M a ria L u iz a S ilv a , L u c y M a s s a c o M iy a c h i, L ig ia M a ria Is h im u ra F u k u m o ri, S o ra ia R e g in a d a S ilv a
D irect im m unofluorescence in Lupus Erythem atosus (LE)
Study performed at the General Hospital Dermatology Clinic of the
University of Silo Paulo Medical School. Silo Paulo.
O n e h u n d re d a n d tw e n ty-six p a tie n ts w ith L E w e re stu d ie d . T h e y w e re d istrib u te d a s fo llo w s: 8 4 w ith O L E , 1 3 w ith S A L E a n d 2 9 w ith S L E . B io p sie s fro m th e skin le sio n s w e re p e rfo rm e d a n d su b m itte d to D IF . P o sitive re su lts w e re e q u a l to 6 9 ,6 1 .5 a n d 7 2 .4 p e rce n t o f th e O L E , S A L E a n d S L E ca se s, re sp e ctive ly. T h e se d a ta a re in a cco rd a n ce w ith th e lite ra tu re . Ig M w a s th e m o st fre q u e n tly fo u n d im m u n o g lo b u lin , fo llo w e d b y th e a sso cia tio n Ig M + C 3 .
U N IT E R M S : D ire ct im m u n o flu o re sce n ce (D IF ). L u p u s e ryth e m a to su s (L E ). D isco id lu p u s e ryth e m a to su s (O L E ). S u b a cu te lu p u s e ryth e m a to su s (S A L E ). S yste m ic lu p u s e ryth e m a to su s (S L E ). Im m u n o g lo b u lin s (Ig s).
IN T R O D U C T IO N
I
detectedm m unoglobulin (lg ) and com plem entby the direct im m unofluorescence(C 3) deposits,technique (D IF ) at the derm oepiderm al junction of skin lesionsfrom patients w ith lupus erythem atosus (L E ), w ere first
described by B U R H A M et al. in 1963.4 L ater,
C O R M A N E 5 dem onstrated that such deposits also
occurred in clinically-norm al skin of patients w ith system ic
lupus erythem atosus (S L E ), but w ere not found in norm al
skin of patients w ith discoid lupus erythem atosus (D L E ).
S ince then, a num ber of studies have been undertaken
w hich lead to the conclusion that im m unoglobulin deposits
in the skin in the basal m em brane zone (B M Z ) are
A d d re s s fo r c o rre s p o n d e n c e : R o s e li S v a rtm a n Is fe r
R u a D ia n a , 1 0 3 9 - a p to . 1 2 3 - V ila P o m p e ia S a o P a u lo /S P - B ra s il- C E P 0 5 0 1 9 -0 0 0
characteristic of L E , thus having diagnostic, and possibly,
prognostic value.
T he present study evaluates the incidence of positi ve
D IF in skin lesions of patients .w ith discoid lupus
erythem atosus (D L E ), subacute lupus erythem atosus
(S A L E ) and system ic lupus erythem atosus (S L E ), as w ell
as the incidence of different im m unoglobulins (Igs) and
of com plem ent (C 3).
M A T E R IA L A N D M E T H O D S
O ne hundred and tw enty-six patients w ith L E , treated
at the G eneral H ospital D erm atology C linic of the
U niversity of S ao P aulo M edical S chool betw een 1990
and 1992, w ere retrospectively studied. T he patients w ere
distributed as follow s: 84 w ith D L E , 13 w ith S A L E and
29 w ith S L E . T he classification of the patients into these
subgroups w as based on clinical, histopathologic and
IS F E R , R S .; S A N C H E S Jr., J.A .; F E S T A N E T O , C . e t a l. - D ire ct im m u n o flu o re sce n ce in L u p u s E ryth e m a to su s (L E )
D I S C O I D L U P U S E R Y T H E M A T O U S
S E X D I S T R I B U T I O N
S Y S T E M I C L U P U S E R Y T H E M A T O U S
S E X D I S T R I B U T I O N
F e m a le , 6 0 7 1 %
M a le , 2 4 2 9 %
F e m a le , 2 6 9 0 %
M a le , 3
1 0 %
F ig u r e 1 - D is c o id L u p u s E r y t h e m a t o s u s - S e x d is t r ib u t io n .
s e ro lo g ic d a ta . T h e p a tie n ts w ith S L E fu lfille d a t le a s t fo u r
o f th e A m e ric a n R h e u m a tis m A s s o c ia tio n (A R A ) c rite ria . IS
T h e th re e s tu d y g ro u p s w e re p re d o m in a n tly fe m a le ,
w ith d iffe re n t re la tiv e fre q u e n c ie s w ith in e a c h g ro u p (F ig s .
