article title, journal title, publicationyear, and origin of corresponding author. Each paper wasassigned to a single country in accordance with the corre-sponding author’s address because the corresponding authoris usually primarily and mainly responsible for the wholestudy project [18]. To evaluate the relative impact of a pub-lished paper, the citation density (“number of citations/yearssince publication”) was calculated as described before [12].Furthermore, each article was analyzed and in case of aclinical study a level of evidence was attributed to thepaper based on the guidelines for clinical articles by OxfordCentre for Evidence-Based Medicine 2011 Levels of Evidence(Oxford, UK: http://www.cebm.net/) [19]. Three categorieswere established: basic science, clinical science, and reviewsand guidelines. The papers were analyzed and attributed toone of these categories.

3. Results

The fifty most cited articles on osteoporosis and relatedresearchwere cited from877 to 3056 times (mean 1141±537),the top ten papers at least 1741 times. For the whole list seeTable 1. The most frequently cited paper was by Lacey et al.published in 1998 with a mean number of 184,5 citations peryear. The top ten papers according to citation density can beseen in Table 2.Themajority of articles could be attributed tothe basic science category (𝑛 = 23). The distribution of theother categories can be seen in Figure 1. Level of evidencecould be analyzed in 17 clinical papers (from the ClinicalScience category) and can be seen in Table 1. The majorityof papers (𝑛 = 13) were level of evidence I, one paper waslevel of evidence II, and three papers level of evidence III (seeFigure 2).

Eleven search terms were found in the title of the papers;altogether these terms were found 70 times (mean: 6.4 ± 5.5times). For the list of all search terms found see Table 3.Search terms “fracture” (𝑛 = 18) and “osteoporosis” (𝑛 = 14)

Basic scienceClinical scienceReview and guideline

10

17

23

Figure 1: Distribution of categories.

13

1

3

0 00

2

4

6

8

10

12

14

I II III IV V

Figure 2: Level of evidence in the clinical papers.

were found most frequently (45.7% of all terms searched).Other terms searchedwere found between one andnine times(mean: 4.2 ± 2.9 times). More search terms were found in theabstract and the keywords of the papers.

All together 395 authors contributed to the papers of thetop 50 list. A single paper had between one and 62 authors(mean: 10.02 ± 9.9 times). 12 authors (3.04%) contributed tobetween seven and four papers, 13 authors (3.3%) to three,and 30 twice (7.6%). 340 authors (86.1%) were named at leastonce. The top 12 authors are presented in Table 4.

Eight countries contributed to the Top 50 list (seeFigure 3). Authors from the United States contributed mostfrequently as a corresponding author (𝑛 = 34, 68%), followedby authors from the United Kingdom (𝑛 = 6), Japan (𝑛 = 3),Canada and France (2 papers each), and Sweden, Israel, andAustralia with one paper each.

Papers were published in 18 different journals publishingboth basic and clinical research. Most papers (𝑛 = 9)were published in the New England Journal of Medicine.Other journals include Cell (𝑛 = 8), Nature (𝑛 = 5), TheJournal of the AmericanMedicalAssociation,The Lancet, andScience (𝑛 = 4), Proceedings of the National Academy ofSciences (𝑛 = 3), Journal of Bone and Mineral Researchand Journal of Clinical Investigation (two paper each), andAmerican Journal of Clinical Nutrition, American Journal ofMedicine, British Medical Journal, Cell and Tissue Research,Endocrinology, Endocrine Review, Epidemiology Reviews,Genes & Development, and Osteoporosis International one

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Journal of Osteoporosis 3

Table1:Th

efifty

citatio

ncla

ssicsinosteop

orosisandrelated

research.

Rank

Paper

Absolutenu

mbero

fcitatio

nsCitatio

ndensity

Levelof

evidence

1M.R

.Uris

t,“Bon

e-form

ationby

autoindu

ction,”

Scien

ce,vol.150,pp.893–899,1965.

3056

63,6

N/A

2

D.L.L

acey,E

.Tim

ms,H.L.Tan,M

.J.K

elley,C

.R.D

unstan,T.B

urgess,R

.Elliott,A.

Colom

bero,G

.Elliott,S.Scully,

H.H

su,J.Sullivan,N

.Haw

kins,E

.Davy,C.

Capp

arelli,A.

Eli,Y.X.

Qian,

S.Ka

ufman,I.Sarosi,V.

Shalho

ub,G

.Senaldi,J.G

uo,J.D

elaney,and

W.J.

Boyle,“O

steop

rotegerin

ligandisac

ytok

inethatregulates

osteoclastdifferentiatio

nand

activ

ation,”

Cell,vol.93,pp.165–176,1998.

2768

184,5

N/A

3J.M.W

ozney,V.

Rosen,

A.J.C

eleste

,and

L.M.M

itsock,“N

ovelregu

latorsof

bone-fo

rmation-m

olecular

clonesa

ndactiv

ities,”Scien

ce,vol.242,pp.528–1534,1988.

2662

106,4

N/A

4

W.S.Sim

onet,D

.L.L

acey,C

.R.D

unsta

n,M.K

elley,M.S.C

hang

,R.Luthy,H

.Q.N

guyen,

S.Woo

den,

L.Be

nnett,T.Bo

one,G.Shimam

oto,M.D

eRose,R.

