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Translation of clinical problems in osteoarthritis into pathophysiological research goals

Abstract

Osteoarthritis (OA) accounts for more disability among the elderly than any other disease and is associated with an increased mortality rate. The prevalence in Europe will rise in the future since this continent has a strongly ageing population and an obesity epidemic; obesity and age both being major risk factors for OA. No adequate therapeutic options, besides joint replacement, are available, although they are greatly needed and should be acquired by adequate research investments. However, the perspective on OA from a researcher's point of view is not always aligned with the perspective of a patient with OA. Researchers base their views on OA mainly on abnormalities in structure and function while patients consider OA as a collection of symptoms. In this viewpoint paper, we discuss the possibility of translating the most important clinical problems into pathophysiological research goals to facilitate the translation from bench to bedside and vice versa. This viewpoint is the outcome of a dialogue within the ‘European League Against Rheumatism study group on OA’ and People with Arthritis/Rheumatism across Europe (PARE) representatives.

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Translation of clinical problems in osteoarthritis into pathophysiological research goals

Author: van der Kraan, Peter M,Berenbaum, Francis,Blanco, Francisco J,Cosimo, de Bari,Lafeber, Floris,Hauge, Ellen,Higginbottom, Adele,Ioan-Facsinay, Andreea,Loughlin, John,Meulenbelt, Ingrid,Moilanen, Eeva,Pitsillidou, Irene,Tsezou, Aspasia,van Meurs, Joyce,Vin
Year: 2016
Source: https://trepo.tuni.fi/bitstream/10024/99572/1/translation_of_clinical_problems_2016.pdf
VIEWPOINT
T ansla ion o clinical p oblems in
os eoa h i is in o pa hophysiological
esea ch goals
Pe e M an de K aan,
1
F ancis Be enbaum,
2
F ancisco J Blanco,
3
de Ba i Cosimo,
4
Flo is La ebe ,
5
Ellen Hauge,
6
Adele Higginbo om,
7
And eea Ioan-Facsinay,
8
John Loughlin,
9
Ing id Meulenbel ,
10
Ee a Moilanen,
11
I ene Pi sillidou,
12
Aspasia Tsezou,
13
Joyce an Meu s,
14
Tonia Vincen ,
15
Ru h Wi oek,
16
Rik Lo ies,
17
On behal o he EULAR S udy g oup in OA (h p://
www.eula .o g/in es iga i e_ heuma ology_s udy_g oups.c m)
To ci e: an de K aan PM,
Be enbaum F, Blanco FJ,
e al. T ansla ion o clinical
p oblems in os eoa h i is
in o pa hophysiological
esea ch goals. RMD Open
2016;2:e000224.
doi:10.1136/ mdopen-2015-
000224
▸P epublica ion his o y o
his pape is a ailable online.
To iew hese iles please
isi he jou nal online
(h p://dx.doi.o g/10.1136/
mdopen-2015-000224).
Recei ed 8 Decembe 2015
Re ised 29 Feb ua y 2016
Accep ed 7 Ma ch 2016
Fo numbe ed a ilia ions see
end o a icle.
Co espondence o
D Pe e M an de K aan;
pe e . ande k aan@
adboudumc.nl
ABSTRACT
Os eoa h i is (OA) accoun s o mo e disabili y among
he elde ly han any o he disease and is associa ed
wi h an inc eased mo ali y a e. The p e alence in
Eu ope will ise in he u u e since his con inen has a
s ongly ageing popula ion and an obesi y epidemic;
obesi y and age bo h being majo isk ac o s o OA.
No adequa e he apeu ic op ions, besides join
eplacemen , a e a ailable, al hough hey a e g ea ly
needed and should be acqui ed by adequa e esea ch
in es men s. Howe e , he pe spec i e on OA om a
esea che ’s poin o iew is no always aligned wi h
he pe spec i e o a pa ien wi h OA. Resea che s base
hei iews on OA mainly on abno mali ies in s uc u e
and unc ion while pa ien s conside OA as a collec ion
o symp oms. In his iewpoin pape , we discuss he
possibili y o ansla ing he mos impo an clinical
p oblems in o pa hophysiological esea ch goals o
acili a e he ansla ion om bench o bedside and ice
e sa. This iewpoin is he ou come o a dialogue
wi hin he ‘Eu opean League Agains Rheuma ism
s udy g oup on OA’and People wi h A h i is/
Rheuma ism ac oss Eu ope (PARE) ep esen a i es.