1 , 2 a n d 3 ). T h e p a tie n t's a g e s ra n g e d fro m 6 to 7 9 y e a rs
w ith a m a jo rity in th e ir 3 0 's (F ig s . 4 , 5 a n d 6 ).
P u n c h b io p s ie s o f s k in le s io n s w e re p e rfo rm e d o n
th e 1 2 6 p a tie n ts . T h e tis s u e fra g m e n ts w e re
im m e d ia te ly fro z e n , c u t in to 5 m m -th ic k s e c tio n s a n d
in c u b a te d w ith flu o re s c e in -la b e le d a n tib o d ie s in a m o is t
c h a m b e r a t ro o m te m p e ra tu re fo r. 3 0 m in u te s . T h e
s e c tio n s w e re th e n w a s h e d tw ic e (fo r 1 0 m in u te s ) w ith
T B S (p H 7 .5 ), a n d c o v e re d w ith p h o s p h a te -b u ffe re d
g ly c e rin e (p H 9 .0 ). T h e s p e c im e n s w e re e x a m in e d w ith
a Z e is s e p iflu o re s c e n c e -e q u ip p e d m ic ro s c o p e .
S U B A C U T E L U P U S E R Y T H E M A T O U S
S E X D I S T R I B U T I O N
F ig u r e 3 - S y s t e m ic L u p u s E r y t h e m a t o s u s - S e x d is t r ib u t io n .
R E S U L T S
P o s itiv e D IF re s u lts in s k in le s io n s w e re d e te c te d
in 5 8 o f 8 4 p a tie n ts (6 9 p e rc e n t) w ith D L E , 8 o f 1 3
(6 1 .5 p e rc e n t) p a tie n ts w ith S A L E , a n d 2 1 o f 2 9 (7 2 .4
p e rc e n t) p a tie n ts w ith S L E . Im m u n o g lo b u lin s w e re
fo u n d is o la te d o r a s s o c ia te d a n d w ith c o m p le m e n t in
th e B M Z a n d a ls o in th e b lo o d v e s s e ls , a n d in th e fo rm
o f c y to id b o d ie s , a s s h o w n in T a b le s 1 -6 .
A m o n g th e D L E le s io n s w ith p o s itiv e D IF , w e
v e rifie d th e p re s e n c e o f Ig G a n d /o r c o m p le m e n t in th e
B M Z in 5 6 (9 6 .5 p e rc e n t) p a tie n ts . O f th e s e , in 4 6 c a s e s
(7 9 .3 p e rc e n t), D IF w a s p o s itiv e in th e B M Z o n ly , in 4
(6 .9 p e rc e n t), th e d e p o s it'w a s a ls o p re s e n t in th e b lo o d
D I S C O I D L U P U S E R Y T H E M A T O U S
A G E D I S T R I B U T I O N
2 5
2 0 .
o 5 1 0 1 5 2 0 2 5 3 0 3 5 4 0 4 5 5 0 5 5 6 0 6 5 7 0 7 5 8 0
A g e
F e m a le , 1 3 1 0 0 %
lJ ) Q ) lJ )
ro
( ) 1 5 .
-
oCD .c 1 0
E
::::l
Z
5 .
o
F ig u r e 2 - S u b a c u t e L u p u s E r y t h e m a t o s u s
-S e x d is t r ib u t io n . F ig u r e 4 - D is c o id L u p u s E r y t h e m a t o s u s - A g e d is t r ib u t io n .
T a b le 1
IG a n d C 3 in s k in le s io n s o f 5 8 p a tie n ts w ith O L E a n d P o s itiv e O IF in th e v e s s e ls a n d c y to id b o d ie s
C la sse s Iso la te d V e sse ls in T o ta l Iso la te d C yto id b o d ie s T o ta l ve sse ls B M Z a sso c. cyto id b o d ie s B M Z a sso c.
