HALICEPHALOBUS GINGIVALIS (STEFANSKI, 1 9 5 4 ) FROM A FATAL INFECTION IN A HORSE IN ONTARIO, CANADA
w i t h comments
on the v a l i d i t y o f H. DELETRIX and a r e v i e w o f the genus
ANDERSON R.C.*, UNDER K.E.** & PEREGRINE A.S.**
S u m m a r y :
Halicephalobus gingivals (Stefanski, 1954), from a fatal infection in a horse in Ontario, Canada, was cultured and restudied.
Although the original description given by Stefanski (1954) was satisfactory, Anderson & Bemrick (1965), in describing H. deletrix (= Micronema deletrix), claimed Stefanski's description was
« inadequate » and the species a « species inquirenda ». Thus, infections in horses and humans have been assigned to H. deletrix. W e believe the species reported in horses and humans is H. gingivalis and that H. deletrix is its synonym.
H. gingivalis is separated herein from forms found free-living. The genital tract in the advanced fourth stage of H. gingivalis is didelphic and amphidelphic and terminal ends of the horns are reflected, the anterior one ventrally, the posterior one dorsally. In the adult parthenogen the latter forms a short ovary, whereas most of the anterior horn forms a combined uterus-oviduct as a receptacle for a single large egg which is laid in the 2-cell or multi-cell stage. Eggs in the 2-cell stage embryonated to larvae in
17 hours at 2 8 °C but did not hatch until an additional 2 4 hours.
First-stage larvae were unusually large and variable in length (136- 199 µm x = 168). Inactive third-stage larvae were 1 8 0 - 2 4 0 µm (x = 2 0 3 ) in length. The possible route of infection in horses and humans is briefly discussed.
K E Y W O R D S : Halicephalobus gingivalis, Micronema, Nematoda, Panagrolaimidae, horse, taxonomy.
Résumé : HALICEPHALOBUS GINGIVALIS (STEFANSKI, 1 9 5 4 ) DANS UNE INFFETION FATALE CHEZ UN CHEVAL D'ONTARIO, CANADA AVEC
COMMENTAIRE SUR LA VALIDITÉ DE H. DELETRIX ET UNE REVUE DU GENRE Une souche d'Halicephalobus gingivalis (Stefanski, 1954), isolé d'une infection fatale d'un cheval d'Ontario au Canada, a été cultivée et réétudiée. Bien que la description originale de Stefanski ( 1 9 5 4 ) soit satisfaisante, Anderson & Bemrick (1965), dans leur description de H. deletrix (= Micronema deletrixj, ont considéré que la description de Stefanski était « inadéquate » et que l'espèce devrait être considérée comme « species inquirenda ».
Ainsi, les infections chez le cheval et l'humain ont été attribuées à H. deletrix. Nous croyons que l'espèce rapportée chez le cheval et l'humain est H. gingivalis et que H. deletrix est son synonyme.
Dans l'étude présente, H. gingivalis est isolé de formes trouvées libres. La branche génitale du quatrième stade avancé de H. gingivalis est didelphique et amphidelphique et les extrémités des cornes sont repliées, l'antérieure du côté ventral, et la postérieure du côté dorsal. Chez l'adulte parthogénétique, cette dernière forme un petit ovaire, tandis que la majeure partie de la corne antérieure forme un utérus-oviducte réunis en un réceptacle pour un gros œuf unique qui est pondu au stade bicellulaire ou multi-cellulaire. Les œufs du stade bicellulaire se sont developpés en larves en 17 h à 28 °C mais n'ont éclos que 24 h plus tard.
Les larves du premier stade étaient anormalement grosses et variables en longueur (136-199 µm x = I68). Les larves inactives du troisième stade mesuraient 180-240 µm (x = 203). La voie probable d'infection chez le cheval et l'humain est discutée brièvement.
MOTS CLES : Halicephalobus gingivalis, Micronema, Nematoda, Panagrotaimidae, cheval, taxonomy.
