INT R O D UC T IO N
Be hcet disease is characte rized by recurre nt pa inful ora l ulce r a nd ge nita l ulce r, s kin diseases a nd uve itis . It may involve ca rdiovascula r, gastrointestina l a nd centra l ne rvous system, as well as joints . The etiology is
unknown a nd its pathophys iology is incomplete ly unde rstood. The diagnos is of Be hcet disease prima rily de pe nds on the patie nt's history a nd clinica l findings . Arthritic ma nifestation is one of the minor manifestations a nd it is us ua lly ove rlooked. The author a na lyzed 35 cas es of Be hcet disease patie nts , mainly for a rthritic manifestations .
MA T E R IA LS A N D MET HO DS 1. Patie nts
Among the patie nts who vis ited the Rhe umatology Divis ion, Ke imyung Unive rs ity Dongsa n Medica l Ce nte r,
C lin ic a l A n a ly s is o f Be h c e t D is e a s e :
Art h r it ic M a n if e s t a t io n s in Be h c e t D is e a s e m a y p r e s e n t a s S e r o n e g a t iv e R h e u m a t o id
Art h r it is o r P a lin d r o m ic R h e u m a t is m
J a e - Ho P a r k , M . D .
De p a rt m e nt o f Int e rn a l M e d ic in e , Ke im y u ng U n iv e rs ity Do n g s a n M e d ic a l Ce n t e r, 19 4 Do ng s a n - Do ng , C h u ng - K u , T a e g u , 7 0 0 - 7 1 2 , Ko re a
O bj e c t iv e s : T o a n a ly z e a rt h rit ic m a n if e s t at io n s in Be h c e t d is e a s e , w h ic h is o n e o f t h e m o s t c o m m o n m a n if e s t at io n s o f Be h c e t d is e a s e .
M e t h o d s : A m o ng t h e p at ie nt s w h o v is it e d t h e R h e u m a t o lo g y Div is io n , Ke im y u ng U n iv e rs ity Do ng s a n M e d ic a l Ce nt e r, T a e g u , Ko re a f ro m M a rc h 1 9 9 7 t o Fe b ru a ry 1 9 9 8 , 3 5 p a t ie nt s , w it h m o re t h a n 3 m o nt h s f o llo w - u p , w e re c o m p a t ib le f o r t h e d iag n o s is o f Be h c e t d is e a s e a c c o rd ing t o t h e S h im iz u c rit e ria , a f t e r e x c lu s io n o f u n c e rt a in o r p o s s ib le Be h c e t c a s e s . T h e p re s e n c e o f v a rio u s m a n if e s t a t io n s w a s e v a lu a t e d . R e g a rd ing t h e j o int m a n if e s t a t io n s , t h e inv o lv e d j o int , s ig n s a n d t h e p att e rn o f t h e a rt ic u la r s y m p t o m s w e re e x a m in e d . Ba s ic la b o ra t o ry t e s t s , H LA s t u d ie s a n d s im p le ra d io lo g ic s t u d ie s w e re d o n e .
Re s u lt s : A ll 3 5 p at ie nt s h a d e v id e nt , re c u rre nt , p a inf u l o ra l u lc e rs by t h e s t u d y d e f in it io n . G e n it a l u lc e rs w e re f o u n d in 2 9 % , s k in le s io n s in 7 7 % , uv e it is in 9 % , g a s t ro int e s t in a l u lc e rat io n s in 6 % a n d v a s c u la r m a n if e s t at io n s in 6 % . J o in t m a n if e s t at io n s a p p e a re d in 9 7 % . Kn e e ( 9 1% ) , p ro x im a l int e rp h a la ng e a l ( 5 3 %) a n d m e t a c a rp o p h a la ng e a l j o int s ( 2 1% ) w e re t h e m a in s it e s . T e n d e rn e s s w a s p ro m in e nt in 9 1% a n d s w e lling in 4 4 % . Po ly a rt ic u la r p re s e nt a t io n w a s f o u n d in 4 7 % . In m o s t c a s e s ( 7 6 .4 % ) , t h e a rt ic u la r s y m p t o m w a s s h o rt - la s t ing . C - re a c t iv e p ro t e in w a s lik e ly t o b e p o s it iv e in a ct iv e Be h c e t d is e a s e . H LA B5 1 w a s p o s it iv e in 4 6 % .