OSTEOARTHRITIS (OA) IS A HUGE AND EVER
INCREASING PROBLEM
OA is he mos p e alen join disease and
accoun s o mo e disabili y among he
elde ly han any o he disease. I is es ima ed
ha OA a ec s abou 40 million people in
Eu ope.
12
OA can a ec each and e e y
join bu is mos common in he knee, hip,
spine and hand. Clinically, i is cha ac e ised
by join pain, limi a ion o mo emen , en-
de ness, s i ness, c epi us and a ious
deg ees o inflamma ion. OA is conside ed a
disease o he whole join o gan; s uc u al
changes include ca ilage fib illa ion,
fissu es, ull hickness loss o a icula ca il-
age, os eophy e o ma ion, changes in he
subchond al bone pla e, syno i is and fib osis
in syno ium o capsule.
To p o ide exac numbe s on he inci-
dence and p e alence o disease is a di ficul
ask. A majo cause o his is he ac ha
adiog aphic changes a e no always asso-
cia ed wi h join pain and ice e sa.
Mo eo e , OA is gene ally a slow p og essi e
disease. Epidemiological s udies a e di ficul
o compa e due o di e ences in s udy popu-
la ion and disease c i e ia. OA is ela i ely
in equen in people unde he age o
40 yea s bu defini ely inc eases wi h age.
Unde he age o 45 yea s, women a e less
a ec ed han males, bu his gende di e -
ence e e ses abo e 45 yea s. Eu ope has an
inc easingly ageing popula ion as well as an
obesi y epidemic; old age and obesi y a e
bo h majo isk ac o s o OA. Since cu -
en ly no he apeu ic op ions o he han
pain con ol and join eplacemen a e a ail-
able, he bu den o OA will con inue o ise
in he coming decades.
ABSENCE OF EFFECTIVE PHARMACOLOGICAL
TREATMENT
Analgaesics, anging om pa ace amol and
opia es o non-s e oidal an i-inflamma o y
d ugs (NSAIDs), and in a-a icula hyalu o-
nan, a e p esc ibed o ea ing pain bu
hei e ec is o en small (mean e ec -size
om 0.15 o 0.30) and in many pa ien s no
su ficien . Os eoa h i ic join s ha show
signs o inflamma ion a e o en ea ed wi h
in a-a icula co icos e oid. Ano he e y
impo an oppo uni y in OA managemen is
an de K aan PM, e al.RMD Open 2016;2:e000224. doi:10.1136/ mdopen-2015-000224 1
Os eoa h i is
change in li es yle, mainly by inc easing physical ac i i y
and imp o ing physical condi ion, o example, by
weigh loss. T ials a e ongoing wi h newe ea men s o
join pain ha a e p omising bu some imes wi h limi a-
ions due o unexpec ed d awbacks, o ins ance, unex-
pec ed apid disease p og ession in some pa ien s
ea ed wi h an an i ne e g ow h ac o s a egy.
3
T ea men o s uc u al disease p og ession in OA
join s is s ill a big challenge. Nu aceu icals, symp oma ic
slow ac ing d ugs o OA (SYSADOAs) and iscosupple-
men a ion a e p esc ibed wi h his aim in mind,
al hough he e is li le e idence o ully suppo his
claim. S udies wi h s on ium anela e show e ec s on
join space wid h, bu he clinical ele ance o he
epo ed small di e ence and he po en ial ca dio ascu-
la side e ec s ha e jus ified hal ing i s u he de elop-
men o pa ien s wi h OA.
