AS A CAUSE OF SEVERE SKIN DISEASE IN PIGS IN ZAIRE

STEPHANOFILARIA BOOMKERI N . S P . ,

AS A CAUSE OF SEVERE SKIN DISEASE IN PIGS IN ZAIRE

BAIN O.*, VAN DER LUGT J.** & KAZADI L.M.

with the technical assistance of TCHEPRAKOFF R.*

Summary :

A new Stephanofilaria, S. boomkeri n. sp., is described as the cause of skin lesions in pigs in Zaire. It is the first species described in suids. The reservoirs might be wild African suids.

The six valid species of the genus Stephanofilaria form two main groups. In one group, female worms lay sheathed microfilariae ; members of this group are exclusively African and are represented by the parasite of rhinoceros, S. dinnicki, and hippopotamus, S . thelazioides. Their morphology is primitive. In the other group, female worms lay particular « eggs » which contain microfilariae.

S. boomkeri belongs to this group, and is regarded by its cephalic structures as the most primitive representative in this group. The other species S . dedoesi and S. zaheeri. parasitize cattle in the Asiatic region. In the holarctic region, another parasite of cattle, S. stilesi, seems to be a highly specialized member of this second group. In this species as in S . boomkeri, the envelope of the « egg » is very thick and complex, probably from peculiar adaptations in order to withstand the dessication of the microfilaria.

The genus Stephanofilaria seems to have an Aethiopian origin, as in this region the species are more primitive and more varied as are also their hosts.

KEY WORDS : skin disease, pig, Africa, stephanofilariasis, systematics.

Résumé: STHEPHANOFILARIA HOOMKERI N. SP., CAUSE DE GRAVES LÉSIONS CUTANÉES DU PORC AU ZAIRE

Un élevage de porcs au Zaïre présente de graves lésions cutanées caractéristiques de stéphanofilariose. Elles sont en effet dues à un Stephanofilaria, qui est une nouvelle espèce, S. boomkeri n. sp., la première décrite chez les Suidés. Les réservoirs pourraient être les Suidés sauvages africains.

Les six espèces du genre Stephanofilaria forment deux principaux groupes. Dans l'un, les femelles pondent des microfilaires à gaine;

ce groupe, exclusivement africain, est représenté par le parasite du Rhinocéros, S . dinnicki, et le parasite de l'Hippopotame, S. thelazioides ; leur morphologie générale est primitive. Dans l'autre groupe, les femelles pondent des œufs particuliers qui contiennent une microfilaire; S. boomkeri n. sp. appartient à ce groupe et en est le représentant le plus primitif par sa structure céphalique; les autres espèces sont parasites du bétail en région asiatique, S. dedoesi et S . zaheeri. En région holarctique, un autre parasite du bétail, S . stilesi, semble être une forme hyperspécialisée de ce second groupe. L'enveloppe de l'œuf, très épaisse et complexe chez cette espèce comme chez S . boomkeri, résulterait d'adaptations particulières empêchant la dessication de l'embryon.

Le genre Stephanofilaria semble avoir une origine éthiopienne car les espèces y sont plus primitives et plus variées, comme le sont aussi leurs hôtes.

MOTS CLES : lésions cutanées, porc, Afrique, stéphanofilariose, systématique.

Formalin fixed skin samples from pigs w e r e submitted to o n e o f us (JJvdL) for evaluation. T h e s p e c i m e n s ori- ginated from a pig farm in Zaire, w h e r e an outbreak o f u l c e r a t i v e dermatitis in pigs w a s e n c o u n t e r e d . Lesions o c c u r r e d in adult s o w s , predominantly on the teats and less c o m m o n l y on the ears and legs. Histo- pathological examination o f the skin tissues revealed epidermal hyperplasia, dermatitis and nematode worms in the affected dermis. Following dissection o f the fixed skin samples, fragmented portions o f female and male worms were recovered. A morphological study s h o w e d

* Laboratoire de Biologie Parasitaire, Protistologie, Helminthologie, Muséum National d'Histoire Naturelle, 61, rue Buffon, 75231 Paris Cedex 05, France.