Ig M 0 3 3 0 4 4
Ig M + Ig A 0 0 0 1 1 2
Ig M + C 3 0 0 0 1 1 2
C 3 0 1 1 0 0 0
T o ta l 0 4 (6 .9 % ) 4 (6 .9 % ) 2 (3 .4 5 % ) 6 (1 0 .3 % ) 8 (1 3 .8 % )
v essels, an d in 6 (1 0 .3 p ercen t), in th e cy to id b o d ies. In
2 p atien ts (3 .4 p ercen t), D IF w as p o sitiv e o n ly in th e
cy to id b o d ies.
T h e d istrib u tio n o f th e d ifferen t Ig s an d o f C 3 is
sh o w n in T ab les 1 an d 4 . In th e B M Z , Ig M w as th e m o st
co m m o n Ig , fo llo w ed b y th e asso ciatio n Ig M + C 3 an d
Ig M + Ig G + Ig A + C 3 . C 3 w as fo u n d iso lated in th e B M Z in
3 (5 .2 p ercen t) o f th e p atien ts (T ab le 4 ). T h e m o st
co m m o n ly fo u n d Ig in th e b lo o d v essels an d cy to id b o d ies
w as also Ig M (T ab le I).
In th e 8 S A L E p atien ts w ith p o sitiv e D IF , th e B M Z
w as flu o rescen t, in 2 cases th e v essels w ere also
flu o rescen t, an d in 1 p atien t th ere w as flu o rescen ce in th e
cy to id b o d ies (T ab le 2 ). R eg ard in g th e d istrib u tio n o f Ig s
in th e B M Z (T ab le 5 ), th ere w as p red o m in an ce o f Ig M + C 3 .
Ig M w as fo u n d iso lated in o n ly 1 case.
O f th e 2 1 p atien ts w ith S L E an d p o sitiv e D IF ,
1 8 (8 5 .7 p ercen t) sh o w ed d ep o sits in th e B M Z , 2
w ere also p o sitiv e in th e b lo o d v essels, an d 3 in th e
cy to id b o d ies. Iso lated flu o rescen ce in th e v essels
w as fo u n d in 2 cases (9 .5 p ercen t), an d in th e cy to id
b o d ies in 1 p atien t (4 .8 p ercen t) (T ab le 3 ). T h e Ig s'
d istrib u tio n in th e B M Z (T ab le 6 ) rev ealed
p red o m in an ce o f Ig M fo llo w ed b y Ig M + C 3 an d
Ig G + Ig M + Ig A + C 3 . In o n e case, C 3 w as fo u n d
iso lated in th e B M Z . T h e p resen ce o f Ig M + C 3 in th e
v essels w as o b serv ed in o n e p atien t, an d iso lated
C 3 in an o th er, w h ere as in th e cy to id b o d ies,
Ig M + Ig G w ere fo u n d iso lated in o n ly o n e case.
S U B A C U T E L U P U S E R Y T H E M A T O U S
A G E D IS T R IB U T IO N
5
4
IJl Q ) IJl
co
() 3 .•...
o Q;
E
2:J
Z
o
o 5 1 0 1 5 2 0 2 5 3 0 3 5 4 0 4 5 5 0 5 5 6 0 6 5 7 0 7 5 8 0
A g e 1 3 C a se s
F ig u re 5 - S u b a cu te L u p u s E ryth e m a to su s - A g e d istrib u tio n .
T a b le 2
IG a n d C 3 in s k in le s io n s o f 8 p a tie n ts w ith S a le a n d P o s itiv e O IF in th e v e s s e ls a n d c y to id b o d ie s
C la sse s Iso la te d V e sse ls in Iso la te d C yto id b o d ie s
ve sse ls B M Z a sso c. cyto id b o d ie s B M Z a sso c.