4
Ul ima ely, join
eplacemen is he op ion o pa ien s wi h se e e symp-
oms and end-s age OA. Join eplacemen is a apidly
inc easing p ocedu e and o e 90% o join s a e
eplaced due o OA. Howe e , his is a cos ly p ocedu e
and is, especially in ela i ely young people, no a pe -
manen solu ion. Mo eo e , a ound 20% o he pa ien s
con inue o expe ience some o m o join pain e en
a e he p ocedu e has been success ully pe o med.
Thus, he unme needs in pa ien s wi h OA a e high
and he de elopmen o OA ea men s ha can bo h
p e en o ea s uc u al b eak down and imp o e
symp oms is inc easingly needed. Pe sonalised ea -
men , wi h a pa ien -specific s a egy, equi es bioma -
ke s ha s a i y pa ien s based on OA sub ype and
specific pa hophysiological p ocesses in ol ed, also
aking in o accoun ha hese p ocesses e ol e in a pe -
sonal manne du ing he p og ession o disease.
PATIENT AND RESEARCHER PERSPECTIVE ON OA
As is adequa ely exemplified by he pape o K aus e al,
he pe spec i e on OA om a esea che ’s poin o iew
is qui e di e en om he pe spec i e o a pa ien wi h
OA.
5
While he main ocus o he esea che is on
genes, p o eins and cells, signalling, and me abolic pa h-
ways and s uc u al aspec s, he ocus o he pa ien is on
pain, unc ional limi a ions, aes he ic damage due o
bony p oli e a ions and loss o daily and social ac i i ies.
A esea che iews OA as a ‘disease’based on i s abno -
mali ies in s uc u e and unc ion o igina ing om bio-
logical o (bio)chemical e idence while a pa ien
conside s OA as an illness, ‘ he human esponse o
disease’.
6
S a ing om basic pa hophysiological esea ch ques-
ions, esea che s ha e aken majo s eps in unde s and-
ing OA. We ha e come om he opinion on OA as a
simple wea and ea p ocess o a icula ca ilage o a
concep o OA as an o gan disease in complex in e -
ac ion wi h he human body as a whole. Ou unde -
s anding is inc easing eno mously and only some
gene al insigh s can be men ioned he e. Gene ic s udies
ha e shown ha specific gene a ian s (Smad3, Dio2
and GDF5, e c) a e associa ed wi h OA p e alence and
o se e i y.
78
The ole o ageing and cell senescence has
been implica ed in OA.
9
Fu he mo e, i has been
shown ha changes in chond ocy e beha iou , such as
inc eased p oduc ion o p o eoly ic enzymes, and e en
mos likely changes in chond ocy e di e en ia ion, play
a c ucial ole in deg ada ion o he a icula ca ilage
ma ix.
10 11
These changes in chond ocy e beha iou
a e go e ned by changes in ac i a ed signalling pa hways
and changed esponses o aged and senescen chond o-
cy es o hese s imuli.
12 13
Changes in he subchond al
bone can p edic subsequen symp oms o s uc u al
p og ession, and, ecen ly, i has been shown ha no
only local join inflamma ion bu also low-g ade sys emic
inflamma ion could con ibu e o he OA disease
p ocess.
14–16
To gain a u he and mo e obus unde s anding o
p ocesses ha occu in OA, i is impo an o ake in o
accoun in e ac ions be ween gene exp ession, epigen-
e ic egula ion and en i onmen in clinically well-
defined pa ien s.
RECOGNITION OF DIFFERENT OA PHENOTYPES
OA has been his o ically classified based on join loca-
ion bu no on he unde lying pa hophysiological
p ocess.
17
I becomes mo e and mo e clea ha OA,
e en in a specific join , is be e classified acco ding o
specific ea u es ha a e p esumably a esul o specific
unde lying disease p ocesses.
18
End-s age OA in a pa -
icula join in di e en pa ien s can be iewed as he
final common ou come o a a ie y o pa hophysiological
p ocesses ha di e , o ha e di e ed, be ween hese
pa ien s. Classifica ion, no based on loca ion bu on he
unde lying disease p ocess, will be a aluable ins umen
no only o u he elucida e OA pa hophysiology and
also o op imise clinical ials, in pa icula pa ien
selec ion.