INTRODUCTION
H a l i c e p b a l o b u s gingivalis w a s first d e s c r i b e d a c c u r a t e l y b y Stefanski ( 1 9 5 4 ) o n t h e b a s i s o f w o r m s f o u n d in a g r a n u l o m a in t h e g i n g i v a e o f a h o r s e in P o l a n d . H e p l a c e d t h e s p e c i e s in t h e g e n u s Rhabditis. It w a s transferred t o t h e g e n u s Tri- cephalobus b y D o u g h e r t y ( 1 9 5 5 ) , a d e c i s i o n r e p r o - d u c e d w i t h o u t c o m m e n t b y B a k e r ( 1 9 6 2 ) a n d L e v i n e
* D e p a r t m e n t o f Z o o l o g y , U n i v e r s i t y o f G u e l p h , G u e l p h , O n t a r i o C a n a d a N 1 G 2 W 1 .
** D e p a r t m e n t o f P a t h o b i o l o g y , O n t a r i o V e t e r i n a r y C o l l e g e , U n i v e r - sity o f G u e l p h , G u e l p h , O n t a r i o , C a n a d a N 1 G 2 W 1
C o r r e s p o n d e n c e : R.C. A n d e r s o n .
Tel.: ( 5 1 9 ) 8 2 4 - 4 1 2 0 , e x t . 2 7 1 5 - F a x : ( 5 1 9 ) 7 6 7 - 1 6 5 6 . E m a i l : < r a n d e r s o @ u o g u e l p h . c a > .
( 1 9 6 8 ) . S u d h a u s ( 1 9 7 6 ) p l a c e d gingivalis in Trilabiatus a n d later A n d r a s s y ( 1 9 8 4 ) p l a c e d t h e s p e c i e s in Hali-
cephalobus T i m m , 1 9 5 6 w h e r e it r e m a i n s t o d a y . Although H. gingivalis w a s r e p o r t e d in a h o r s e a n d has priority, r e p o r t s o f similar i n f e c t i o n s in h o r s e s a n d h u m a n s h a v e almost invariably ignored this s p e c i e s a n d identified t h e a g e n t as Micronema deletrix or, m o r e r e c e n t l y , Halicephalobus deletrix. Micronema deletrix from a « nasal t u m o u r » o f a h o r s e in M i n n e s o t a , USA w a s d e s c r i b e d b y A n d e r s o n & B e m r i c k ( 1 9 6 5 ) ; t h e cli- nical p a t h o l o g y o f this c a s e w a s d e s c r i b e d b y J o h n s o n
& J o h n s o n ( 1 9 6 6 ) w h o r e p o r t e d the n e m a t o d e s mainly in large g r a n u l o m a s in t h e m a x i l l a e . A n d e r s o n & B e m - rick ( 1 9 6 5 ) s t a t e d in a s h o r t p o s t s c r i p t t o t h e i r p a p e r
« Rhabditis gingivalis Stefanski ( 1 9 5 4 ) d e s c r i b e d from a g r a n u l o m a o f t h e g u m o f a h o r s e a p p e a r s to b e a s p e c i e s o f Micronema but is i n a d e q u a t e l y d e s c r i b e d
Parasite, 1 9 9 8 , 5 , 2 5 5 - 2 6 1
Mémoire 255
Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1998053255
and must b e c o n s i d e r e d species inquirenda ». Thus it c a m e about that s u b s e q u e n t reports o f these kinds o f n e m a t o d e s , causing serious and generally fatal infec
tions in horses and humans, ignored Stefanski's spe
cies and w e r e invariably assigned to Micronema dele- trix o r later Halicephalobus deletrix. B l u n d e n et al.
( 1 9 8 7 ) placed a further cloud over gingivalis w h e n they stated in references to « Stefanski ( 1 9 5 3 ) » « ... n e m a t o d e not described ... ».
