AN ELECTROPHYSIOLOGICAL INVESTIGATION OF
SKELETAL MUSCLES IN POLYMYOSITIS
R . E . P . S I C A O L G A P . S A N Z * N I D I A A G U I L E R A A . C O L O M B I
T h e a i m of the present investigation is to report the results of a detailed electrophysiological examination of muscle a n d motor nerve functions in patients w i t h polymyositis.
T h e present study has involved mainly the quantification of operative motor units within the extensor digitorum brevis ( E . D . B . ) , thenar and hypo thenar muscles.
M A T E R I A L A N D M E T H O D S
A l t o g e t h e r 25 p a t i e n t s w e r e s t u d i e d , t h e y w e r e a g e d 17 t o 59 y e a r s a n d , o n c l i n i c a l , l a b o r a t o r y a n d h i s t o p a t h o l o g i c a l g r o u n d s , w e r e j u d g e d t o h a v e p o l y m y o -s i t i -s ( T y p e a l p h a , W o r l d F e d e r a t i o n o f N e u r o l o g y R e -s e a r c h G r o u p o n N e u r o m u -s c u l a r D i s o r d e r s , 1 9 6 8 ) .
T h e p a t i e n t s w e r e d i v i d e d i n t o t w o g r o u p s : t h e f i r s t g r o u p o f 21 p a t i e n t s c o m -p r i s e d t h o s e s u f f e r i n g f r o m -p r i m a r y , c h r o n i c -p o l y m y o s i t i s ; t h e r e m a i n i n g 4 -p a t i e n t s w i t h a c u t e p o l y m y o s i t i s m a d e u p a s e c o n d g r o u p . 125 h e a l t h y s u b j e c t s a g e d 16 t o 59 y e a r s s e r v e d a s c o n t r o l s f o r o n e o r m o r e i n v e s t i g a t i o n s .
T h e n u m b e r o f m o t o r u n i t s i n t h e E . D . B . m u s c l e w a s e s t i m a t e d b y t h e m e t h o d o f M c C o m a s , F a w c e t t , C a m p b e l l a n d S i c a w h i l e t h e n u m b e r o f o p e r a t i v e m o t o r u n i t s w i t h i n t h e t h e n a r a n d h y p o t h e n a r m u s c l e s w a s o b t a i n e d b y t h e t e c h n i q u e d e s c r i b e d b y S i c a , M c C o m a s , U p t o n a n d L o n g m i r e » .
M e a s u r e m e n t s w e r e m a d e o f i m p u l s e c o n d u c t i o n v e l o c i t i e s a n d t e r m i n a l l a t e n -c i e s in m o t o r n e r v e f i b r e s f o l l o w i n g a -c o n v e n -c t i o n a l t e -c h n i q u e .
I n a l l t h e p a t i e n t s c o n c e n t r i c n e e d l e e l e c t r o m y o g r a p h y w a s p e r f o r m e d ; t h e s e s t u d i e s o f t e n s e r v e d t o c l a r i f y t h e d i a g n o s i s b u t t h e r e s u l t s w i l l n o t b e r e p o r t e d .
T h r o u g h o u t t h e t e x t m e a n v a l u e s h a v e b e e n g i v e n w i t h t h e i r s t a n d a r d d e -v i a t i o n s . T h e s i g n i f i c a n c e o f d i f f e r e n c e b e t w e e n m e a n s w a s c a l c u l a t d e b y t h e " t " t e s t .
R E S U L T S
Numbers of motor units — T a b l e I s h o w s t h e i n d i v i d u a l v a l u e s o f o p e r a t i v e m o t o r u n i t s in e a c h o f t h e m u s c l e s i n v e s t i g a t e d in b o t h g r o u p s o f p a t i e n t s .