No only migh be e classifica ion o pa ien s by OA
pheno ype be a majo ad ance, bu imp o ed me hods
o ea ly de ec ion o OA a e o c ucial impo ance as
well. As ea ly OA has an ex ended subclinical disease
phase ea ly changes in an OA-a ec ed join emain
unde he ada . As a consequence, in e en ion is
in a iably delayed un il se e e, and maybe e en i e e s-
ible, s uc u al damage has occu ed. To imp o e
disease-modi ying in e en ions, me hods and s a egies
ha e o be de eloped ha can de ec ea ly, meaning ul
and p edic i e OA-associa ed changes in he join and
ha can ack he esul o an e en ual in e en ion.
THE OSTEOARTHRITIS RESEARCH SOCIETY
INTERNATIONAL DEFINITION OF OA
OA is a he e ogeneous disease and in his iewpoin and
p eceding discussions wi hin he Eu opean League
Agains Rheuma ism (EULAR) s udy g oup, we use he
d a defini ion o he Os eoa h i is Resea ch Socie y
2 an de K aan PM, e al.RMD Open 2016;2:e000224. doi:10.1136/ mdopen-2015-000224
RMD Open
In e na ional
5
as a wo king defini ion. The au ho s o his
defini ion and he OA s udy g oup a e ully awa e ha his
defini ion will be modified acco ding o he u he eluci-
da ion o OA p ocess(es) and disease pheno ypes.
Os eoa h i is is a diso de in ol ing mo able join s cha ac-
e ised by cell s ess and ex acellula ma ix deg ada ion
ini ia ed by mic o- and mac o-inju y ha ac i a es maladap-
i e epai esponses including p o-inflamma o y pa hways
o inna e immuni y. The disease mani es s fi s as a molecu-
la de angemen (abno mal join issue me abolism) ol-
lowed by ana omic, and/o physiologic de angemen s
(cha ac e ised by ca ilage deg ada ion, bone emodelling,
os eophy e o ma ion, join inflamma ion and loss o
no mal join unc ion) ha can culmina e in illness.
5
TRANSLATION OF CLINICAL PROBLEMS INTO
PATHOPHYSIOLOGICAL RESEARCH GOALS
A ecen EULAR ini ia i e iden ified ou esea ch p io -
i y a eas: epidemiology, imaging and bioma ke s, pa ho-
genesis and he apy,
2
which se ed as he basis o he
fi s call o p ojec s issued by Founda ion o esea ch
in heuma ology. In his iewpoin pape , classifica ion
o ele an pa hophysiological esea ch goals is based on
hese p io i y a eas (box 1). The esea ch goals ha
we e iden ified wi hin he s udy g oup a e no p io i-
ised, as in ou opinion he esea ch goals ha e o be
eached in pa allel. Fo example, iden ifica ion and al-
ida ion o a ge s o he apy a e no achie able wi hou
be e insigh in o he OA pa hogenesis and imp o e-
men o ea ly de ec ion and disease s a ifica ion.
Mo eo e , ea ly de ec ion and disease s a ifica ion
canno be accomplished wi hou us wo hy imaging
and unc ional bioma ke s.
EPIDEMIOLOGY
Epidemiology is, in a s ic sense, no he majo me hod-
ology o pa hophysiological esea ch. Howe e , due o
he in eg a ion o epidemiology and gene ics (gene ic
epidemiology) and he ecogni ion o di e en OA phe-
no ypes, esea ch in his a ea is o high alue in b inging
oge he clinical p oblems, and pa hophysiological
esea ch goals and unde s anding. Iden ifica ion o
gene ic a ian s in pa ien s wi h OA, bo h genomic and
mi ochond ial, will iden i y pheno ype-specific pa ho-
genic pa hways ha will be undamen o pheno ype-
specific OA he apies. Mo eo e , elucida ion o he ole
o epigene ic changes in specific OA pheno ypes has he
po en ial o p o ide a oadmap o a ge ed and pa ien
g oup-specific he apy.