Ellio

tt,A.C

olom

bero,H

.L.

Tan,

G.Trail,J.Sullivan,

E.Davy,N.B

ucay,L.R

enshaw

Gegg,T.M.H

ughes,D.H

ill,W

.Pattison,P.Ca

mpb

ell,S.Sand

er,G

.Van,J.Tarpley,P.D

erby,R

.Lee,and

W.J.B

oyle,

Cell,vol.

89,pp.309–

319,1997.

2629

164,3

N/A

5

H.Yasud

a,N.Shima,N.N

akagaw

a,K.

Yamaguchi,M

.Kinosaki,S.Mochizuki,A

.Tom

oyasu,

K.Yano

,M.G

oto,A.M

urakam

i,E.

Tsud

a,T.Morinaga,K.

Higashio,N.U

dagawa,N.

Takahashi,andT.Suda,“Oste

oclastdifferentiatio

nfactor

isaligandforo

steop

rotegerin

osteoclasto

genesis-in

hibitory

factor

andisidenticalto

TRANCE

/RANKL

,”Proceedingso

ftheN

ationa

lAcademyo

fScie

ncesoftheU

nitedStatesofAm

erica

,vol.95,pp

.3597–3602,1998.

2206

147

N/A

6

T.Ko

mori,H.Yagi,S.Nom

ura,A.Yam

aguchi,K

.Sasaki,K.

Sasaki,K

.Deguchi,Y.Shimizu,

R.T.Bron

son,

Y.H.G

ao,M

.Inada,M

.Sato,R.

Okamoto,Y.Kitamura,S.Yo

shiki,andT.

Kishim

oto,“Targeteddisrup

tionof

Cbfa1resultsin

acom

pletelackof

bone

form

ationow

ing

toaturationalarresto

foste

oblasts

,”Ce

ll,vol.89,pp.755–764,1998.

2132

133,2

N/A

7S.R.

Cumming,M.C

.Nevitt,W

.S.B

rowner,K.

Ston

e,K.

M.Fox,K

.E.E

nsrud,J.C.

Cauley,

D.B

lack,and

T.M.V

ogt,“R

isk-fa

ctorsfor

hipfracture

inwhitewom

en,”Th

eNew

Engla

ndJourna

lofM

edicine,vol.332,pp.767–773,1995.

2102

116,7

I

8

D.M

.Black,S.R

.Cum

ming,D.B.K

arpf,J.A

.Cauley,D.E

.Thom

pson

,M.C

.Nevitt,D

.C.

Bauer,H.K

.Genant,W.L.H

askell,R.

Marcus,S.M.O

tt,J.C.

Torner,S.A

.Quand

t,T.F.

Reiss,and

K.E.

Ensrud

,“Ra

ndom

isedtrialofeffectof

alendron

ateo

nris

kof

fracture

inwom

enwith

existingvertebralfractures,”La

ncet,vol.348,pp.1535–1541,1996.

2067

121,5

I

9M.C

.Chapu

y,M.E

.Arlo

t,F.Dub

oeuf,J.B

run,B.

Crou

zet,S.Arnaud,P.D.D

elmas,and

P.J.

Meunier,“Vitamin-D

(3)a

ndcalcium

topreventh

ip-fr

acturesinelderly

wom

en,”Th

eNew

Engla

ndJourna

lofM

edicine,vol.23,pp

.1637–1642,1992.

1771

84,3

I

10

Y.Y.Ko

ng,H

.Yoshida,I.Sarosi,H.L.Tan,E

.Tim

ms,C.

Capp

arelli,S.Moron

y,A.J.

Oliveira-dos-Santos,G.V

an,A

.Itie,W

.Kho

o,A.W

akeham

,C.R

.Dun

stan,

D.L.L

acey,T.

W.M

ak,W

.J.B

oyle,

andJ.M.Penninger,“OPG

Lisak

eyregulator

ofosteoclasto

genesis

,lymph

ocyted

evelo

pmentand

lymph

-nod

eorganogenesis,”N

ature,vol.397,pp

.315–323,

1999.

1741

124,3

N/A

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4 Journal of Osteoporosis

Table1:Con

tinued.

Rank

Paper

Absolutenu

mbero

fcitatio

nsCitatio

ndensity

Levelof

evidence

11

B.Ettin

ger,D.M

.Black,B

.H.M

itlak,R

.K.K

nickerbo

cker,T.N

ickelse

n,H.K

.Genant,C.

Chris

tiansen,P.D

.Delmas,J.R

.Zanchetta,J.Stakkestad,C.

C.Gluer,K

.Krueger,F.J.

Coh

en,S.E

ckert,K.

E.En

srud

,L.V

.Avioli,P.Lips,and

S.R.

Cummings,“Re

ductionof

vertebralfracturer

iskin

postmenop

ausalw

omen

with

osteop

orosistre

ated

with

raloxifene,”

TheJournaloftheA

merica

nMedica

lAsso

ciatio

n,vol.282,pp

.637–6

45,1999.

1732

123,7

I

12B.

L.Riggs,andL.J.Melton

,“Involutio

nalO

steop

orosis,”Th

eNew

Engla

ndJourna

lof

Medicine,vol.314,pp.1676–1686,1986.