Co nc lu s io n s : In Be h c e t d is e a s e , v a rio u s m a n if e s t at io n s c a n b e f o u n d . T h e a rt h rit ic m a n if e s t at io n s e e m s q u it e c o m m o n . It m ay p re s e nt a s s e ro n e g at iv e rh e u m a t o id a rt h rit is . Ot h e rw is e , it m ay p re s e n t a s p a lin d ro m ic rh e u m at is m .
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Ke y W o rd s : Be h c e t , A rt h rit is , S e ro n e g a t iv e , R h e u m a t o id
Address reprint reques ts to : Jae - Ho Park, M.D., Departm ent of Internal Medicine, Keimy ung University Dongsan Medical Center, 194 Dongsan- Dong, Chung- Ku, Taegu, 700- 712, Korea
The present res earch has been conducted by the Bisa Res earch Grant of Keimy ung University in 1997.
Taegu, Korea from March 1997 to Februa ry 1998, 52 patie nts were compatible for the diagnos is of Behcet diseas e according to the Shimizu crite ria
1 ). Forty seve n patie nts with more tha n 3 months follow- up we re e nrolled in this study. Forty three patie nts we re refe rred to the Rhe umatology Divis ion by prima ry ca re phys icia ns , two from De partment of Ophtha lmology a nd two from Ge ne ra l S urgery in Ke imyung Unive rs ity Dongsa n Medica l Ce nte r.
They had bee n diagnos ed as having Be hcet disease by ca reful history ta king, medical record review and thorough phys ica l exa mination. On initia l vis it, it us ua lly took more tha n thirty minutes . All patie nts we re followed- up close ly a nd they vis ited the hos pita l eve ry two wee ks . A direct te le phone number was give n to the patie nts and, whe neve r they fe lt uncomfortable with ill- defined symptoms , they discuss ed with the exa mine r. The S himizu crite ria we re retros pective ly a nd strictly a pplied aga in, a nd five unce rta in patie nts we re excluded.
Es pecially, regarding a n ora l ulce r, only the patie nts who compla ined of a n evide nt, recurre nt, pa inful one were included. "Poss ible " type of five Behcet cas es we re excluded a nd two patie nts , who ca rried anothe r a utoimmune diagnos is (S LE), we re excluded, too. Thirty five patie nts we re fina lly included in this study.
2. Clinica l fe atures
The prese nce of various ma nifestations we re eva luated a nd recorded as pos itive or negative . Recurre nt a phthous ulce ration in the mouth, va rious s kin les ions (e rythe ma nodos um- like e ruptions , s ubcuta neous thrombophle bitis , hype r- irrita bility of the s kin), eye les ions (recurre nt hypopyon iritis or iridocyclitis , chorioretinitis) a nd genita l ulce rations we re eva luated. The pres ence of joint ma nifestations , gastrointestina l a nd vascula r les ions , e pididymitis a nd centra l ne rvous syste m involve me nts we re eva luated too.
They we re class ified according to the s ubtypes .
3 . J oint ma nifestations
Arthropathy was defined as arthralgia with the pres ence of swe lling a nd/or te nde rness . Regarding the joint ma nifestations , the involved joints , te nde rness , swe lling and the pattern of the a rticula r symptoms we re eva luated. The patte rn of involve me nt included the number of involved joints and the duration of a rthropathy.
4 . La boratory a nd radiologic eva luation
Bas ic la boratory tests , including CBC, e rythrocyte
s edime ntation rate (ES R, Weste rgre n), C- reactive protein (CRP), complement, immunoglobulin, rhe umatoid factor (RF) a nd a ntinuclea r a ntibody (ANA), we re done . HLA studies we re done us ing Te rasa ki tray(One La mbda, Inc.
U.S.A.). Synovia l fluid ana lys is was tried whe neve r the patie nt had s ufficie nt amount of swe lling a nd agreed to as pirate.
Simple radiologic studies of ma inly involved joints we re done .
5. Compa ris on with rhe umatoid a rthritis (RA)
The prese nce a nd the duration of morning stiffness , which is re lieved by exe rcise , we re a lso eva luated. The involved joints , tende rness , swe lling a nd the numbe r of involved joints we re eva luated, as a lready me ntioned a bove . RF a nd s imple radiologic studies of ma inly involved joints we re eva luated aga in, as a lready mentioned above , for the purpose of compa ring the data with those of rhe umatoid a rthritis .