IMAGING AND BIOMARKERS
Iden ifica ion and alida ion o imaging echnologies
and bioma ke s is o u mos impo ance o ea ly disease
de ec ion, o classifica ion o OA pheno ypes, disease
ac i i y and p ognosis and o e alua ion o he apy
esponse. Imaging and bioma ke s should bo h o m a
eliable eflec ion o unde lying disease p ocesses.
Ideally, a bioma ke i sel should be an in eg al pa o
he ac ual disease p ocess in OA and a sign o a specific
OA pheno ype. Iden ifica ion o OA pheno ypes and he
esponse o s a ified in e en ions will mos likely
depend on he combina ion o join imaging and bio-
ma ke quan ifica ion.
PATHOGENESIS
The pa hogenesis o OA is a om unde s ood and will
be di e en in he a ious OA pheno ypes. I has
become mo e and mo e clea ha he whole join is
a ec ed in OA and ha he di e en issues o he join
communica e and influence each o he ’s eac ions. To
eally comp ehend he OA disease p ocess, he commu-
nica ion be ween he a ious join issues should be
unde s ood in a pheno ype-specific con ex and be
s udied in he e y ea ly s ages o OA de elopmen .
In many pa ien g oups, a causal ela ionship be ween
mechanical changes in he join and OA is p obable.
Box 1 Majo pa hophysiological esea ch goals
Epidemiology (gene ic epidemiology)
▸To iden i y and elucida e he ole o gene ic a ian s in
Os eoa h i is (OA) pheno ypes;
▸To iden i y and elucida e he ole o epigene ics in OA
pheno ypes;
▸To iden i y and elucida e he ole o mi ochond ial gene ic a -
ian s in OA pheno ypes.
Imaging and bioma ke s
▸Iden i y ma ke s o ea ly OA;
▸Iden i y ma ke s o OA pheno ypes;
▸Iden i y ma ke s o disease ac i i y;
▸Iden i y ma ke s o disease p og ession;
▸Iden i y p edic i e ma ke s o he apeu ic esponse;
▸Iden i y ma ke s o e alua e he he apeu ic esponse.
Pa hogenesis
▸To unde s and issue communica ion in OA (be ween ca ilage,
subchond al bone, syno ium, essels, adipose issue);
▸To unde s and non-ca ilage pa hology in OA;
▸To unde s and he ole o chond ocy e di e en ia ion in OA;
▸To unde s and he ole o join auma and epai in OA;
▸To unde s and he mechanism o mechanical join inju y and
he ansla ion o in lamma ion and epai ;
▸To unde s and he ela ionship be ween syno i is and adio-
g aphic p og ession;
▸To unde s and he ea lies s ages o OA;
▸To unde s and he di e ence be ween OA pheno ypes;
▸To unde s and he o igins o pain;
▸To unde s and he ela ionship be ween pain and s uc u e;
▸To unde s and he ela ionship be ween syno i is and pain;
▸To unde s and he ela ionship be ween ageing and OA;
▸To unde s and he ela ionship be ween gende and OA;
▸To unde s and he ole o sys emic ac o s in OA;
▸To de ine he mechanisms by which como bidi ies in luence
he OA p ocess ( a and glucose me abolism).
The apy
▸To iden i y and alida e a ge s o he apy (symp oms and
s uc u e).
an de K aan PM, e al.RMD Open 2016;2:e000224. doi:10.1136/ mdopen-2015-000224 3
Os eoa h i is
Howe e , he exac ole o mechanical (o e ) load in
no mal join physiology and OA is no ye known.
Mo eo e , he ole o in insic join epai o ailing
in insic join epai in OA is s ill obscu e. The ela ion-
ship be ween s uc u al join changes and symp oms,
among o he s, pain, is s ill an enigma. I is no clea
which issues a e he majo sou ce o join pain, pe haps
bone o syno ium o whe he he e is a ole o p o-
duc s eleased by damaged ca ilage in join pain.
The ela ionship be ween una oidable ac o s, such as
ageing and gende , and OA pheno ype-specific pa ho-
physiology has s ill o be elucida ed. Fu he mo e, how
sys emic ac o s and como bidi ies, such as obesi y and
diabe es, a ec he de elopmen and p og ession o OA,
needs u he insigh .