1719

63,6

N/A

13D.M

arshall,O.Joh

nell,andH.W

edel,

“Meta-analysisof

howwellm

easureso

fbon

emineral

density

predicto

ccurrenceo

foste

oporoticfractures,”

British

Medica

lJournal,vol.312,pp.

1254–1259,1996.

1689

99,3

I

14

R.M.N

eer,C.

D.A

rnaud,J.R.

Zanchetta

,R.P

rince,G

.A.G

aich,J.Y.R

eginste

r,A.B

.Hod

sman,E

.F.E

riksen,

S.Ish-Shalom

,H.K

.Genant,O.H

.Wang,andB.

H.M

itlak,“Eff

ect

ofparathyroidho

rmon

e(1-3

4)on

fracturesa

ndbo

nemineraldensity

inpo

stmenop

ausal

wom

enwith

osteop

orosis,”L

ancet,vol.344,pp

.1434–

1441,2001.

1686

140,5

I

15S.R.

Cummings,D

.M.B

lack,M

.C.N

evitt,W

.Browner,J.Ca

uley,K

.Ensrud,H.K

.Genant,

L.Palerm

o,J.Scott,andT.M.V

ogt,“Bon

e-density

atvario

ussites

forp

redictionof

hip-fractures,”

TheN

ewEn

gland

Journa

lofM

edicine,vol.341,pp.72–75,1993.

1667

83,3

I

16W.J.B

oyle,

W.S.Sim

onet,and

D.L.L

acey,“Oste

oclastdifferentiatio

nandactiv

ation,”

Cell,

vol.423,pp

.337–342,2003.

1651

165,1

N/A

17P.Soria

no,C

.Mon

tgom

ery,R.

Geske,and

A.B

radley,“Targeted

disrup

tionof

thec

-src

protoo

ncogeneleads

toosteop

etrosis

inmice,”

Nature,vol.64,pp

.693–702,1991.

1609

73,1

N/A

18J.A.K

anis,

L.J.Melton

,C.C

hristiansen,C

.C.Joh

nston,

andN.K

haltaev,“Perspective-the

diagno

sisof

osteop

orosis,”C

ell,vol.9,pp.1137–1141,1994.

1532

80,6

N/A

19

F.Otto

,A.P.Th

ornell,T.Cr

ompton

,A.D

enzel,K.

C.Gilm

our,I.R.

Rosewell,G.W

.H.

Stam

p,R.

S.P.Be

ddington

,S.M

undlos,B

.R.O

lsen,

P.B.

Selby,andM.J.O

wen,“Cb

fa1,a

cand

idateg

enefor

cleidocranialdysplasia

synd

rome,isessentialfor

osteob

last

differentiatio

nandbo

nedevelopm

ent,”

Journa

lofB

onea

ndMineralResearch,vol.89,pp

.765–771,1997.

1529

95,5

N/A

20

U.A.Liberman,S.R

.Weiss,J.B

roll,H.W

.Minne,H

.Quan,N.H

.Bell,J.Ro

driguezportales,

R.W.D

owns,J.D

equeker,M.Favus,E

.Seeman,R

.R.R

ecker,T.Ca

pizzi,A.C

.Santora,A

.Lo

mbardi,R.

V.Sh

ah,L.J.H

irsch,and

D.B

.Karpf,“Eff

ecto

foralalend

ronateon

bone-m

ineraldensity

andtheincidence

offracturesinpo

stmenop

ausaloste

oporosis,”Th

eNe

wEn

gland

Journa

lofM

edicine,vol.333,pp.1437–144

3,1995.

1484

82,4

I

21N.A

.Morris

on,J.C

.Qi,A.Tok

ita,P.J.K

elly,

L.Cr

ofts,T.V.

Nguyen,

P.N.Sam

broo

k,andJ.

A.E

isman,“Predictio

nof

bone-densityfro

mvitamin-d

receptor

alleles,”

Nature,vol.367,pp.

284–

287,1994.

1372

72,2

N/A

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Journal of Osteoporosis 5

Table1:Con

tinued.

Rank

Paper

Absolutenu

mbero

fcitatio

nsCitatio

ndensity

Levelof

evidence

22S.L.Teitelbaum,“Bo

neresorptio

nby

osteoclasts

,”Scien

ce,vol.289,pp.1504–1508,2000.

1370

105,3

N/A

23

N.B

ucay,I.Sarosi,C.

R.Dun

stan,

S.Moron

y,J.Tarpley,C.

Capp

arelli,S.Scully,

H.L.Tan,

W.L.X

u,D.L.L

acey,W

.J.B

oyle,

andW.S.Sim

onet,“Oste

oprotegerin

-deficientm

ice

developearly

onseto

steop

orosisandarteria

lcalcification,”

Genes&Develo

pment,vol.12,pp.

1260–1268,1998.

1292

86,1

N/A

24

S.T.Harris

,N.B

.Watts,

H.K

.Genant,C.

D.M

cKeever,T.Hangartner,M.K

eller,C.

H.

Chesnu

t,J.Brow

n,E.

F.Eriksen,

M.S.H

oseyni,D

.W.A

xelro

d,andP.D.M

iller,“Eff

ectsof

risedronatetre

atmento

nvertebraland

nonvertebralfracturesinwom

enwith

postmenop

ausaloste

oporosis-a

rand

omized

controlledtrial,”Th

eJourna

lofthe

America

nMedica

lAsso

ciatio

n,vol.282,pp

.1344–

1352,1999.