Andrassy ( 1 9 8 4 ) r e c o g n i z e d the n a m e Micronema was p r e o c c u p i e d and h e transferred the s p e c i e s o f Micro
nema to the g e n u s Halicephalobus Timm, 1 9 5 6 . He p l a c e d gingivalis in this genus. Andrassy ( 1 9 8 4 ) and Geraert et al. ( 1 9 8 8 ) in reviews o f the genus Halice
phalobus apparently regarded H. deletrix as a possible s y n o n y m o f H. gingivalis. Although they gave n o rea
sons for this possibility it can probably b e assumed that it w a s b e c a u s e H. gingivalis and H. deletrix w e r e both from lesions in horses.
W e have recently c o l l e c t e d n e m a t o d e s from a fatal infection in a horse in Ontario that agree in all parti
culars with Stefanski's species. In addition, w e have successfully cultured the n e m a t o d e for the first time and studied its d e v e l o p m e n t and are able to provide a n e w and m o r e detailed description b a s e d o n abun
dant living and fixed material. W e establish H. gingi
valis as a valid s p e c i e s o f Halicephalobus and confirm that H. deletrix is a synonym. In addition, w e consider briefly the possible relationship o f H. gingivalis to the k n o w n free-living m e m b e r s o f Halicephalobus.
MATERIALS & METHODS
I
n D e c e m b e r 1 9 9 7 an 1 8 - y e a r o l d h o r s e w a s admitted at the Ontario Veterinary College with a fatal infection o f H. gingivalis1. Nematodes w e r e c o l l e c t e d from lesions within the mandible at post mortem by maceration o f tissue in saline. Parasites w e r e then inoculated o n t o Luria broth agar containing 50 p g / m l ampicillin o n t o w h i c h ampicillin-resistant Escherichia coli w e r e also plated, and maintained o n the b e n c h at 18-22 °C. Active proliferation, with g e n e ration o f all life-cycle stages o c c u r r e d o n this medium.Parasites from these plates w e r e then established as actively proliferating populations in saline containing E. coli, solute o f sterilized b o v i n e faeces and 4 m m3 p i e c e s o f agar, as this culture system produced larger n u m b e r s o f parasites than the solid agar system.
Live n e m a t o d e s w e r e studied in saline under covers- lips sealed with vaseline. T h e adults remained active for p r o l o n g e d periods and laid eggs. T h e eggs readily
1. T h e c l i n i c a l a c c o u n t o f this c a s e will b e p u b l i s h e d e l s e w h e r e .
e m b r y o n a t e d and h a t c h e d and the larvae grew for several days. It was possible to n o t e the rate o f deve
l o p m e n t and hatching under these conditions.
S o m e adult n e m a t o d e s w e r e placed o n a glass slide in a drop o f saline and subjected to mild heat which immobilized them without affecting their anatomy. T h e drop o f saline with the relaxed nematodes was covered with a coverslip sealed with vaseline and major mor
phological measurements w e r e made. Droplets o f lipid in the intestinal cells o f the n e m a t o d e s tended to o b s c u r e t h e m o r p h o l o g y o f parts o f the reproductive system. T o solve the problem s o m e n e m a t o d e s w e r e fixed in hot glycerine alcohol ( 7 0 % ethanol and 5 % glycerine) and the mixture was e x p o s e d to air for a day or two to allow the alcohol to evaporate. T h e n e m a todes w e r e then e x a m i n e d in pure glycerine. T h e pro
c e s s removed lipid and h e l p e d e x p o s e the details o f t h e r e p r o d u c t i v e s y s t e m . S o m e n e m a t o d e s w e r e immersed in a solution o f aniline blue which differen
tially stained the ovary in the mature w o r m s and the genital primordia in third and fourth-stage nematodes.
RESULTS
HALICEPHALOBUS GINGVALIS (STEFANSKI, 1 9 5 4 ) (Fig. 1-8)
Synonyms
Rhabditis gingivalis Stefanski, 1 9 5 4 ;
Tricephalobus gingivalis (Stefanski, 1 9 5 4 ) Dougherty, 1 9 5 5 ;
Halicephalobus gingivalis (Stefanski, 1 9 5 4 ) Andrassy, 1 9 8 4 ;
Trilabiatus gingivalis (Stefanski, 1 9 5 4 ) Sudhaus, 1 9 7 6 ; Micronema deletrix Anderson & B e m r i c k , 1 9 6 5 ; Halicephalobus deletrix (Anderson & B e m r i c k , 1 9 6 5 ) ; Andrassy, 1 9 8 4 .