THERAPY
The majo goal o pa hophysiological esea ch in OA is
he iden ifica ion and alida ion o a ge s o he apy.
These a ge s can ei he be s uc u al a ge s o symp-
oma ic a ge s, mainly pain. Ideally, hese a ge s should
be combined as a single agen , albei wi hou igno ing
he ac ha di e en OA pheno ypes may equi e di e -
en a ge ed he apies.
This iewpoin a icle a emp s o b idge he gap
be ween majo clinical p oblems o OA wi h pa ho-
physiological esea ch goals o he OA esea ch commu-
ni y, o acili a e he ansla ion om bed o bench and
ice e sa. I is an icipa ed ha his a icle can be a
guide o OA esea che s, in e na ional o ganisa ions
and unding agencies o acili a e hei discussions on
di ec ions o esea ch and unding.
Au ho a ilia ions
1
Depa men o Expe imen al Rheuma ology, Radboud Uni e si y Medical
Cen e , Nijmegen, The Ne he lands
2
Facul y o Medicine Pie e and Ma ie Cu ie Pa is VI, INSERM UMR-S938,
Sain -An oine Hospi al, Pa is, F ance
3
Rheuma ology Di ision, Ins i u o de In es igación Biomédica de A Co uña
(INIBIC), Complexo Hospi ala io Uni e si a io de A Co uña (CHUAC), Se gas,
Uni e sidade da Co uña (UDC), A Co uña, España
4
Musculoskele al Resea ch P og amme, Ins i u e o Medical Sciences,
Fo es e hill, Abe deen, UK
5
Depa men o Rheuma ology and Clinical Immunology, Uni e si y Medical
Cen e U ech , U ech , The Ne he lands
6
Depa men o Clinical Medicine, The Sec ion o Rheuma ology, Aa hus,
Denma k
7
EULAR PARE Pa ien Resea ch Pa ne and Keele Uni e si y, Newcas le-
unde -Lyme, UK
8
Depa men o Rheuma ology, Leiden Uni e si y Medical Cen e , Leiden,
The Ne he lands
9
Musculoskele al Resea ch G oup, Newcas le Uni e si y, Ins i u e o Cellula
Medicine, The Medical School, Newcas le upon Tyne, UK
10
Depa men o Molecula Epidemiology, LUMC, Leiden, The Ne he lands
11
The Immunopha macology Resea ch G oup, Uni e si y o Tampe e School
o Medicine and Tampe e Uni e si y Hospi al, Tampe e, Finland
12
EULAR PARE Pa ien Resea ch Pa ne , Nicosia, Cyp us
13
Depa men o Biology, Uni e si y o Thessaly, School o Medicine, La issa,
G eece
14
Gene ic Labo a o y, Depa men o In e nal Medicine, E asmus MC,
Ro e dam, The Ne he lands
15
ARUK Cen e o OA Pa hogenesis, Uni e si y o Ox o d, Ox o d, UK
16
Depa men o Rheuma ology, Uni e si y Hospi al Ghen , Ghen , Belgium
17
Labo a o y o Tissue Homeos asis and Disease, Depa men o De elopmen
and Regene a ion, KU Leu en and Di ision o Rheuma ology, Skele al Biology
and Enginee ing Resea ch Cen e , Uni e si y Hospi als Leu en, Leu en,
Belgium
Compe ing in e es s None decla ed.
P o enance and pee e iew No commissioned; ex e nally pee e iewed.
Da a sha ing s a emen No addi ional da a a e a ailable.
Open Access This is an Open Access a icle dis ibu ed in acco dance wi h
he C ea i e Commons A ibu ion Non Comme cial (CC BY-NC 4.0) license,
which pe mi s o he s o dis ibu e, emix, adap , build upon his wo k non-
comme cially, and license hei de i a i e wo ks on di e en e ms, p o ided
he o iginal wo k is p ope ly ci ed and he use is non-comme cial. See: h p://
c ea i ecommons.o g/licenses/by-nc/4.0/
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