The na mes of the initia l diagnos is of the patie nts with joint ma nifestations we re as ked. Rega rding oro- ge nital ulce rs or s kin les ions , the a uthor as ked whethe r they we re as ked of the prese nce of them by the ir prima ry ca re phys icia ns .
R E S U LT S
1. Patie nt cha racte ristics
These a re s hown in Table 1. Mea n age was 37 a nd disease onset was 3 1. The ra nge of duration betwee n the first clinica l ma nifestation and the diagnos is was from 1 to 25 yea rs . Eighty pe rce nt of the patients we re female .
Ta ble 1. Cha ra cte ris tic s of Patie nts (n=35 )
Age (yrs) 36.6 ± 11.6
Ons et Age (yrs) 30.5 ± 10.1
Sex(M:F) 7 : 28
Data s hown as mea n ± SD.
2. Clinica l feature s a nd inte rpretation a ccording to the s ubtype
All 35 patients had evide nt, recurre nt, pa inful ora l
ulce rs by the study definition. In 46%, they pres ented as
multiple forms . Ge nita l ulcers we re found in 29%. Va rious
s kin les ions , including e rythema nodos um- like e ruption,
s ubcuta neous thrombophle bitis a nd hype r- irrita bility of the s kin we re noted in 77%. Uve itis was evide nt in 9% of the patie nts . J oint ma nifestations appea red in 97%.
Gastrointestina l ulce rations and vas cula r ma nifestations we re found only in 6%, res pective ly. In vas cula r ma nifestations , one patie nt s howed three vascula r eve nts (ce re bra l infa rction a nd carotid, fe mora l a ne urys ms).
Epididymitis a nd ce ntra l ne rvous syste m involve me nt we re not prese nt.
The complete type was found only in 3%. Most of the m we re incomplete a nd the s us pected type. The poss ible type was 0%, s ince it was excluded origina lly.
These a re s umma rized as Ta ble 2.
Ta ble 2 . C linic a l Fe ature s a nd S ubtype s (n=35)
No .of Pt %
Ma nife s tatio ns
Ora l ulce r 35 100
Ge nita l ulce r 10 29
Skin les ion 27 77
Uve itis 3 9
Arthropathy 34 97
GI ulce r 2 6
Vascula r 2 6
Epididymitis 0 0
CNS les ion 0 0
S ubtype
Complete 1 3
Incomplete 5 14
Suspected 29 83
Poss ible 0 0
3 . J oint ma nifestations
J oint ma nifestations a ppea red in 34 out of 35 patie nts (97%). Knee, proxima l inte rphala ngea l a nd metaca rpopha la ngea l joints we re the ma in s ites . Othe r involved joints included wrist, e lbow, s houlde r, a nkle , MTP a nd DIP. Tende rness was prominent in 9 1% and swe lling was noted in 44%. In numbe r of affected joints , monoa rticula r was 38%, oligoa rticula r 15% a nd polya rticula r 47%. In most cas es , the a rticula r symptom was s hort- lasting. The duration of a rthropathy was less tha n one wee k in 59%, one to four wee ks in 18%, pe rs isting more tha n 4 wee ks in 18%.
These a re s umma rized as Ta ble 3.
Ta ble 3 . Jo int Ma nife s tatio ns in Pe rc e ntag e s (n=34 )
Involved J oint Knee 9 1
PIP 53
MCP 2 1
Wrist 18
Elbow 15
Shoulde r 12
Ankle 9
MTP 3
DIP 3
Sign Te nde rness 9 1
Swe lling 44
Numbe r of J oint Monoa rticula r 38 Oligoa rticula r 15
Polya rticula r 47
Duration < 1 week 58.8
1 to 4 wee k 17.6
> 4 wee k 17.6
Unclea r 5.8
PIP : proxima l inte rpha la ngea l MCP : metaca rpopha la ngea l MTP : metata rsopha la ngea l DIP : dista l interpha la ngea l
4 . La boratory a nd radiologic studie s
Bas ic la boratory tests , including CBC, ES R, comple me nt a nd immunoglobulin were nons pecific(data not s hown) exce pt CRP. CRP was pos itive in 12 patie nts a nd the mea n conce ntration was 2.02 mg/dl (normal <
0.32). It was pos itive in a ll complete type a nd in most of incomplete type . It was also pos itive in some of s us pected type who had ve ry active or adva nced manifestations . Thes e a re s ummarized as Ta ble 4.