G e n e r a l
N e m a t o d a , R h a b d i t o i d e a , P a n a g r o l a i m i c l a e T h o r n e 1937, T r i c e p h a l o b i n a e Andrassy, 1 9 7 6 . Small parthe- n o g e n e t i c n e m a t o d e s . O e s o p h a g u s with median swel
ling.
P a r t h e n o g e n e t i c F e m a l e ( F o r m o r p h o m e t r i e s s e e T a b l e I ) . B o d y curved slightly ventrally w h e n fixed (Fig. 8 ) . Six prominent but transparent, r o u n d e d lips (Fig. 4 ) . Cuticle s m o o t h and thin with e x t r e m e l y o b s cure transverse striations in anterior region. Tail conical, ending in fine point, phasmids short distance b e h i n d anus (Fig. 7 ) . Buccal cavity elongate, divided into two sections with ring at b a s e (Fig. 4 ) . Nerve ring b e t w e e n v a l v e d b u l b and m e d i u m swelling o f o e s o p h a g u s (Fig. 8 ) . Excretory p o r e adjacent to nerve ring. Intes
tinal cells p a c k e d with r o u n d lipid droplets along
Parasite, 1 9 9 8 , 5, 2 5 5 - 2 6 1
256- Mémoire
HALICEPHALOBUS GINGIVALIS F R O M A F A T A L I N F E C T I O N I N A H O R S E
Figs. 1-8. - Halicephalobus gingivalis ( S t e f a n s k i , 1 9 5 4 ) .
Fig. 1-3. - D e v e l o p m e n t o f t h e e g g s from t h e t w o - c e l l e d s t a g e t o larva.
Fig. 4 . - C e p h a l i c e n d s h o w i n g r o u n d e d , t r a n s p a r e n t lips a n d b u c c a l cavity.
Fig. 5. - G e n i t a l p r i m o r d i u m o f t h e third-stage larva.
Fig. 6. - G e n i t a l s y s t e m in t h e fourth s t a g e larva ( d i d e l p h i c , a m p h i d e l p h i c ) . Fig. 7. - C a u d a l e n d o f p a r t h e n o g e n s h o w i n g a n u s a n d p h a s m i d s .
Fig. 8. - G r a v i d p a r t h e n o g e n (lateral v i e w ) w i t h fully d e v e l o p e d b u t u n s e g m e n t e d e g g in m o d i f i e d a n t e r i o r h o r n o f r e p r o d u c t i v e tract a n d s h o r t r e f l e x e d o v a r y o f t h e p o s t e r i o r h o r n . Lipid d r o p l e t s a b u n d a n t in intestinal c e l l s .
Parasite, 1 9 9 8 , 5, 2 5 5 - 2 6 1
Mémoire 257
A u t h o r ( s )
S t e f a n s k i
(1954)
G u e l p h ( p r e s e n t )
A n d e r s o n
& B e m r i c k
(1965)
N 1 0 ? 2 8
M e t h o d F r o m t i s s u e Living, F r o m f r o z e n
f i x e d i m m o b i l i z e d tissue in f o r m a l i n w i t h m i l d h e a t
L e n g t h b o d y 2 5 0 - 4 3 0 3 1 1 - 4 1 1 ( 3 6 7 ) 2 5 0
a 1 7 - 2 3 1 5 - 2 0 ( 1 8 ) 1 5 - 2 0 ( 1 7 )
b 3 . 5 - 3 . 8 3 . 2 - 4 . 5 ( 3 . 9 ) 2 . 9 - 3 . 6 ( 3 . 3 ) c 5 . 5 - 7 . 0 4 . 5 - 6 . 6 ( 5 . 5 ) 4 . 4 - 6 . 3 ( 5 . 1 )
V 6 0 - 6 5 4 6 - 6 1 ( 5 6 ) 5 6 - 6 3 ( 5 9 )
M a x i m u m w i d t h 1 4 - 2 0 1 8 - 2 1 ( 2 0 )
—
L e n g t h B u c c a l c a v i t y ? 4-5** 8 - 1 1 ( 1 0 )
—
L e n g t h O e s o p h a g u s 7 0 - 9 0 7 6 - 9 0 ( 8 4 )
—
V u l v a ( f r o m ant. 9 0 - 2 1 0 1 5 5 - 2 5 5 ( 2 0 3 )