T a b l e 1 s h o w s t o o t h a t t h e loss o f u n i t s w a s a l r e a d y e v i d e n t in s o m e m u s c l e s s h o r t l y a f t e r t h e s t a r t i n g o f t h e d i s e a s e . H o w e v e r t h e r e w a s a l i g h t c o r r e l a t i o n b e t w e e n t h e loss o f f u n c t i o n i n g m o t o r u n i t s a n d t h e l e n g t h o f h i s t o r y , b e i n g t h i s b e h a v i o u r m o r e e v i d e n t in t h e E . D . B . m u s c l e a n d less c o n s i s t e n t in t h e h y p o t h e n a r m u s c l e s ( r f o r E . D . B . : - 0 . 5 2 , P < 0 . 0 2 ; f o r t h e n a r : - 0 . 3 9 , P < 0 . 1 ; f o r h y p o t h e n a r : - 0 . 3 8 , P > 0 . 1 ) .
I n t h e second g r o u p o f p a t i e n t s w h o w e r e a f f e c t e d by a c u t e p o l y m y o s i t i s o n l y o n e o f t h e m , w h o w a s t h e o n e w i t h t h e l o n g e s t h i s t o r y o f disease, s h o w e d a d i m i n i s h e d n u m b e r o f m o t o r units in t h e E . D . B . a n d t h e n a r m u s c l e s .
Sizes of the remaining motor units — I n f i g u r e 1 t h e m e a s u r e m e n t s o f m o t o r u n i t p o t e n t i a l a m p l i t u d e s h a v e b e e n p o o l e d f o r a l l t h e p a t i e n t s a f f e c t e d b y c h r o n i c a n d a c u t e p o l y m y o s i t i s in s e p a r a t e d p i c t u r e s , i r r e s p e c t i v e o f t h e d u r a t i o n o f t h e d i s e a s e o r t h e n u m b e r o f s u r v i v i n g u n i t s .
I t c a n be seen t h a t t h e v a l u e s d e r i v e d f r o m m u s c l e s in p a t i e n t s a f f e c t e d b y c h r o n i c p o l y m y o s i t i s t e n d to be s m a l l e r t h a n t h e c o n t r o l s d e s p i t e t h a t t h e m o d e in E . D . B . and h y p o t h e n a r m u s c l e s c o i n c i d e s w i t h t h e n o r m a l s ; in a c u t e p o l y m y o s i t i s t h e r e is a d e f i n i t e t e n d e n c y f o r t h e r e s u l t s t o be s m a l l e r .
w a s n o t n o t e d in t h e h y p o t h e n a r m u s c l e s ( r f o r h y p o t h e n a r : 0 . 1 0 ) . H o w e v e r w h e n t h e n u m b e r s o f t h e r e m a i n i n g u n i t s w e r e c o m p a r e d w i t h t h e i r m e a n s i z e s t h e t h r e e m u s c l e s i n v e s t i g a t e d b e h a v e d i n a s i m i l a r w a y ( r f o r E . D . B . : - 0 . 5 2 , P < 0 . 0 2 ; f o r t h e n a r : - 0 . 5 6 , P < 0 . 0 1 ; f o r h y p o t h e n a r : - 0 . 6 3 , P < 0 . 0 1 ) s h o w i n g t h a t t h e s t i l l s u r v i v i n g u n i t s t r y t o c o m p e n s a t e t h e loss o f o p e r a t i v e m o t o r units b y i n c r e a s i n g t h e i r t e r r i t o r i e s ( f i g u r e 2 ) .
Motor conduction velocities and terminal latencies — I n a l l t h e p a t i e n t s t h e m a x i m u m c o n d u c t i o n v e l o c i t i e s o f i m p u l s e s i n m o t o r n e r v e f i b r e s o f t h e d e e p p e r o -neal, m e d i a n and u l n a r n e r v e s w e r e w i t h i n t h e n o r m a l r a n g e f o r t h i s l a b o r a t o r y ( d e e p p e r o n e a l : 40-60 m / s ; m e d i a n : 50-71 m / s ; u l n a r : 51-72 m / s ) .