1291

92,2

I

25S.R.

Cummings,J.L.K

elsey,M.C

.Nevitt,and

K.J.Odo

wd,“Epidemiology

ofosteop

orosis

andosteop

oroticfractures,”

Epidem

iologicR

eview

s,vol.7,pp

.178–208,1985.

1259

44,9

N/A

26

A.K

libanski,L.Ad

ams-Ca

mpb

ell,T.B

assfo

rd,S.N

.Blair,

S.D.B

oden,K

.Dickersin,D

.R.

Gifford,L.Glasse,S.R.

Goldring,K.

Hruska,S.R.

John

son,

L.K.

McC

auley,andW.E

.Ru

ssell,“O

steop

orosispreventio

n,diagno

sis,and

therapy,”

TheJourna

lofthe

America

nMedica

lAsso

ciatio

n,vol.285,pp

.785–795,2001.

1254

104,5

N/A

27

S.R.

Cummings,D

.M.B

lack,D

.E.Th

ompson

,W.B

.App

legate,E

.Barrett-Con

nor,T.A.

Muslin

er,L.Palermo,R.

Prineas,S.M.R

ubin,J.C

.Scott,

T.Vo

gt,R

.Wallace,A

.J.Yates,and

A.Z

.LaC

roix,“Eff

ecto

falend

ronateon

riskof

fracture

inwom

enwith

lowbo

nedensity

but

with

outvertebralfractures-

Results

from

thefractureinterventiontrial,”Th

eJourna

lofthe

America

nMedica

lAsso

ciatio

n,vol.280,pp

.2077–2082,1998.

1245

83I

28D.R

.Bertolin

i,G.E

.Nedwin,and

T.S.Bringm

an,“Stim

ulationof

bone-resorptionand

inhibitio

nof

bone-fo

rmationinvitro

byhu

man-tu

mor

necrosisfactors,”

Nature,vol.319,pp.

516–

518,1986.

1176

43,5

N/A

29B.

Daw

sonH

ughes,S.S.Harris

,E.A

.Krall,andG.E

.Dallal,“Effectof

calcium

andvitamin

Dsupp

lementatio

non

bone,densityin

men

andwom

en65

yearso

fage

orolder,”

TheN

ewEn

gland

Journa

lofM

edicine,vol.337,pp.670–

676,1997.

1170

73,1

I

30

P.D.D

elmas,N

.H.B

jarnason

,B.H

.Mitlak,A

.C.R

avou

x,A.S.Shah,W.J.H

uster,M.

Draper,andC.

Chris

tiansen,“Eff

ectsof

raloxifene

onbo

nemineraldensity,serum

cholesterolcon

centratio

ns,and

uterinee

ndom

etriu

min

postmenop

ausalw

omen,”Th

eNew

Engla

ndJourna

lofM

edicine,vol.337,pp.1641–1647,1997.

1164

72,7

I

31T.Suda,N

.Takahashi,N

.Udagawa,E.

Jimi,M.T.G

illespie,T.J.Martin

,“Mod

ulationof

osteoclastdifferentiatio

nandfunctio

nby

then

ewmem

bersof

thetum

ornecrosisfactor

receptor

andligandfamilies,”En

docrineR

eview

s,vol.20,pp.345–357,1999.

1162

83N/A

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6 Journal of Osteoporosis

Table1:Con

tinued.

Rank

Paper

Absolutenu

mbero

fcitatio

nsCitatio

ndensity

Levelof

evidence

32K.

Nakashima,X.

Zhou

,G.K

unkel,Z.

P.Zh

ang,J.M.D

eng,R.

R.Be

hringer,andB.

deCr

ombrug

ghe,“Th

enovelzinc

finger-containing

transcrip

tionfactor

Oste

rixisrequ

iredfor

osteob

lastdifferentiatio

nandbo

neform

ation,”

Cell,vol.108,pp

.17–29,2002.

1143

103,9

N/A

33

A.M

.Parfitt,C.

H.E

.Mathews,A.R

.Villanueva,M

.Kleerekop

er,B

.Frame,andD.S.R

ao,“

Relationships

betweensurfa

ce,volum

e,andthickn

esso

filiactrabecularb

oneinagingand

inosteop

orosis-im

plications

forthe

microanatom

icandcellu

larm

echanism

sofb

oneloss,”

TheJournalofClinica

lInvestigation,vol.72,pp.1396–140

9,1983.

1117

37,2

N/A

34S.R.

Cummings,and

L.J.Melton

,“Ep

idem

iology

andou

tcom

esof

osteop

oroticfractures,”

Proceedingso

fthe

Natio

nalA

cademyo

fScie

ncesoftheU

nitedStatesofAm

erica

,vol.359,pp.

1761–1767,2002.

1089

99N/A

35

E.A.W

ang,V.

Rosen,

J.S.Dalessand

ro,M

.Baudu

y,P.Cordes,T.Harada,D.I.Israel,R.

M.

Hew

ick,K.

M.K

erns,P.L

apan,D

.P.Luxenberg,D

.McQ

uaid,I.K

.Mou

tsatsos,J.Nove,and

J.M.W

ozney,“R

ecom

binant

human

bone

morph

ogeneticproteinindu

cesb

one-form

ation,”

Lancet,vol.87,pp

.2220–

2224,1990.