—
E n d )
L e n g t h T a i l 4 0 - 6 0 5 9 - 7 5 ( 6 6 )
S i z e o f E g g s 4 0 x 2 0 4 8 - 5 1 x 1 6 - 2 1 3 2 - 4 6 x 9 - 1 1
* The D e M a n r a t i o s (a t o c + v) f a v o u r e d b y p l a n t a n d soil n e m a - t o l o g i s t s a r e a s f o l l o w s : a = body l e n g t h / m a x i m u m w i d t h ; b = b o d y l e n g t h / l e n g t h o f o e s o p h a g u s ; c = b o d y l e n g t h / t a i l l e n g t h ; v = dis
t a n c e o f v u l v a f r o m a n t e r i o r e n d a s p e r c e n t of total l e n g t h . O t h e r m e a s u r e m e n t s a r e in µm.
** S t e f a n s k i ' s f i g u r e s f o r t h e l e n g t h o f t h e b u c c a l c a p s u l e a r e o b v i o u s l y in e r r o r a s his illustration s h o w s t h e figures s h o u l d b e a b o u t 1 0 µm.
T a b l e I. - C o m p a r a t i v e M e a s u r e m e n t s o f ( a d u l t s ) Halicephalubus gin- givalis a n d H. deletrix from H o r s e s * .
entire length. Vulva a b r o a d lateral slit o n slight ele
vation. R e p r o d u c t i v e s y s t e m clearly d i d e l p h i c and a m p h i d e l p h i c in fourth-stage larva (Fig. 6 ) . In fully d e v e l o p e d adult posterior arm o f reproductive tract r e d u c e d to ovary only with about 9-12 o o c y t e s increa
sing in size from posterior e n d to anterior region (Fig. 8 ) . Terminal e n d o f ovary curved ventrally. In fully gravid n e m a t o d e anterior arm o f reproductive tract modified as c o m b i n e d oviduct and uterus containing single large, e l o n g a t e e g g (16-21 x 4 8 - 5 1 µm in size) with thin pliable shell. Terminal e n d o f anterior arm finger-like, non-functional and bent dorsally and poste
riorly. Egg unusually large (Figs. 1-3), s e g m e n t e d or u n s e g m e n t e d in situ but generally deposited by female in 2-cell o r 8-cell stage, but larvating and hatching in m o r i b u n d p a r e n t (matricidal e n d o t o k y ) . Egg c o m pressed laterally w h e n b e i n g e x p r e s s e d from parent.
Eggs embryonating from 2-cell stage to larva in 17- 18 hours at 2 8 °C and 24 hours at 24-25 °C (Fig. 1-3).
Eggs hatching about 24 hours after larvae formed in egg. Newly h a t c h e d larvae unusually long, 1 3 6 - 1 9 9 ( x = 1 6 8 ) p m in length and 9-10 (x = 9 . 6 ) p m in width (N = 1 0 ) . In unsuitable conditions larvae c e a s e to develop and b e c o m e quiescent at third-larval stage 180- 2 4 0 (x = 2 0 3 ) p m in length and 9-10 ( x = 9-5) pm in width (N = 1 0 ) .
Cultured n e m a t o d e s w e r e identical in m o r p h o l o g y to those found in the lesions from the horse.
Host and Locality: Horse (Equus caballus L.), Ontario, Canada.
Location in Host: G u m s (gingivae) mandible ( m a r r o w ) and brain.
S p e c i m e n s : United States National Parasite Collection No. 8 7 8 3 7 .