Ta ble 4 . CRP Po s itiv ity in Ea c h S ubtype
S ubtype No .of Patie nt %
Complete (n=1) 1 100
Incomplete (n=5) 4 80
Suspected(n=29) 7 24
Tota l(n=35 ) 12 34
RFs we re found in 9% a nd they we re all in low tite r.
ANA was not found at a ll. HLA B5 1 was pos itive in 46%(13/28). Synovia l fluid ana lys is was ava ila ble in 3 patie nts . All patie nts s howed infla mmatory synovia l fluid with polymorphonuclear ce lls domina nt.
Radiologic studies of ma inly involved joints we re
ava ila ble in 85% (29/34) of patie nts . Among these , 90%
we re norma l. Abnorma l findings included minima l joint s pace narrowing and bony osteophytes .
5. Compa ris on with RA
Thirty five pe rce nt(12/34) of patients compla ined of morning stiffness . It lasted less tha n 15 minutes in a ll patie nts .
Polya rticula r presentation was found in 47%. PIP, MCP, wrist, e lbow, s houlde r, ankle and knee were commonly involved. These we re a lready s hown in Table 3.
Thirty one patie nts vis ited loca l medica l clinics due to the ir joint proble ms . In Ta ble 5, initia l diagnoses of the patie nts by the ir prima ry ca re phys icia ns , late r found as Be hcet a rthritis , we re s ummarized.
Ta ble 5 . Initia l Dia g no s is By Prima ry Ca re P hys ic ia ns (n=3 1)
Diagnos is No.of Patie nt %
RA, se ropos itive 2 6.4
RA, se ronegative 14 45.2
Arthritis , unce rta in 15 48.4
Sixtee n patie nts out of 3 1 with joint ma nifestations we re ca rrying a diagnos is of rhe umatoid a rthritis . None of the m we re as ked by the ir prima ry ca re phys icia ns whethe r they had recurre nt oro- ge nita l ulce rs or e rythe ma nodos um- like s kin les ions . No definite answe r was obta ined from the ir prima ry ca re phys icians whe n the patie nts as ked about the re lation of s kin les ion a nd the a rticula r symptoms .
D IS C US S IO N
Be hcet disease is a syste mic disease clas s ified a mong vasculitis . The clinica l picture is cha racte rized by mucocuta neous a nd ophtha lmologic ma nifestations . It is see n mostly in countries a long the "Silk Road", which include Turkey, Ira n, J a pa n, China a nd, poss ibly, Korea . Be hcet disease is diagnosed by a few set of diagnostic criteria , including the S himizu diagnostic crite ria
1)a nd the Inte rnational Study Group crite ria
2 ). In this study, the S himizu crite ria we re us ed s ince they we re useful in dea ling with minor ma nifestations , including a rthritis . The S himizu crite ria a re composed of major a nd minor crite ria . Major crite ria include recurre nt a phthous
ulce ration in the mouth, s kin les ions (e rythe ma nodos um- like e ruptions , s ubcuta neous thrombophlebitis , hyper- irrita bility of the s kin), eye les ions (recurrent hypopyon iritis or iridocyclitis , chorioretinitis) a nd genita l ulce rations . Minor criteria include a rthritic symptoms and s igns (a rthra lgia , swelling, redness ), gastrointestina l les ions (a ppe ndicitis- like pains , me le na, etc.), e pididymitis , vas cula r les ions (occlus ion of blood ves se ls , a ne urys ms), a nd ce ntra l ne rvous syste m involve me nts (bra in ste m syndrome , me ningo- e nce pha lomyelitic syndrome , confus iona l type). It was proposed by the m that if a ll four of the major symptoms a ppea red during the clinica l course of the disease , the syndrome would be class ified as "complete ". The "incomplete " type requires three majors or one major symptom a nd definite ocula r involve me nt. The "s us pected" type requires two major symptoms , a nd the "poss ible " type requires one major symptom.