1077

46,8

N/A

36S.C.

Manolagas,and

R.L.Jilka,“Mechanism

sofd

isease-

bone-m

arrow,

cytokines,and

bone

remod

eling

-emerging

insig

htsintothep

atho

physiology

ofosteop

orosis,”Th

eNew

Engla

ndJourna

lofM

edicine,vol.332,pp.305–311,1995.

1047

58,1

N/A

37C.

Coo

per,G.C

ampion

,and

L.J.Melton

,“Hip-fr

acturesinthee

lderly-a

worldwide

projectio

n,”Oste

oporosisInternationa

l,vol.2,pp.285–289,1992.

1037

49,3

N/A

38H.K

.Genant,C.

Y.Wu,C.

Vank

uijk,and

M.C

.Nevitt,“Ve

rtebralfracturea

ssessm

entu

sing

asem

iquantitativ

etechn

ique,”Scien

ce,vol.8,pp.1137–1148,1993.

1018

50,9

III

39

Y.Q.G

ong,R.

B.Slee,N

.Fuk

ai,Y.Q

.Gon

g,R.

B.Slee,N

.Fuk

ai,G

.Raw

adi,S.

Roman-Rom

an,A

.M.R

eginato,H.W

.Wang,T.Cu

ndy,F.H.G

lorie

ux,D

.Lev,M

.Zacharin

,K.

Oexle,

J.Marcelin

o,W.Suw

airi,

S.Heeger,G.Sabatakos,S.A

pte,W.N

.Adk

ins,J.Allgrove,

M.A

rslan-Kirchn

er,J.A

.Batch,P.B

eighton,

G.C

.M.B

lack,R

.G.B

oles,L.M

.Boo

n,C.

Borron

e,H.G

.Brunn

er,G

.F.C

arle,

B.Dallap

iccola,A

.DeP

aepe,B

.Floege,M.L.H

alfhide,

B.Hall,R.

C.Hennekam,T.H

irose,A

.Jans,H.Jup

pner,C

.A.K

im,K

.Keppler-N

oreuil,A.

Kohlschu

etter,D.L

aCom

be,M

.Lam

bert,E

.Lem

yre,T.Lette

boer,L.Pelton

en,R

.S.

Ramesar,M

.Rom

anengo,H

.Som

er,E

.Steichen-Gersdorf,B.

Steinm

ann,

B.Sullivan,

A.

Superti-F

urga,W

.Swob

oda,M.J.van

denBo

ogaard,W

.Van

Hul,M

.Vikku

la,M

.Votruba,

B.Za

bel,T.Garcia,R.

Baron,

B.R.

Olse

n,andM.L.W

arman,“LD

Lreceptor-related

protein

5(LRP

5)affectsbo

neaccrualand

eyed

evelop

ment,”

Cell,vol.107,pp

.513–523,2001.

1009

84N/A

40

R.L.Jilka,G

.Hangoc,G.G

irasole,

G.Passeri,

D.C

.Williams,J.S.Ab

rams,B.

Boyce,H.

Broxmeyer,and

S.C.

Manolagas,“Increasedosteoclastdevelopm

entaftere

strogenloss-

mediatio

nby

interle

ukin-6,”Th

eAmerica

nJourna

lofC

linica

lNutrition,vol.257,pp

.88–91,

1992.

1008

48N/A

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Journal of Osteoporosis 7

Table1:Con

tinued.

Rank

Paper

Absolutenu

mbero

fcitatio

nsCitatio

ndensity

Levelof

evidence

41R.

B.Mazess,H.S.B

arden,

J.P.Bisek,andJ.Hanson,

“Dual-e

nergyX-

rayabsorptio

metry

fortotal-bod

yandregion

albo

ne-m

ineralandsoft-tissuec

ompo

sition,”

Journa

lofB

onea

ndMineralResearch,vol.51,pp

.1106–

1112,1990.

1000

43,4

III

42

B.L.Riggs,H.W

.Wahner,W.L.D

unn,

R.B.

Mazess,K.

P.Offo

rd,and

L.J.Melton

,“D

ifferentia

lchanges

inbo

ne-m

ineraldensity

ofthea

ppendiculara

ndaxialskeletonwith

aging-rela

tionshipto

spinalosteop

orosis,”Th

eJournalofClinica

lInvestigation,vol.67,pp.

328–335,1981.

971

30,3

III

43C.

Maniatopo

ulos,J.Sod

ek,and

A.H

.Melc

her,“Bon

e-form

ationinvitro

bystromalcells

obtained

from

bone-m

arrowof

youn

g-adultrats,”

CellandTissu

eResearch,vol.254,pp

.317–330,1988.

964

38,5

N/A

44

M.R

.McC

lung

,P.G

eusens,P.D

.Miller,H

.Zippel,W.G

.Bensen,

C.Ro

ux,S.A

dami,I.

Fogelm

an,T.D

iamon

d,R.

Easte

ll,P.J.Meunier,J.Y.R

eginste

r,R.

D.W

asnich,M

.Greenwald,J.Ka

ufman,and

C.H.C

hestnu

t,“Effectof

risedronateon

ther

iskof

hipfracture

inelderly

wom

en,”Th

eNew

Engla

ndJourna

lofM

edicine,vol.344

,pp.333–340,2001.