** Onderstepoort Veterinary Institute, Section of Pathology, PO Box 12502. Onderstepoort 0110, South Africa.

***Pathology Service, Veterinary Laboratory, PO Box 8842, Kinshasa, Zaire.

that they represent a n e w species o f Stephanofilaria.

Its interest is also phylogenetic, b e c a u s e it is the first representative o f the genus in suids.

MATERIAL

S

everal histological sections o f infected skin and several w o r m s dissected out from the skin were available. Female worms: seven anterior regions, of w h i c h o n e is the h o l o t y p e , and four posterior regions. Male worms: t w o anterior regions, and two posterior regions, o f which o n e is the allotype. All spe- c i m e n s are registered under the n u m b e r 158 SE. T y p e s p e c i m e n s and several paratype s p e c i m e n s are h o u s e d in the MNHN collections o f Paris, the other paratypes are in the Onderstepoort Veterinary Institute collec- tions.

Parasite, 1996, 4, 377-381 Mémoire 377

Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/1996034377

378 Parasite, 1996, 4, 377-381 BAIN О., VAN DER LUCT J & KAZADI L.M.

STEPHANOFILARIA BOOMERI N. SP., AS A CAUSE OF SEVERE SKIN DISEASE IN PIGS IN ZAIRE

•«| Fig. 1. — Stepbanofilaria boomkeri n. s p .

A t o E , f e m a l e ; A: p a r a t y p e , a n t e r i o r r e g i o n , lateral v i e w (frills n o t d r a w n ) ; B: h o l o t y p e , ventral v i e w (frills d r a w n ) ; C: idem, detail o f cuti­

c u l a r frills, at 2 0 0 uM from a p e x , lateral v i e w ; D: p a r a t y p e , c u t i c u l a r frills 1 m m from the c a u d a l e x t r e m i t y , lateral v i e w ( a small s u r f a c e o f t h e w o r m is p r e s e n t e d ) ; E: f e m a l e tail, lateral v i e w .

F to K, m a l e ; F: a n t e r i o r f r a g m e n t o f a p a r a t y p e ; G : i d e m , a n t e r i o r r e g i o n w i t h h e a d c o v e r e d b y a c a p o f host tissue r e a c t i o n , m e d i a n v i e w (frills d r a w n a n t e r i o r t o n e r v e r i n g ) ; H t o J , a l l o t y p e ; H: c a u d a l r e g i o n , ventral v i e w ( e n d o f frills d r a w n ) ; I: s p i c u l e s , ventral v i e w ; J : tail, lateral v i e w ; K : p a r a t y p e , c a u d a l r e g i o n a n d e x t r e m i t i e s o f t h e s p i c u l e s , v e n t r a l v i e w ( s c a l e s : F, 5 0 0 Um; A, F, G, I, 5 0 Um; 15. C, D , H, J , K, 3 0 u m ) .

Fig. 2. — Stephanofilaria boomkeri n. sp.

A to D, head; A: apical view of a female paratype to show the position of the 8 external labial papillae and the peribuccal ring; B and C: other female paratype, lateral and median views (internal spines not visible in these paratypes); D: holotype, showing the crown of the 12 internal labial spines in semi-apical view.

E: microfilaria in an • egg •, its soft envelope compressed and distorted in the ovijector; F: microfilaria in egg almond-shaped after extra­

ction from the ovijector; G: same microfilaria, from a profile view of the egg (last caudal nuclei represented); H: head of the microfilaria, ventral view (scale 20 pm).

Parasite, 1996, 4, 377-381

379

B A I N O . , V A N D E R L U G T J . & K A Z A D I L . M .

DESCRIPTION

FEMALE

(Figs.

1

et

2 )

C

uticle o f the b o d y with frills; the spines are soft, directed posteriorly and irregular; they are sparse and small in the cervical region; they r e a c h a m a x i m u m length (2 p m ) and density b e t w e e n 100 and 5 0 0 pm a p p r o a c h i n g from the head (Fig. 1 C ) ; posteriorly and far to the tail, they are again very tiny (Fig. I D ) . Deirids not observed.