The re are two comme nts that s hould be e mphas ized.
First, in most cases with Be hcet disease , va rious clinica l manifestations occur in seque nce
3 ). Recurrent ora l ulcer is the most common a nd the ea rliest symptom, a nd it is followed by ge nita l a nd s kin les ions . After the s kin les ions , a rthritis , ne urologica l ma nifestations a nd ocula r les ions occur which mea ns , a lthough ocula r involve me nt te nds to be the most se rious proble m, it us ua lly does not occur ve ry ea rly in the course of the disease . In othe r words , a lthough the a ppea ra nce of uve itis makes the diagnos is of Be hcet disease "complete", it dose not necessa rily mea n that we s hould wa it till the patie nt deve lops full syste mic, letha l ma nifestations to confirm the diagnos is . Second, among the so- ca lled minors , arthritic manifestation is known as the most common manifestation
4 - 7 ).
The purpose of this study is to e mphas ize the clinica l
s ignifica nce of Be hcet dis ease , es pecia lly whe n the
patie nts prese nt with a rthritic ma nifestations . In Korea ,
there we re two re ports focus ing a rthritic ma nifestations in
Be hcet disease among 150 pa pe rs for Be hcet disease
8 ,9 ).
Howeve r, one
8 )of them was done in Be hcet Disease
S pecia lty Clinic with a lready known Be hcet diseas e
patie nts , a nd the othe r
9 )did not mention in deta il how the
patie nts prese nted to the doctors . The pres ent study was
not conducted at Be hcet Disease Specia lty Clinic, a nd the
a uthor did not inte nd to collect a ll Be hcet patie nts from
other de pa rtme nts . Most of the m just ca me to the
Rhe umatology Divis ion with a rthra lgia or a rthritis , one
a mong va rious ea rly ma nifestations . That is why the
a rthropathy was the most common ma nifestation, excluding ora l ulce r, s ince it was pre requis ite to be e nrolled in this study. S ince most of the m compla ined of a rthritis , the earlie r ma nifestation, the s us pected type occupied most of this study group, instead of the clinica lly more adva nced type , s uch as the incomplete type . The lesse r prese nce of HLA B5 1 is a lso explainable by this reas on. It was known that the re was a n ass ociation between the prese nce of HLA B5 and more seve re types of Be hcet disease
1 0 - 13 ). Freque ncy of non- a rthritic clinica l features we re s imila r to those of previous re ports
4 - 7 ), a lthough the s ize of the prese nt study group was too s mall to compa re with.
Knee was the most commonly affected joint, as previous ly re ported
8 , 9 , 1 4 ). Sixtee n patie nts with joint ma nifestations we re ca rrying a diagnos is of RA whe n they we re first e nrolled in the prese nt study. Most of the m we re notified by the ir prima ry ca re phys icia ns as having se ronegative RA. It is s peculative that they a re regarded as satisfying the class ification crite ria for RA by the a rticula r involve me nt, morning stiffness
1 5 ). It was like ly that most doctors we re awa re of RA a nd they knew that rhe umatoid factor might not be found in some RA patie nts . To be class ified as RA, the joint swe lling s hould be prese nt a nd pe rs iste nt, instead of s imple te ndernes s or tra ns ie nt a rthritic episode . Morning stiffness s hould be re ma rka ble , instead of brief dis comfort. By ca reful history ta king a nd thorough phys ica l exa mination, the a uthor could find out quite eas ily that they had Be hcet a rthritis , afte r a ll poss ible rhe umatic diseas es had bee n excluded.
With full a nd careful inte rpretation of a ll clinica l ma nifestations , it may not be a proble m for a n expe rienced phys icia n to diffe rentiate RA with most of Be hcet dis ease . Howeve r, for those who do not understand the hete roge ne ity of rheumatic diseases , Be hcet dis ease may pos e a diagnostic dile mma, es pecially whe n it pres ents ve ry s imila r to RA with polya rticula r involve me nt on PIP, MCP of ha nds a nd with equivocal morning stiffnes s .