DISCUSSION
M
o r p h o m e t r i c data indicate that the s p e c i m e n s d e s c r i b e d b y Stefanski ( 1 9 5 4 ) and t h o s e d e s c r i b e d h e r e i n a r e c o n s p e c i f i c ( T a b l e I ) . In addition, Stefanski's illustration a c c o r d s with the n e w observations, including the structure o f the reproductive system w h i c h h e n o t e d w a s amphidelphic.
Unfortunately the type s p e c i m e n s o f H. deletrix c a n n o t b e found and m a y n o l o n g e r exist. In d e s c r i b i n g H. deletrix, Anderson & B e m r i c k ( 1 9 6 5 ) apparently m e a s u r e d 2 8 individuals but they g a v e the length o f t h e b o d y as 0 . 2 5 0 m m (without r a n g e s ) w h i c h is s m a l l e r than t h e s p e c i m e n s s t u d i e d h e r e i n but is a c c o m m o d a t e d b y the original description o f H. gin- givalis. W e a s s u m e Anderson & B e m r i c k ( 1 9 6 5 ) m e a sured smaller adult w o r m s w h i c h w e r e not yet fully grown. T h e s e types o f adults w e r e predominant in our cultures but not included in our data in favour o f larger adults with fully-shelled eggs. Presumably Stefanski ( 1 9 5 4 ) included s o m e smaller adults in his data as well as h e reported a range o f 2 5 0 - 4 3 0 µm w h i c h c o v e r s not only our s p e c i m e n s but those o f Anderson & B e m rick ( 1 9 6 5 ) .
Anderson & Bemrick ( 1 9 6 5 ) gave the width o f the eggs as o n l y 9 - 1 1 p m . T h e s e s m a l l e r f i g u r e s c a n b e e x p l a i n e d if o n e a s s u m e s e g g s w e r e m e a s u r e d only in utero and w e r e not d e v e l o p e d to the extent that the shell had formed ( s e e Fig. 1 in Anderson & B e m r i c k , 1 9 6 5 ) . In the present study e g g s w e r e m e a s u r e d after they w e r e e x p e l l e d . Even e g g s with shells c a n b e c o m p r e s s e d in utero as the shell is markedly flexible.
Fine cuticular « annulations » w e r e reported in the cuticle o f H. deletrix b y Anderson & B e m r i c k ( 1 9 6 5 ) . Such « annulations » have n e v e r b e e n reported in any o t h e r description o f Halicephalobus spp. although extremely fine striations can b e s e e n in the anterior region in our material. It is possible that the s p e c i m e n s used by Anderson & B e m r i c k ( 1 9 6 5 ) w e r e s o m e w h a t contracted by freezing since the w o r m s w e r e r e m o v e d from frozen tissue. Very fine striations are e x c e e d i n g l y difficult to depict in illustrations and there is n o d o u b t the authors have o v e r e m p h a s i z e d t h e m in their figure.
All o t h e r features, including the illustration o f the reproductive system a g r e e c o m p l e t e l y with H. gingi- valis and w e regard H. deletrix as a s y n o n y m o f this s p e c i e s .
258 P a r a s i t e , 1 9 9 8 , 5, 2 5 5 - 2 6 1
Mémoire
HALICEPHALOBUS GINGIVALIS F R O M A F A T A L I N F E C T I O N I N A H O R S E
In addition to H. gingivalis and H. deletrix w h i c h w e r e originally d e s c r i b e d from s p e c i m e n s found in horses, s e v e n o t h e r s p e c i e s have b e e n described in various situations as follows:
( 1 ) H. limuli Timm, 1 9 5 6 (the g e n o t y p e ) found at the mouth o f a freshwater stream in Pakistan.
( 2 ) H. similigaster (Andrassy, 1 9 5 2 ) found in dark b r o w n w a t e r in the trunk o f a tree in G e r m a n y . ( 3 ) H. minutum (Korner, 1 9 5 4 ) found in moist mulch in the trunks o f spruce and sycamore trees in Germany.