954

79,5

I

45P.Ducy,M.A

mlin

g,S.Takeda,M

.Prie

mel,

A.F.Schilling,F.T.Be

il,J.H.Shen,

C.Vinson

,J.

M.R

ueger,andG.K

arsenty,“Leptin

inhibitsbo

neform

ationthroug

hah

ypothalamicrelay

:Acentralcon

trolofb

onem

ass,”

Cell,vol.100,pp

.197–207,200

0.946

72,7

N/A

46

R.Lind

say,D.M

.Hart,J.M.A

itken,E

.B.M

acDon

ald,J.B.

And

erson,

andA.C

.Clarke,

“Lon

g-term

preventio

nof

postm

enop

ausaloste

oporosisby

estro

gen-e

videncefor

anincreasedbo

nemassa

fterd

elayed

onseto

festrogen-tre

atment,”La

ncet,vol.1,pp.1038–1041,

1976.

938

25,3

II

47

H.L.H

su,D

.L.L

acey,C

.R.D

unsta

n,I.Solovyev,A

.Colom

bero,E

.Tim

ms,H.L.Tan,G

.Ellio

tt,M.J.K

elley,I.Sarosi,

L.Wang,X.

Z.Xia,R.

Ellio

tt,L.Ch

iu,T.B

lack,S.Scully,C

.Ca

pparelli,S.Moron

y,G.Shimam

oto,M.B

.Bass,andW.J.B

oyle,

“Tum

ornecrosisfactor

receptor

family

mem

berR

ANKmediateso

steoclastdifferentiatio

nandactiv

ationindu

ced

byosteop

rotegerin

ligand,”

Nature,vol.96,pp

.3540–

3545,1999.

904

64,5

N/A

48M.G

owen,D

.D.W

ood,E.

J.Ihrie

,M.K

.B.M

cGuire,and

R.G.G

.Russell,“Aninterle

ukin-1

likefactorstim

ulates

bone-resorptionin

vitro

,”Proceedingso

fthe

Natio

nalA

cademyo

fScien

ceso

fthe

UnitedStatesofAm

erica

,vol.306,pp.378–380,1983.

903

30,1

N/A

49D.C

.Klein,and

L.G.R

aisz,“Prostaglandins

-stim

ulationof

bone

resorptio

nin

tissue

cultu

re,”En

docrinology,vol.86,pp.1436–4

0,1970.

880

20,4

N/A

50S.C.

Manolagas,“Birthanddeathof

bone

cells:B

asicregulatorymechanism

sand

implications

forthe

pathogenesisandtre

atmento

foste

oporosis,”A

merica

nJourna

lof

Medicine,vol.21,pp

.115–137,200

0.877

67,4

N/A

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8 Journal of Osteoporosis

Table2:Th

etop

tenpapersaccordingto

citatio

ndensity.

Rank

Paper

Absolutenu

mbero

fcitatio

nsCitatio

ndensity

Levelof

evidence

1

D.L.L

acey,E

.Tim

ms,andH.L.Tan,M

.J.K

elley,C.

R.Dun

stan,

T.Bu

rgess,R.

Ellio

tt,A.C

olom

bero,G

.Elliott,S.Scully,

H.H

su,J.Sullivan,N

.Haw

kins,E

.Davy,

C.Ca

pparelli,A.E

li,Y.X.

Qian,

S.Ka

ufman,I.Sarosi,V.

Shalho

ub,G

.Senaldi,J.

Guo

,J.D

elaney,and

W.J.B

oyle,

“Oste

oprotegerin

ligandisac

ytok

inethatregulates

osteoclastdifferentiatio

nandactiv

ation,”

Cell,vol.93,pp.165–176,1998.

2768

184,5

N/A

2W.J.B

oyle,

W.S.Sim

onet,and

D.L.L

acey,“Oste

oclastdifferentiatio

nand

activ

ation,”

Cell,vol.423,pp

.337–342,2003.

1651

165,1

N/A

3

W.S.Sim

onet,D

.L.L

acey,C

.R.D

unsta

n,M.K

elley,M.S.C

hang

,R.Luthy,H

.Q.

Nguyen,

S.Woo

den,

L.Be

nnett,T.Bo

one,G.Shimam

oto,M.D

eRose,R.

Ellio

tt,A.

Colom

bero,H

.L.Tan,G

.Trail,J.Sullivan,

E.Davy,N.B

ucay,L.R

enshaw

Gegg,T.

M.H

ughes,D.H

ill,W

.Pattison

,P.C

ampb

ell,S.Sand

er,G

.Van,J.Tarpley,P.D

erby,

R.Lee,andW.J.B

oyle,

Cell,vol.89,pp.309–

319,1997.

2629

164,3

N/A

4

H.Yasud

a,N.Shima,N.N

akagaw

a,K.

Yamaguchi,M

.Kinosaki,S.Mochizuki,A

.To

moyasu,K.

Yano

,M.G

oto,A.M

urakam

i,E.

Tsud

a,T.Morinaga,K.

Higashio,N.

Udagawa,N.Takahashi,and

T.Suda,“Oste

oclastdifferentiatio

nfactor

isaligand

foro

steop

rotegerin

osteoclasto

genesis-in

hibitory

factor

andisidenticalto

TRANCE

/RANKL

,”Proceedingso

fthe

Natio

nalA

cademyo

fScie

ncesoftheU

nited

StatesofAm

erica

,vol.95,pp

.3597–3602,1998.