Ig M 0 1 0 4
Ig M + C 3 0 1
T o ta l 0 2 (2 5 % ) 0 1 (1 2 .5 % )
IS F E A , A .S .; S A N C H E S Jr., J.A .; F E S T A N E T O . C . e t a l. - D ire ct im m u n o flu o re sce n ce in L u p u s E ryth e m a to su s (L E )
T a b le 3
IG a n d C 3 in s k in le s io n s o f 2 1 p a tie n ts w ith S L E a n d P o s itiv e O IF in th e v e s s e ls a n d c y to id b o d ie s
C la s s Is o la te d V e s s e ls in T o ta l Is o la te d C y to id b o d ie s T o ta l
v e s s e ls B M Z a s s o c . c y to id b o d ie s B M Z a s s o c .
Ig M 3 3
Ig M + Ig A 1 1
Ig M + C 3 1 1
C 3 1 1 2
Ig M + lg M + C 3 1 1
T o ta l 0 2 (9 .5 % ) 0 2 (9 .5 % ) 4 (1 9 % ) 0 1 (4 .0 % ) 0 3 (1 9 .3 % ) 4 (1 9 .1 % )
T a b le 4
IG a n d C 3 in s k in le s io n s o f 5 8 p a tie n ts w ith O L E a n d P o s itiv e O IF
C la s s e s B M Z V e s s e ls C y to id b o d ie s
Ig G 3 (1 )* 0 0
Ig G + C 3 1 0 0
Ig G + Ig M 3 0 0
Ig G + Ig A 1 ** 0 0
Ig G + Ig M + C 3 6 0 0
Ig G + Ig A + C 3 1 0 0
Ig G + lg M + lg A + C 3 7 (1 )# # 0 0
Ig M 1 7 (3 )* 0 0
Ig M + C 3 7 (2 )***
(1 )# 0 0
Ig M + Ig A 0 0 1
Ig M + Ig A + C 3 4 (1)@ 0 0
Ig A 2 0 0
Ig A + C 3 1 0 1
C 3 3 0 0
5 6 (9 6 .5 % ) 0 2 (3 .5 % )
* Ig M flu o re s c e n c e in c y to id b o d ie s
Ig M a n d Ig A flu o re s c e n c e in c y to id b o d ie s Ig M a n d C 3 flu o re s c e n c e in c y to id b o d ie s # Ig M flu o re s c e n c e in th e v e s s e ls
# # C 3 flu o re s c e n c e in th e v e s s e ls
@ Ig M flu o re s c e n c e in c y o tid b o d ie s a n d v e s s e ls
D IS C U S S IO N
In a s tu d y p e rfo rm e d b y T U F F A N E L L I in 1 9 7 5 ,
D IF w a s p o s itiv e in 9 4 p e rc e n t o f D L E c a s e s .17 T h e
re s u lts o f th e p re s e n t s tu d y (6 9 p e rc e n t) a g re e w ith m o re
re c e n t s tu d ie s s u c h , a s th o s e o f P R O E N c ;A e t a !.,III in
w h ic h D IF w a s p o s itiv e in th e s k in le s io n s o f 5 8 .3 3
p e rc e n t o f th e p a tie n ts w ith D L E , a n d o f B L A S Z C Z Y K
a n d D A H L ,3 in w h ic h th e p o s itiv e re s u lts re a c h e d 7 9
p e rc e n t. A s tu d y p e rfo rm e d b y S U G A I e t a !. a t o llr c lin ic
re v e a le d p o s itiv e re s u lts in 6 6 .2 p e rc e n t o f th e s e c a s e s .14
S e v e ra l fa c to rs m a y a ffe c t th e p o s itiv e re s u lt o f
D IF , s u c h a s th e d u ra tio n o f th e le s io n s , th e ir
S Y S T E M IC L U P U S E R Y T H E M A T O U S
A G E D IS T R IB U T IO N
1 0
B .
en
Q )
en
ctI
() 6 .•...
o
Q>
.c 4
E ::J Z
2 .
o
o 5 1 0 1 5 2 0 2 5 3 0 3 5 4 0 4 5 5 0 5 5 6 0 6 5 7 0 A g e
2 9 C a s e s
F ig u re 6 - S y s te m ic L u p u s E ry th e m a to s u s - A g e d is trib u tio n .