( 4 ) H. parvum (Korner, 1 9 5 4 ) found in moist mulch in the trunk o f o a k and linden trees in G e r m a n y . ( 5 ) H. palmaris (Lordello & Oliveira, 1 9 6 3 ) found in the stem o f a plant Roystonea oleracea in Brazil.
( 6 ) H. intermedia (Pokrovskaja, 1 9 6 4 ) found in galls o n c u c u m b e r roots in Russia.
( 7 ) H. laticauda Geraert, Sudhaus, Lenaerts and B o s - mans, 1 9 8 8 found in a water pit in a c o a l m i n e in B e l gium.
T h e D e Man measurements (for definitions see T a b l e I) are not helpful in distinguishing s p e c i e s o f Halice- phalobus b e c a u s e there is so m u c h overlap in the data
b e t w e e n s p e c i e s ( T a b l e I I ) . T h e s h a p e o f the tail and descriptions o f the reproductive tract s e e m to distin
guish H. gingivalis from other s p e c i e s in the genus.
T h e reproductive tract o f H. limuli is said to b e pro- delphic and m o n o d e l p h i c unlike that in H. gingivalis.
H. minutum and H. parvum have m u c h m o r e slender tails than that in H. gingivalis. In H. intermedia the reproductive tract is s h o w n to b e didelphic and amphi- delphic but the specimen illustrated was apparently not gravid and the reproductive tract is similar to that in the fourth-stage larvae o f H. gingivalis; the p r e s e n c e o f this s p e c i e s in galls o n the roots o f c u c u m b e r s sug
gests it must b e distinct from H. gingivalis. H. palmaris is d e s c r i b e d as m o n o d e l p h i c , unlike H. gingivalis.
H. laticauda r e s e m b l e s H. gingivalis but the c e p h a l i c e n d is wider and the authors refer to « ... inner scle- rotizations at the tip ... » o f the tail. T h e reproductive tract has not b e e n properly described.
T h e r e h a v e b e e n three reports o f Halicepbalobus (= Micronemd) infections in h u m a n s , all in North America and fatal. In o n e c a s e in Canada, the n e m a -
S p e c i e s L e n g t h a b c V
gingivalis" 3 1 1 - 4 1 1 ( 3 6 7 ) 1 5 - 2 0 3 . 2 - 4 . 5 4 . 6 - 6 . 6 4 6 - 6 1 limuli 4 2 6 - 4 6 0 2 0 . 0 - 2 1 . 3 4 . 0 - 4 . 8 6 . 7 - 7 . 0 5 9 . 3 - 6 1 . 2 similigaster 2 3 5 - 3 8 5 ( 3 8 0 ) 1 7 . 3 - 2 1 . 0 3 . 7 - 4 . 3 4 . 0 - 4 . 6 5 3 . 6 - 5 5 . 8 minutum 2 6 6 - 2 8 3 2 2 . 2 - 2 4 . 8 3 . 9 - 4 . 3 5 . 2 - 6 . 5 5 7 . 4 - 6 3 . 1 parvum 2 5 1 - 4 0 9 1 7 . 0 - 2 4 . 2 4 . 0 - 5 . 2 3 . 8 - 4 . 5 5 3 . 3 - 5 5 . 8 palmaris 3 6 1 - 4 1 0 1 6 . 8 - 1 8 . 6 3 . 8 - 4 . 5 6 . 9 - 7 . 5 5 6 . 6 - 6 0 . 2 intermedia 2 3 0 - 3 2 4 1 2 . 7 - 2 2 . 6 3 . 2 - 4 . 5 5 . 0 - 6 . 8 5 8 . 2 - 6 5 . 8 laticauda 2 5 5 - 3 4 7 2 4 - 2 9 3 . 3 - 4 . 2 4 . 5 - 7 . 3 4 . 1 - 6 . 2
T a b l e II. - D e M a n ' s ratios of the v a r i o u s s p e c i e s o f Halicepbalobus ( f o r e x p l a n a t i o n s e e T a b l e I ) .