A c o m p a r i s o n w a s a l s o m a d e o f t h e t e r m i n a l l a t e n c i e s in t h e c o n t r o l a n d 111 p o p u l a t i o n s , t h i s l a t e n c y b e i n g m e a s u r e d as t h e t i m e e l a p s i n g b e t w e e n t h e s t i m u l a t i o n o f t h e m o s t d i s t a l p o i n t o f t h e n e r v e ( a n k l e f o r t h e d e e p p e r o n e a l a n d w r i s t f o r m e d i a n a n d u l n a r ) a n d t h e o n s e t o f p o s t - s y n a p t i c a c t i v i t y in t h e c o n c e r n e d m u s c l e . I n c h r o n i c p o l y m y o s i t i s s o m e o f t h e p a t i e n t s s h o w e d l a t e n c i e s l o n g e r t h a n t h e c o n t r o l p o p u l a t i o n ( t a b l e 1 ) ; i n d e e d t h e d i f f e r e n c e s b e t w e e n t h e n o r m a l a n d p a t i e n t s m e a n s w e r e s i g n i f i c a n t f o r t h e t h r e e n e r v e s i n v e s t i g a t e d ( d e e p p e r o n e a l : p a t i e n t s 4 . 7 7 ± 0 . 8 0 ms, c o n t r o l s 4 . 2 3 ± 0 . 5 7 , P < 0 . 0 1 ; m e d i a n : p a t i e n t s 3 . 5 3 ± 0 . 7 9 ms, c o n t r o l s 2 . 9 5 ± 0 . 5 6 , P < 0 . 0 1 ; u l n a r : p a t i e n t s 3 . 0 3 ± 0 . 6 8 ms, c o n t r o l s 2 . 5 6 + 0.47, P < 0 . 0 1 ) . T h e s a m e s o r t o f b e h a v i o u r c o u l d be seen in a c u t e p o l y m y o s i t i s , but t h e s m a l l s a m p l e s d i d n o t a l l o w a s t a t i s t i c a l e v a l u a t i o n .
D I S C U S S I O N
T h e loss of operative motor units which w a s noted in chronic
poly-myositis and also in one of the four patients with acute polypoly-myositis m a y
have different explanations; one of them would be the involvement of the
peripheral nervous system in the disease as the main cause, if this would
be so, one would expect that, as happens with other forms of dennervation,
the remaining healthy units will enlarge their muscle fiber territories
8.
This behaviour w a s noted in chronic polymyositis when the correlation between
number of surviving units and their mean sizes w a s analyzed, in thenar and
E . D . B . muscles that enlargement w a s lightly related with the lengtn of
history. H o w e v e r looking at figure 1 it can be seen that the sizes of the
remaining units are within the distribution of the control population tending
to bunch up on the left side of the picture. This behaviour is quite different
to the one which can be expected if healthy, undamaged units would take
over the muscle fibers relinquished by its original innervation. Therefore
the explanation which can be given so f a r is that the disease affects at the
same time the muscle fibers and their motor innervation.
sizes similar to the normal units; in this last condition the fact that there
is an attempt of the remaining units to increase their sizes when the total
number of operative units shows a tendency to be reduced suggests that,
somehow, the peripheral nervous system is involved.
B a u w e n s
2in 1949 described a syndrome compound by signs of
neuropa-thic and myopaneuropa-thic degeneration believing that it resulted from a lesion of
the motor axon distal to its point of branching; Guy, Lefebvre, Lerique and
S c h e r r e r
5in 1950 demonstrated the same sort of features in dermatomyositis
which lately w a s attributed by B a u w e n s
1to a degeneration of the distal
portion of the axonal branches; Coers and W o o l f
3in 1959 demonstrated the
swelling of subterminal nerve fibres and end-plates as well as the axonal
sprouting and collateral reinnervation of muscle fibers in polymyositis, these
changes in motor innervation apparently involved the most distal part of
the nerve fibres. Recently Engel, Jerusalem, Tsujihata and G o m e z
4demons-trated the presence of degenerating nerve terminals in polymyositis and
morphometric abnormalities consisting in an increased mitochondrial content
and decreased synaptic vesicle density in the nerve terminal supporting the
assumption that intramuscular nerves may be affected in this disease. These
findings lead to the interpretation that in polymyositis there is a combination
of primary and secondary involvement of muscle fibers.