H e a d with projecting cuticular ring bearing very small spines, 12 in n u m b e r in the type s p e c i m e n (Fig. 2 D ) ; in other s p e c i m e n s , the spines w e r e blunt or hidden under a c a p o f reactive tissue o f the host (Fig. 2 A ) . At the basis o f the peribuccal ring, there are four pairs (or bifid) o f conspicuous submedian spines, which cor­

r e s p o n d t o t h e four e x t e r n a l - l a b i a l papillae, e a c h divided, and t w o amphids. T h e r e are four cephalic- papillae p l a c e d at the b a s e o f the spines, s e e n only o n the type s p e c i m e n . Buccal cavity flattened laterally.

Vulva a n d nerve ring both at mid-length o f the o e s o ­ p h a g u s (Fig. 1 A ) . Intestine with thick wall and thin lumen. Tail conical and very short.

Ovaries coiled in the posterior region, like other Ste- phanofilaria s p e c i e s ; uteri parallel and fused at 7 5 0 pm from the vagina. Several mature female s h o w that n o free microfilariae are present in t h e ovijector; e a c h is e n c l o s e d in a large e g g - s h a p e d e n v e l o p e (Fig. 2 E , F, G ) . T h e microfilaria is tightly c o i l e d in h e l i x ; its head bears a h o o k , and t w o small spines on the opposite s i d e ; its caudal extremity is r o u n d e d and nucleated.

T h e e n v e l o p e o f the - e g g » presents a c o m p l e x struc­

ture and is variable in shape, showing that it is not rigid. W h e n c o m p r e s s e d in the ovijector (Fig. 1 A ) , the microfilaria is in an anterior cavity lined b y a double thin m e m b r a n e ; the posterior part o f the e g g is dilated by a voluminous b o d y placed b e t w e e n the inner and outer egg m e m b r a n e s . After extraction from the female worm, the internal b o d y b e c o m e s uniformely distri­

b u t e d ; the egg b e c o m e s almond-shaped, and its cavity central. T h e external egg membrane is granular and not rigid. T h e substance b e t w e e n the inner and outer sur­

faces o f the egg-shell has a c o n s i s t e n c y difficult to define; after fixation it s e e m s gelatinous but it c o u l d b e fluid o n fresh material. T h e egg-shell t h i c k e n s during the intra-uterine e m b r y o g e n e s i s .

Measurements: the longest fragment (which is an ante­

rior part) is 4 , 3 5 p m long and 2 0 0 p m wide. Holotype and a paratype: b u c c a l cavity 1 7 - 2 0 p m high, external- labial papillae 8-6 pm from a p e x , nerve ring at 7 0 - 90 pm, and vulva at 8 5 - 1 0 0 pm from a p e x ; oesophagus 1 7 0 - 1 6 0 pm long. Tail o f t w o paratypes: 9-16 pm. Egg extracted from the ovijector 5 2 / 3 0 pm in larger dia­

meters, with a central spherical cavity 1 5 / 1 8 um; micro­

filariae 8 0 pm long ( a p p r o x i m a t e l y ) a n d 6 p m wide.

MALE

Frills similar to that o f the female w o r m but m o r e tenuous. Peribuccal ring with spines t o o small to b e counted. Four pairs o f external labial spines. Cephalic papillae not seen.

Caudal alae absent. Papillae not pedunculated: o n e precloacal papilla, two subventral postcloacal pairs, and the phasmids; s e v e n lateral-ventral pairs, o f w h i c h the most posterior is p a r a c l o a c a l ; t w o lateral pairs, o n e p a r a c l o a c a l a n d o n e p r e c l o a c a l in p o s i t i o n . T h e papillae are small but c o n s p i c u o u s o n the tail itself;

the most anterior lateral-ventral papillae are hardly per­

ceptible and their n u m b e r is not certain.

Left spicule with shaft a n d lamina equal in length, a n d pointed distal extremity; right spicule short a n d stout, with a small subterminal dorsal h e e l a n d a r o u n d e d distal extremity. Gubernaculurn simple.

Measurements: the longest fragment ( w h i c h is an ante­

rior part) is 1,72 m m long and 150 p m wide. Anterior region o f t w o paratypes: b u c c a l cavity 2 0 - 1 8 pm l o n g ; nerve ring 9 0 - 7 0 pm from a p e x ; o e s o p h a g u s 165- 165 p m l o n g ; anterior l o o p o f the testis 5 0 0 pm from the a p e x . Posterior regions o f the allotype and a para­

type: tail 32 - 3 0 pm long; left spicule 2 2 0 - 2 3 0 pm long with shaft 110-120 m m long; right spicule 5 5 - 5 0 pm long; gubernaculurn 1 5 - 1 0 pm long.