Be hcet dis ease was cha racte rized by attacks a nd re miss ions
1 6 ). It was known that the duration of attacks va ried from a few days to a few wee ks , a nd attacks were followed by re miss ions . J oint ma nifestations we re known us ua lly as non- e ros ive , eve n afte r exte nded pe riods of time . In the prese nt study, the duration of each attack was less than 4 wee ks in 76%, a nd this res ult was s imilar to the previous report
9 ). Knee , PIP, MCP, wrist a nd s houlde r we re commonly involved, a nd the a rthritic
manifestation was prese nt only for seve ra l days in more than ha lf of the patie nts . In this context, it see med feas ible to say that arthritic manifestations in Be hcet disease may pres ent as pa lindromic rhe umatis m
1 7 - 1 9 ). Pa lindromic rhe umatis m is characte rized by recurre nt acute e pisodes of a rthritis . The joints involved in initial attacks in pa lindromic rheumatis m a re mostly knee, wrist, MCP, P IP a nd s houlde r
1 8 ). Each e pisode of palindromic rheumatis m lasts , not infreque ntly, for a few wee ks
1 9 ), a nd there is no bone a nd ca rtilage destruction eve n afte r re peated e pis odes .
CRP was pos itive in a ll complete type a nd most of incomplete type . It was also pos itive in some of s us pected type who had ve ry active or adva nced manifestations , s uch as wides pread erythe ma nodos um- like s kin les ion, crippling a rthritis (Fig.1- 2), gastrointestina l ulce ration or vascula r ane urys m. It is likely that CRP may be pos itive in "active " Be hcet diseases .
In Korea , eve n afte r publication of about 150 pa pe rs
mentioned a bove , it see ms that Be hcet disease is still
rega rded as a ve ry ra re disease to prima ry ca re
phys icia ns a nd patients , a nd es pecially, the a rthritic
manifestations in Be hcet disease is us ua lly ove rlooked. It
is likely that many doctors do not completely understand
the complex nature of Be hcet diseas e, which includes the
various clinical s pectrum a nd clinica l evolution that was
mentioned a bove in deta il. It is s peculative that they
us ua lly unde rsta nd Be hcet disease as "strict" symptom
triad which is composed of ora l ulcer, ge nita l ulce r a nd
uve itis . Since they us ua lly think that a ll ma nifestations
F ig . 1. Twe nty- two- yea r old young ma n prese nted with crippling a rthritis at left knee joint with ma rkedly elevated CRP. He had a rthroscopy at a nothe r hospita l due to ma rked swe lling a nd it was unre ma rkable .s hould a ppea r at the sa me time , at prese ntation to the m, they will not diagnose a patient as Behcet dis ease if the patie nt has only one or two manifestations . Patie nts with oro- ge nita l ulce rs may not see k he lp s ince the clinica l ma nifestation is sometimes tole ra ble or re lieved by topica l age nts . Othe rwise , they may fee l uncomforta ble in vis iting a doctor's office with genita l proble ms which are not ve ry urge nt. Va rious s kin les ions , including e rythema nodos um- like e ruptions , s ubcuta neous thrombophle bitis a nd hype r- irrita bility of the s kin, ma nifest so dive rse a nd a re mostly s ubclinica l. From thes e contexts , arthralgia or a rthritis ca n be the first prese nting proble m in many Be hcet dis ease patie nts .
The prese nt study had a few limitations . The s ize of the sa mple was too s ma ll a nd the duration of follow- up was too s hort to discus s the e ntire clinica l progress ion.
Most patie nts we re the incomplete or s us pected type , instead of the complete type, s ince the a uthor focus ed on ea rly prese nting ma nifestations a nd ea rly detection. By the way, rece ntly, the re was a re port focus ing hee l pa in in Be hcet dis ease patie nts which s uggested that a rthropathy in Be hcet disease might be rega rded as a nothe r e ntity of se ronegative s pondyloarthropathy
2 0 ). In the prese nt study, hee l pa in was prese nt in one patient.
The prese nt study was focused only on a rticula r manifestations a nd future study, including the e nthesopathy, seems to be required.
C O NC L US IO N
In Be hcet disease , va rious ma nifestations ca n be found. The arthritic ma nifestation see ms quite common. It may prese nt as s eronegative rhe umatoid arthritis . Othe rwise , it may prese nt as pa lindromic rhe umatis m.
Much more atte ntion to this disease a nd a nationwide s urvey in Korea seem to be required for better unde rsta nding, ea rly detection a nd a ppropriate treatme nt.
R E F E R E NC E S
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