2206

147

N/A

5

T.Ko

mori,H.Yagi,S.Nom

ura,A.Yam

aguchi,K

.Sasaki,K.

Sasaki,K

.Deguchi,Y.

Shim

izu,R.

T.Bron

son,

Y.H.G

ao,M

.Inada,M

.Sato,R.

Okamoto,Y.Kitamura,S.

Yoshiki,andT.Kishim

oto,“Targeteddisrup

tionof

Cbfa1resultsin

acom

pletelack

ofbo

neform

ationow

ingto

aturationalarresto

foste

oblasts

,”Ce

ll,vol.89,pp.

755–764,1998.

2132

133,2

N/A

6

Y.Y.Ko

ng,H

.Yoshida,I.Sarosi,H.L.Tan,E

.Tim

ms,C.

Capp

arelli,S.Moron

y,A.J.

Oliveira-dos-Santos,G.V

an,A

.Itie,W

.Kho

o,A.W

akeham

,C.R

.Dun

stan,

D.L.

Lacey,T.W.M

ak,W

.J.B

oyle,

andJ.M.Penninger,“OPG

Lisak

eyregulator

ofosteoclasto

genesis,lym

phocyted

evelop

mentand

lymph

-nod

eorganogenesis,”

Nature,vol.397,pp.315–323,1999.

1741

124,3

N/A

7

B.Ettin

ger,D.M

.Black,B

.H.M

itlak,R

.K.K

nickerbo

cker,T.N

ickelse

n,H.K

.Genant,C.

Chris

tiansen,P.D

.Delm

as,J.R

.Zanchetta,J.Stakkestad,C.

C.Gluer,K

.Kr

ueger,F.J.Coh

en,S.E

ckert,K.

E.En

srud

,L.V

.Avioli,P.Lips,and

S.R.

Cummings,“Re

ductionof

vertebralfracturer

iskin

postmenop

ausalw

omen

with

osteop

orosistre

ated

with

raloxifene,”Th

eJourna

lofthe

America

nMedica

lAssocia

tion,vol.282,pp

.637–6

45,1999.

1732

123,7

I

8

D.M

.Black,S.R

.Cum

mings,D

.B.K

arpf,J.A

.Cauley,D.E

.Thom

pson

,M.C

.Nevitt,D

.C.B

auer,H

.K.G

enant,W.L.H

askell,R.

Marcus,S.M.O

tt,J.C.

Torner,

S.A.Q

uand

t,T.F.Re

iss,and

K.E.

Ensrud

,“Ra

ndom

isedtrialofeffectof

alendron

ateo

nris

kof

fracture

inwom

enwith

existingvertebralfractures,”La

ncet,

vol.348,pp

.1535–1541,1996.

2067

121,5

I

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Journal of Osteoporosis 9

Table2:Con

tinued.

Rank

Paper

Absolutenu

mbero

fcitatio

nsCitatio

ndensity

Levelof

evidence

9S.R.

Cummings,M

.C.N

evitt,W

.S.B

rowner,K.

Ston

e,K.

M.Fox,K

.E.E

nsrud,J.

C.Ca

uley,D

.Black,and

T.M.V

ogt,“R

isk-fa

ctorsfor

hipfracture

inwhitewom

en,”

TheN

ewEn

gland

Journa

lofM

edicine,vol.332,pp.767–773,1995.

2102

116,7

I

10J.M.W

ozney,V.

Rosen,

A.J.C

eleste

,and

L.M.M

itsock,“N

ovelregu

latorsof

bone-fo

rmation-m

olecular

clonesa

ndactiv

ities,”Scien

ce,vol.242,pp.528–1534,

1988.

2662

106,4

N/A

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10 Journal of Osteoporosis

Table 3: Most frequent search terms (𝑛 = 11).

Search term Number of search terms foundFracture 18Osteoporosis 14Bone formation 9Osteoclast 8Bone mineral density 5Bone density 5Bone resorption 4Osteoblast 3Bone mass 2Dual energy X-ray absorptiometry 1Estrogen replacement therapy 1

Table 4: Top 12 authors who contributed to the top 50 list.

Author’s name Number of papers by authorS. R. Cummings 7W. J. Boyle 6H. K. Gennant 6D. L. Lacey 6D. M. Black 5C. R. Dunstan 5L. J. Melton 5M. C. Nevitt 5H. L. Tan 5C. Caparelli 4K. E. Ensrud 4I. Sarosi 4

paper each. The distribution of the most cited papers in thevarious journals can be seen in Figure 4.

The number of most cited papers according to the decadeof publication can be found in Figure 5. The majority ofpapers were published since 1990 (𝑛 = 39), whereas there isjust one in the 1960s. Eight of the top 10 papers according tothe citation density were published in the 1990s.

4. Discussion

In this study, Thomson ISI Web of Science was searched toanalyze the most cited papers on osteoporosis and relatedresearch and to define a list of “citation classics” in this field.