DISCUSSION

T

he genus Stephanofilaria Ihle & Ihle-Landen- berg, 1933 has been recently analysed by Boomker et al. (1995). Nine taxa have been proposed. Two are species inquirandae: S. andamani Sinha & Das, 1958, a parasite of the water buffalo, Bubalus bubali, in the Andaman islands, and S. sri- vastavi Bhattacharjee, 1967, a parasite of the asiatic ele­

phant, Elepbas maximus, in India. Three taxa are pro­

bable synonyms of the type species S. dedoesi Ihle &

Ihle-Landenberg, 1933, described from cattle in Indo­

nesia: S. assamensis Pande, 1936, S. kaeli Buckley, 1937, and S. okinawaensis Ueno & Chibana, 1977, all from cattle, respectively in India, Malaysia and south of Japan. The four other valid species are S. zabeeri Singh, 1958, a parasite of Bubalus bubali in Pakistan, S. stilesi Chitwood, 1934, described from Bos taurus in North-America, and found later in Russia, S. dinniki Round, 1964, a parasite of the black rhinoceros, Diceros bicornis, in Kenya, and S. thelazioides Boomker, Bain, Chabaud et Kriek, 1995, a parasite of Hippopotamus africanus, in South Africa. Boomker et al. (1995) pro­

posed a phyletic classification of these species based

380 Parasite, 1996, 4, 377-381

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STEPHANOFILARIA BOOMKERI. N.SP,. as a cause o f severe skin disease: in figs in Zaire

o n the n u m b e r and position o f the spines on the h e a d ; these spines derive from the six internal labial papillae and the four external labial papillae o f the Thelazioid ancestors. T h e discussion follows this classification.

Our s p e c i m e n s r e s e m b l e S. dinniki and S. thelazioides in the primitive c e p h a l i c structure: small n u m b e r o f internal labial spines (six bifid in thelazioides, 12 equi­

distant in dinnicki and our material), four pairs o f external labial spines. H o w e v e r t h e s e t w o s p e c i e s differ from our s p e c i m e n s b y n u m e r o u s characters:

vulva near the mouth and vulvar tube very elongated, nerve ring near the oesphageal-intestinal junction, n o frills o n the cuticle o f the body, tail o f the female longer than wide and with rounded extremity, spicules and gubernaculum three-four times longer, caudal alae present with papillae p e d u n c u l a t e d ; in addition, the male o f S. thelazioides has an area rugosa. In the a b o v e two species, the ultimate stage o f embryogenesis present in the ovijector is a s h e a t h e d microfilaria.

T h e three other s p e c i e s lay « eggs » containing micro­

filariae as d o our s p e c i m e n s .

However, S. dedoesi and its close relative, the species S.

zaheeri, are distinct from our specimens by the more evolved cephalic structure: 15 spines or more forming the internal labial crown, external labial spines multiplied ( 1 6 to 32) forming a second posterior crown. T h e other dis­

tinctive characters are the denser frills and the egg with thin and simple membrane, from which the microfilaria escapes easily (Ramachandran et al., 1 9 6 6 ; Singh, 1958, respectively for S. dedoesi and S. zaheeri). Moreover, the microfilaria o f S. dedoesi is longer ( 1 4 0 um), the mature egg o f S. zaheeri is smaller (36-39/23-29 um).

S. stilesi is distinct by the very specialized cephalic mor­

p h o l o g y (five s u b m e d i a n lateral-ventral s p i n e s , in Hibler, 1966 and Anderson, 1 9 6 8 ) , the frills absent, the n o n coiled and shorter microfilaria (40-60 pm instead o f 8 0 u m ) , t h e l a r g e r e g g ( 6 7 / 5 0 um i n s t e a d o f 5 2 / 3 0 p m ) . T h e egg e n v e l o p e , which resembles that o f our s p e c i m e n s , presents in addition internal b i c o n c a v e bodies, grouped close to the microfilaria (Hibler, 1966).