In keeping with this concept, in chronic polymyositis a motor unit could
be losing muscle fibers by primary involvement of them or by damage o f
some of its terminal axonal branches and simultaneously acquiring muscle
fibers by adopting those which have been denervated by the already mentioned
axonal damage. This would result in a sort of equilibrium where a motor
unit could mantain a size similar to the controls. Of course, one cannot
reject the possibility that in acute polymyositis the motor innervation would
have been damaged as well as in chronic polymyositis, but probably the
severe muscle involvement which occurs in this condition maskes any
electro-physiological manifestation of the peripheral nervous system participation
with the technical approach employed in the present study, except the
pro-longed terminal latencies in motor fibres.
T h e above reasons lead to the conclusion that in polymyositis w h o l e
motor units can be lost by t w o individual mechanisms or, more probably,
a combination of both; the first one would be a primary muscle involvement
which might "kill" individual muscle fibers up to the disappearance of the
whole unit and the second would be the axonal degeneration.
T h e axonal damage can explain too the prolonged terminal latencies
seen in these patients, not only by the damage itself but by the branches
sprouted from an undamaged axon which have diminished conduction velocity
6.
S U M M A R Y
polymyositis. I t w a s found a reduction of the n u m b e r of functioning motor units in some patients w i t h chronic polymyositis and only in one of those affected b y acute polymyositis. T h e sizes of the surviving units suggested that the results could be explained in terms of a primary muscle involvement mainly in acute polymyositis, while in chronic polymyositis a combination of primary and neurogenic involvement of muscle fibers might take place.
R E S U M O
Investigação eletrofisiológica de músculos esqueléticos na polimíosite
Foi feito estudo eletromiográfico do curto extensor dos dedos e dos músculos tenares e hipotenares em 25 pacientes com polimíosite crônica e a g u d a . Foi encontrada diminuição no número de unidades motoras funcio¬ nantes e m alguns pacientes com polimíosite crônica e somente em u m caso de polimíosite aguda. Os tamanhos das unidades restantes sugerem que os resultados podem ser explicados em termos de u m envolvimento primário dos músculos especialmente na polimiosite aguda, ao passo que na polimiosite crônica ocorre uma combinação de acometimento primário e neurogênico.
R E F E R E N C E S
1. B A U W E N S , P . — E l e c t r o d i a g n o s i s i n m o t o r u n i t d y s f u n c t i o n . P r o c . R . S o c . M e d . 48:194, 1955.
2 . B A U W E N S , P . 1949 — Q u o t e d b y C O É R S & W O O L F , 1959.
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n e u r o m u s c u l a r j u n c t i o n in m y o p a t h i e s . A q u a n t i t a t i v e u l t r a s t r u c t u r a l s t u d y . I n " R e c e n t A d v a n c e s in M y o l o g y " . E d . W . B r a d l e y , D . G a r d n e r - M e d w i n & J . N . W a l t o n . A m s t e r d a m , 1 9 7 5 . p p . 132-143.
5 . G U Y , E . ; L E F È B V R E , J . ; L È R I Q U E , J . & S C H E R R E R , J . — L e s s i g n e s e l e c t r o ¬ m y o g r a p h i q u e s d e s d e r m a t o m y o s i t i s . R e v . N e u r o l . ( P a r i s ) 83:278, 1 9 5 0 .
6 . L U D I N , H . P . — P a t h o p h y s i o l o g i s c h e G r u n d l a g e n E l e k t r o m y o g r a p h i s c h e r Be¬ funde b e i N e u r o p a t h i e n u n d M y o p a t h i e n . G e o r g T h i e m e V e r l a r g , S t u t t g a r t , 1975. p p . 61-62.
7 . M c C O M A S , A . J . ; F A W C E T T , P . ; C A M P B E L L , M . J . & S I C A , R . E . P . — E l e c t r o -p h y s i o l o g i c a l e s t i m a t i o n o f t h e n u m b e r o f m o t o r units w i t h i n a h u m a n m u s c l e . J. N e u r o l . N e u r o s u r g . P s y c h i a t . 34:121, 1 9 7 1 .
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