In order to identify the most cited papers and coverall aspects and the whole field of osteoporosis and relatedresearch not only the term “osteoporosis” per se, but alsoprocesses involved in the biology and pathology of boneand bone metabolism as well as risk factors and the conse-quences of the disease were used. Furthermore, diagnosticand therapeutic options were considered. Altogether 20search terms were used. The majority of articles could beattributed to “fractures” and “osteoporosis” (45.7% of papersaltogether). This underlines the magnitude of osteoporosisand osteoporotic fractures. Eleven out of 20 search termswerefound in the title of the papers, others in the abstract and

USAUKJapanCanada

FranceSwedenIsraelAustralia

11

1

22

3

6

34

Figure 3: Distribution of countries.

9

8

5

44

4

3

13

NEJMCellNatureJAMA

ScienceLancetPNASOthers

Figure 4: Distribution of journals.

1 2

8

29

10

0

5

10

15

20

25

30

35

60s 70s 80s 90s 00s

Figure 5: Number of papers published in each decade.

keywords. All keywords were found, but some papers did notreach enough citations to be put onto the list of the Top 50.

Articles on osteoporosis and related research were citedup to 3056 times; the top ten papers according to absolutenumbers were cited at least 1744 times. This fact shows theimportance of osteoporosis as it affects a large number ofpatients worldwide and being of interest for many differentmedical specialities. Papers on other conditions such as acute

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Journal of Osteoporosis 11

pancreatitis had amaximum of 1281 citations [13]; the highestcited papers on septic conditions reached 2932 [14], whereaspapers on epilepsy were cited even more frequently thanosteoporosis (3749 citations) [15]. Top ranked articles in otherfields such as papers on arthroscopic surgery or traumareached about 500 citations [9, 10]. In orthopaedic paediatricsjust four papers reached 100 citations [11].

The most cited paper in the present list was cited 3056times. It is the oldest in the list and was published by a singleauthor in 1956. The reason why this paper has been citedso often could be that “bone morphogenetic proteins” weredescribed and for years their existence seemed to be the coreof possible solutions for all aspects in bone metabolism [20].

395 authors contributed to the papers of the top 50list. This reflects the wide range of osteoporosis and relatedresearch. Some authors contributed more than once; oneauthor contributed seven times (Steven C. Cummings).

Regarding corresponding authors, in total, eight coun-tries contributed to the list. Authors from the United Statescontributed most frequently as corresponding author (𝑛 =34), followed by authors from the United Kingdom (𝑛 =6), Japan (𝑛 = 3), Canada and France (2 papers each),and Sweden, Israel, and Australia with one paper each. Allcountries are highly industrialized and are ranked among thetop in both economical and health-care expenditure. This isin accordance with previous analyses of other specialties ordiseases [3–17].

The ranking is led by the United States with 34 papers(68%).This predominance is in accordance with other analy-ses where theUS had the highest number ofmost cited papers[3–17]. This reflects the high frequency of research and thehigh scientific output in general and also in osteoporosis inthe United States.

All papers were published in English.This clearly demon-strates the predominance of the English language in publica-tions on osteoporosis and related research.

The spectrumof osteoporosis is also expressed in the largenumber of journals in which results of osteoporosis researchare published. Papers were published in 18 different journals.Although there are journals focusing on osteoporosis itselfand, more generally, on bone and bone metabolism, studiesare also published in journals with a wide spectrum andmoregeneral medical background as such.

Papers were attributed to three different categories. Theirdistribution can be seen in Figure 1. Most papers werefocusing on basic science.

Evidence Based Medicine has been introduced justrecently using levels of evidence. Level of evidence couldbe analyzed in 17 clinical papers (from the Clinical Sciencecategory). According to the guidelines of the Oxford Centrefor Evidence-BasedMedicine themajority of articles (𝑛 = 13)were level of evidence I, one paper was level of evidence II,and three papers level of evidence III. This points to the factthat there is a high quality of study design and evidence inclinical osteoporosis research.

Interestingly, the majority of papers were published since1990 (𝑛 = 39), whereas there is just one from the 1960s.Although bone changes were recognized quite early manysignificant advancements have been made in recent years.

Considering this trend further developments in the field areto be expected.

This study has limitations. Identifying the 50 most citedpapers they still remain a selection although using welldefined criteria. So, important and influential papers withlower citation frequency might have been missed. In somecases the value of contribution to the field cannot be quan-tified by the number of citations. However, with respect tothe aim of this study a bottom line is drawn. This approachseems to be more objective. Any other selection based onthe importance of papers would depend on personal favour.The absolute or relative number of citations of articles can beinfluenced by several factors and does not necessarily reflectthe importance of research that has been performed or hasbeen published [12], nor does it directly translate into clinicalpractice changes. The search was performed in the ThomsonISI Web of Science database. Therefore citations of articlesfrom other sources, such as textbooks, lectures, or digitalmedia could not be considered. Another weakness might bethe cross-sectional study design and research at a single pointin time with focus on the absolute number of citations.

A list of 50 most cited papers in osteoporosis and relatedresearch covers a broad range of medical subspecialities.This is reflected by the number of journals and decades.Studies focusing on basic and clinical science of osteoporosismainly dominate the literature in respect to absolute citationsnumbers. Considering the high number of high impactpapers in the last two decades further developments in thefield are to be expected.

Conflict of Interests

Lukas A. Holzer, Andreas Leithner, and Gerold Holzerdeclare that there is no conflict of interests regarding thepublication of this paper.

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