T h e s p e c i m e n s from the pig in Zaire represents a n e w species, Stephanofiaria boomkeri n. sp., dedicated to our c o l l e a g u e , Professor J . B o o m k e r .

CONCLUSION

T h e c u t a n e o u s disease o f pigs, w h i c h had b r o k e n out in a piggery in Zaire, is c a u s e d by a particular para­

site, Stephanofilaria boomkeri n. sp. Wild African suids, s u c h as warthogs, might b e the reservoirs.

T h e six s p e c i e s in the genus Stephanofilaria d o not represent an h o m o g e n e o u s line. S. boomkeri has pri­

mitive c e p h a l i c characters, like the two other s p e c i e s present in the Aethiopian region, S. dinnicki from rhi­

n o c e r o s and S. thelazioides from hippopotamus, but

these two last form a distinct group, b e c a u s e they lay sheathed microfilariae. T h e n e w species, w h i c h lay

« eggs », is c l o s e to the b r a n c h formed b y the species parasite o f cattle in Asiatic region, S. dedoesi-S. zaheeri, o f w h i c h it is a primitive representative. S. stilesi, w h i c h also lays eggs, but w h i c h has a very peculiar cephalic structure and a cuticle without frills, may b e considered as a highly specialized representative o f this branch, or a distinct branch.

A priori the s p e c i e s with s h e a t h e d microfilariae are m o r e e v o l v e d than those w h i c h lay eggs. However, in the c a s e o f Stephanofilaria, the eggs are peculiar and contain a microfilaria. Moreover, it is noted that the adult m o r p h o l o g y o f the s p e c i e s with microfilariae is m o r e primitive than that o f the « oviparous » species:

female tail less atrophied, caudal alae o f the male pre­

sent. Thus it is c o n c e i v a b l e that, in this c a s e , the « ovi­

parous » s p e c i e s w o u l d derive from those with micro­

filariae, either directly, or through a c o m m o n ancestor.

T h e m o r e c o m p l e x anatomy o f the egg e n v e l o p e is observed in two distant species, S. boomkeri and S. sit- lesi, showing its adaptative value. As suggested b y Hibler ( 1 9 6 6 ) for S. stilesi, it could e n a b l e the micro­

filaria to withstand drying before being ingested by the m u s c i n e or s t o m o x i n e vectors.

T h e representatives o f the two main groups, with sheathed microfilariae and with « eggs », are present in the Aethiopian region (Zaire, Kenya, South Africa) and they are morphologically primitive. It is also in this region that the hosts are the most varied: artiodactyls s u c h as suids and the hippopotamus, perissodactyls such as the rhinoceros. T h e s e observations strengthen the conclusions o f B o o m k e r et al. ( 1 9 9 5 ) w h o p r o p o s e an African origin for the genus Stephanofilaria.

REFERENCES

ANDERSON R.C. The comparative morphology of cephalic structures in the superfamily Filarioidea (Nematoda). Cana­

dian Journal of Zoology, 1 9 6 8 , 46. 1 8 1 - 1 9 9 .

BOOMKER J , BAIN O., CHABAUD A. & KRIEK N.P.J. Stephanofi­

laria thelazioides n. sp. (Nematoda: Filariidae) from a hip­

popotamus and its affinities with the species parasitic in the African black rhinoceros. Systematic Parasitology, 1 9 9 5 , 32, 2 0 5 - 2 1 0 .

HIBLER CP. Development of Stephanofilaria stilesi in the horn fly. Journal of Parasitology, 1 9 6 6 , 52, 8 9 0 - 8 9 8 .

RAMACHANDRAN CP., LORE Y.M. & NAGENDRAM C. Studies on Stephanofilaria kaeli in cattle. Medical Journal of Malaya, 1 9 6 6 , 2 0 , 3 4 4 - 3 4 7 .

SINGH S.N. On a new species of Stephanofilaria causing der­

matitis of buffaloes' ears in Hyderabad (Andhra Pradesh) India. Journal of Helminthology, 1 9 5 8 , 32, 2 3 9 - 2 5 0 .

Recu le 2 0 mai 1 9 9 6 Accepte le 2 6 septembre 1 9 9 6

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