P a r a s i t e , 1 9 9 8 , 5, 2 5 5 - 2 6 1
todes presumably e n t e r e d lacerations c o n t a m i n a t e d with manure (Hoogstraten & Y o u n g , 1 9 7 5 ) and in another c a s e (in the United States) the route o f entry was conjectured to b e decubitus ulcers o n the buttocks (Gardiner et al, 1 9 8 0 ) . In the third case, also in the United States, n o o b v i o u s lesion was observed that w o u l d have e x p l a i n e d entry ( S h a d d u c k et al, 1 9 7 9 ) . S o m e 2 5 c a s e s o f infection have b e e n reported in horses and they have a w i d e g e o g r a p h i c distribution as follows:
Poland - (Stefanski, 1 9 5 4 ) ;
United Kingdom - (Angus et al, 1 9 9 2 ; Blunden et al, 1 9 8 7 ; Khalil et al, 1 9 7 9 ) ;
Netherlands - ( K e g et al, 1 9 8 4 , Linde-Sipman & Gruys, 1 9 7 0 ) ;
Switzerland - ( P o h l e n z et al, 1 9 8 1 ) ; Columbia - (Payan et al, 1 9 7 9 ) ; Egypt (Ferris et al, 1 9 7 2 ) ; J a p a n ( Y o s h i h a r a et al, 1 9 8 5 ) ;
North America - (Alstad & Berg, 1 9 7 9 ; Cho, 1 9 8 5 ; D a r i e n et al, 1 9 8 8 ; D u n n et al, 1 9 9 3 ; J o h n s o n
& J o h n s o n , 1 9 6 6 ; J o r d a n et al, 1 9 7 5 ; Kreuder et al, 1 9 9 6 ; Pletcher & Howerth, 1 9 8 0 ; Powers & Benz, 1 9 7 7 ; Rames et al, 1 9 9 5 ; Rubin & Woodward, 1 9 7 4 ; Ruggles et al, 1 9 9 3 ; Simpson, 1 9 9 3 ; Simpson et al, 1 9 8 8 ; Spal
ding et al, 1 9 9 0 ; Stone et al, 1 9 7 0 ; Trostle etal, 1993).
Halicephalobus gingivalis s e e m s to b e a cosmopolitan s p e c i e s and o n e w o n d e r s if it might have a predilec
tion to d e v e l o p in e q u i n e manure and this might a c c o u n t for its rather frequent a p p e a r a n c e in horses.
T h e route o f entry into the horse may b e varied. It can p r o b a b l y d e v e l o p in plant material with b a c t e r i a e m b e d d e d in the gums and b e t w e e n the teeth espe
cially in older animals. This would account for reports involving the maxillae and mandibles. T h e worms may eventually get into the b l o o d and b e disseminated to other regions o f the body, including, most importantly, the central nervous system (Ruggles et al, 1 9 9 3 ) . D u n n et al. ( 1 9 9 3 ) & Payan et al. ( 1 9 7 9 ) have reported invasions o f the p r e p u c e and o n e might e x p e c t a soil nematode would have the opportunity to invade this region o f a horse. Simpson et al. (1988) reported H. dele
trix in granulomas in the leg as well as in other regions o f the body. S u c h infections might b e initiated by nematodes invading a lesion in the skin. Rames et al ( 1 9 9 5 ) reported an infection w h i c h started in the orbit and progressed to the brain. Orbital infections could b e initiated b y larvae o f H. gingivalis carried o n the b o d y o f muscoid flies like Musca autumnalis, the face fly introduced in the 1950's to North America and n o w a widespread pest o f horses and cattle.
In making diagnoses it is important to study the n e m a t o d e s carefully. G r e n i e r ( 1 9 9 1 ) found a free-living n e m a t o d e causing mastitis in a mare that could not b e assigned to Halicephalobus. A review o f the literature
Mémoire 259
suggests most infections have b e e n diagnosed correctly but the possibility o f other free-living n e m a t o d e s being involved c a n n o t b e ruled out.
ACKNOWLEDGEMENTS
D
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Reçu le 25 juin 1998 Accepté le 3 juillet 1998
Parasite, 1 9 9 8 , 5, 2 5 5 - 2 6 1 261
Mémoire