(annular or
papulosqua-m ous), w hich is im portant as,
according to the sam e author,
lesions of the
papulos-quam ous type present Ig
deposits at the derm
oepi-derm al junction m ore
frequently. R ecently, a new
D IF pattern in SA L E , called
"dust-like particles", w as
described by N IE B O E R et al.
and considered highly
specific but had low
sensitivityY T his pattern w as
not taken into account in the
present study.
In SL E skin lesions, the
positive results of D IF reported
in the literature varied from 50
percentll to 93 percent. 17 T hus,
our result of 72.4 percent agrees
w ith the previous data.
In a study perform ed by
A H M E D and PR O V O ST in
1979, I w ho analyzed D IF
results in norm al exposed and
unexposed skin of patients w ith
SL E , positive results reached
77 and 37 percent, respectively.
W e believe that the higher
positive results observed by us
m ay be due to the fact that
biopsies w ere alw ays
perform ed on exposed skin.
T he positive D IF in the
three study groups w as alm ost
alw ays observed in the B M Z .
Isolated fluorescence in the
blood vessels occurred in 9.5
percent of the SL E cases, and
did not occur in the D L E and
SA L E patients.
T hese findings confirm the literature data,
w hich states that Ig deposits in the vessels are
m ore frequently observed in SL E . N evertheless, our
frequency of positive results is low er than the one
described in the literature, w hich varied from 30
to 95 percent6 w hen clinically norm al skin w as
considered. T hese differences m ay be related to the
fact that D IF w as only considered positive w hen the
vessel w all w as w ell-defined. B esides, as w e
Table 5
IG and C3 in skin lesions of 8 patients
with Sale and Positive DIF
Table 6
IG and C3 in skin lesions of 21 patients
with SLE and Positive DIF
* Ig M flu o re s c e n c e in c y to id b o d ie s Ig M a n d C 3 in th e v e s s e ls Ig M flu o re s c e n c e in th e v e s s e ls
* Ig M flu o re s c e n c e in c y to id b o d ie s
Ig G , Ig M a n d C 3 flu o re s c e n c e in th e v e s s e ls C 3 flu o re s c e n c e in th e v e s s e ls
C la s s B M Z V e s s e ls C y to id b o d ie s
Ig G + Ig M 2 2
Ig G + Ig M + C 3 2 *(1 ) 2
Ig M 1 1
Ig M + C 3 3 **(1 ) 3
***(1 )
8 (1 0 0 % ) 8 (1 0 0 % )
C la s s B M Z V e s s e ls C y to id
Ig G 1 1
Ig G + C 3 1 1
Ig G + Ig M 2 (1 )* 1 3
Ig G + Ig M + Ig A 1 1
Ig G + lg M + lg A + C 3 3 (1 )**
(1 ) *** 3
Ig M 4 4
Ig M + C 3 3 (1 )* 1 4
Ig M + Ig A + C 3 1 1
Ig M + Ig A 1 (1 )* 1
C 3 1 1 2
1 8 (8 5 .7 % ) 2 (9 .5 % ) 1 (4 .8 % ) 2 1 (1 0 0 % )
distribution (exposed or unexposed area) and previous
treatm ent. 3 In the present study, the biopsies w ere
alw ays taken from exposed skin lesions. N evertheless,
the duration of the lesions and the prebiopsy treatm ent
period could not be analyzed.
SA L E lesions w ere D IF positive in 61.5 percent
of the cases, w hich coincides w ith the 60 percent found by SO N T H E IM E R et al.1 3 It w as not possible to classify
the patients according to the aspect of the lesions
p e rfo rm e d a re tro sp e c tiv e stu d y , it w a s n o t p o ssib le
to d e te rm in e h o w m a n y p a tie n ts w e re a lre a d y u n d e r
tre a tm e n t a t th e tim e o f b io p sy .
T h e iso la te d flu o re sc e n c e o f th e c y to id b o d ie s w a s
n o t fre q u e n t: 3 .4 p e rc e n t in D L E , 0 p e rc e n t in S A L E a n d
4 .8 p e rc e n t in S L E . It se e m s to p re se n t lo w sp e c ific ity ,
a n d m a y o c c u r in th e p h o to d a m a g e d sk in a n d , th u s, h a v e
a n o n -im m u n o lo g ic a l o rig in .'9
T h e m o st fre q u e n tly fo u n d Ig in th e B M Z , a lo n e o r
in a sso c ia tio n w ith o th e r Ig s a n d /o r C 3 , w a s Ig M , in th e
th re e stu d y g ro u p s. In S A L E , Ig M w a s fo u n d in 1 0 0
p e rc e n t o f th e c a se s.
A c c o rd in g to p re v io u s re se a rc h , th e re is
p re d o m in a n c e o fIg M o r Ig O . T U F F A N E L L I, in a stu d y
o f 9 7 1 c a se s, fo u n d a p re d o m in a n c e o f Ig O ,1 8 w h ile
o th e r a u th o rs, stu d y in g sm a lle r sa m p le s, fo u n d a
p re d o m in a n c e o f Ig M .7 .8 .1 6 .1 9A c c o rd in g to H A R R IS T
a n d M IH M , it se e m s p ro p e r to c o n c lu d e , in v ie w o f th e
sm a ll n u m b e r o f p a tie n ts in th e stu d ie s in v o lv in g a
p re d o m in a n c e o f Ig M , th a t th e p re se n c e o f Ig M a lo n e
is u n c o m m o n .6 M a n y a u th o rs a g re e th a t Ig M is m o re
se n sitiv e , w h ile Ig O is m o re sp e c ific ?
C 3 w a s g e n e ra lly fo u n d in a sso c ia tio n w ith th e se
Ig s, a n d se ld o m iso la te d . In th e lite ra tu re , th e p re se n c e
o f C 3 is c o n sid e re d su g g e stiv e o f th e c la ssic p a th w a y
a c tiv a tio n o f th e c o m p le m e n t.7
T h e m o st fre q u e n tly re p o rte d a sso c ia tio n is
Ig O + Ig M ,3 . I{ a n a sso c ia tio n n o t v e rifie d in th e p re se n t
stu d y , w h e re a s th e Ig M + C 3 a sso c ia tio n w a s m o re
fre q u e n t. In a stu d y p e rfo rm e d b y R A T N A M e t a l. in
S in g a p o re ,1 2 C lq w a s th e m o st fre q u e n tly fo u n d
im m u n o re a c ta n t, fo llo w e d b y Ig M .
C O N C L U S IO N
D IF h a s a v e ry im p o rta n t ro le in L E d ia g n o sis.
T h e re su lts o f th e p re se n t stu d y sh o w th a t, a lth o u g h
th e re a re se v e ra l v a ria b le s o f a ra c ia l, c lim a tic a n d
te c h n ic a l o rd e r, it w a s p o ssib le to re p ro d u c e th e
fre q u e n c ie s o f p o sitiv e re su lts re p o rte d in th e
in te rn a tio n a l lite ra tu re .
It is im p o rta n t to stre ss th a t D IF , a s a n y la b o ra to ry
p ro c e d u re , h a s lim ita tio n s a n d m u st a lw a y s b e
c o n sid e re d to g e th e r w ith c lin ic a l, se ro lo g ic a n c l
h isto p a th o lo g ic a l d a ta .
RESUMO
F o ra m e s tu d a d o s c e n to e v in te e s e is p a c ie n te s c o m L E , d is trib u fd o s d a s e g u in te fo rm a : 8 4 c o m L E D , 1 3 c o m L E S A e 2 9 c o m L E S . F o ra m re a liz a d a s b io p s ia s n a p e le le s a d a , q u e fo ra m s u b m e tid a s a IF D . H o u v e p o s itiv id a d e d e 6 9 % p a ra 0 L E D , 6 1 ,5 % p a ra 0 L E S A e 7 2 ,4 % p a ra 0 L E S , d a d o s e s te s q u e e s ta o d e a c o rd o c o m a lite ra tu ra . Ig M fo i a Ig m a is fre q u e n te m e n te e n c o n tra d a , s e g u id a d a a s s o c ia c ;:a o Ig M + C 3 .
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IS F E R , R .S .; S A N C H E S J r., J .A .; F E S T A N E T O , C . e t a l. - D ire c t im m u n o flu o re s c e n c e in L u p u s E ry th e m a to s u s (L E )
