MOUNEUS TORULOSUS
( N E M A T O D A , TRICHOSTRONGYLINA, MOLINEOIDEA)
A PARASITE OF NEOTROPICAL PRIMATES! N E W MORPHOLOGICAL A N D HISTOLOGICAL DATA
DURETTE DESSET M.-C*. FRIBOURG BLANC L.A.* & W O N G P.N.**
S u m m a r y :
Molineus torulosus (Molin, 1 8 6 1 ) parasite of Cebus spp. from South America is redescribed in Cebus apella and C. olivecaeus
(new host) from French Guyana with emphasis on the synlophe.
During the maturation process, the larvae dwelt in the cysts carved alongside the external part of the small intestine. The turn-out of the mature worms and the laid eggs depended on the tissular organisation of cyst w a l l s as the inflammatory process waned and fibrosis progressed to seal the cystic lumen. Adult worms entwine themselves in the cysts, live there permanently as their presence has never been evidenced in the intestinal lumen. They copulated, laid eggs, degenerated and died once entrapped by the fibrotic process. Laid eggs released in the intestinal lumen through a narrow channel ensured the continuation of the developmental cycle. However, erratic migration w a s possible via the vascular channels surrounding the cysts.
KEY WORDS : Molineus torulosus (Molin, 1861), Nematoda, Trichostrongylina, Molineoidea, Neotropical primates, histology.
Résumé : МОИLINEUS TORULOSUS (NEMATODA, TRICHOSTRONGYLINA, MOLINEOIDEA) PARASITE DE PRIMATES NÉOTROPICAUX : NOUVELLES DONNÉES MORPHOLOGIQUES ET BIOLOGIQUES
Molineus torulosus (Molin, 1861) parasite de Cebus spp. en
Amérique du Sud esl redécrit chez Cebus apella et chez
C. olivecaeus (nouvel hôte) en Guyane française en particulier sur les caractères du synlophe et ceux de la femelle qui n'étaient pas connus. Lors de la maturation, les larves résident dans des kystes creusés le long de la partie externe de la paroi intestinale. Le devenir des Vers matures et des oeufs dépend de l'organisation tissulaire de la paroi kystique dont la détersion du processsus inflammatoire est suivie par une fibrose cicatricielle qui tend à colmater la lumière kystique. Les Vers adultes s'enferment dans les kystes, y vivent de façon permanente puisque leur présence n'a jamais été démontrée dans la lumière intestinale. Ils s'accouplent, pondent des oeufs, dégénèrent et meurent une fois englobés dans le tissu fibreux. Les œufs pondus, largués dans la lumière intestinale par un pertuis, assurent la continuité du cycle.
MOTS CLÉS : Molineus torulosus (Molin, 1861), Nematoda, Trichostrongylina, Molineoidea, Primates néotropicaux, histologie.
INTRODUCTION
T
h e g e n u s Molineus Cameron, 1 9 2 3 , is wides- pread throughout the World ( e x c e p t Australia) in t h e C a r n i v o r a a n d N e o t r o p i c a l p r i m a t e s . A m o n g the four s p e c i e s described in these hosts, Moli-neus torulosus (Molin, 1 8 6 1 ) , a parasite o f Cebus spp.
( C e b i d a e ) is the only o n e w h o s e site is very particular.
T h e adult w o r m s dwell in nodular formations, deve- l o p e d alongside the external wall o f the small intes- tine. T h e s e nodules c o m m u n i c a t e with the intestinal lumen through a channel. T h e histological aspect o f these structures has b e e n studied by several authors (Mazza & Parodi, 1 9 3 0 ; Brack, Myers & Kunz, 1973;
R e g o & Schàeffer, 1 9 8 7 ) . However, the morphological
* Laboratoire de Biologie Parasitaire, Protistologie, Helminthologie, IFR 63, CNRS, Muséum national d'Histoire naturelle, 61, rue Buffon.
F-75231 Paris cedex 05.
** Unité d'Anatomie et de Cytologie Pathologiques, Hôpital St- Michel, 33, rue Olivier de Serres, F-75730 Paris cedex 15.
Correspondence : M.-C. Durette-Desset.
Fax : 1 (33) 40 79 38 99.
E-mail : mcdd@cimrsl.mnhn. fr
data c o n c e r n i n g this species have not b e e n thoroughly investigated.
During a mission in French Guyana (July-August 1 9 9 2 ) in the hunting grounds o f the Wayapi Indians, o n e o f the authors (L.A.F.B.) was able to e x a m i n e the small intestines o f s o m e m o n k e y s and to collect n e w mate- rial.
T h e aim o f this w o r k is to redescribe Molineus toru- losus with n e w data (particularly the s y n l o p h e ) and c o m p a r e the histological findings with those already reported b y other authors.
MATERIAL AND METHODS
MATERIAL
O
ut o f six Cebus apella L., 1758, caught b e t w e e n 12 July and 7 August 1992, five w e r e adults and parasitized by nematodes; only the young o n e was negative. O n e Cebus olivaceus Schumburg, 1848, caught on 20 July was also parasitized by n e m a - todes.Parasite. 2001, 8, 53-60
Mémoire 53
Article available athttp://www.parasite-journal.orgorhttp://dx.doi.org/10.1051/parasite/2001081053
DURETTE-DESSET M.-C. FRIBOURG BLANC L.A. & VUONG P.N.
MORPHOLOGICAL STUDY
All o f these m o n k e y s w e r e dissected. In this p a p e r w e study only the Trichostrongyles that dwelt in cysts d e v e l o p e d alongside the d u o d e n u m and the jejunum.
T h r e e cysts w e r e o p e n e d and the n e m a t o d e s c o l l e c t e d and stored in 7 0 % ethanol. N e m a t o d e s w e r e studied in temporary w e t mounts in water and, w h e n n e c e s sary, cleared in lactophenol. Measurements o f 10 males and 10 females are given in micrometres e x c e p t w h e r e otherwise stated. T h e n o m e n c l a t u r e used a b o v e the family-group is that o f D u r e t t e - D e s s e t & C h a b a u d ( 1 9 9 5 ) . T h e s y n l o p h e w a s s t u d i e d f o l l o w i n g t h e m e t h o d o f Durette-Desset ( 1 9 8 5 ) , and the n o m e n c l a ture used for the study o f the caudal bursa is that o f Durette-Desset & Chabaud ( 1 9 8 1 ) . V o u c h e r s p e c i m e n s w e r e deposited in the Helminthological Collections o f the Muséum national d'Histoire naturelle, Paris, France (MNHN).
T h e nomenclature concerning the hosts follows Wilson
& Reeder, 1 9 9 3 .
HISTOLOGICAL STUDY
Samples o f intestine harboring cysts w e r e fixed in 10 % formalin, p r o c e s s e d for paraffin. Histological sections, five m i c r o m e t r e s thick, w e r e stained with H a e m a - toxylin-Eosin-Saffron.
RESULTS
MORPHOLOGY OF MOLINEUS TORULOSUS (MOLIN, 1 8 6 1 )
Studied material: 12 males, 12 females, MNHN 4 7 5 K Q extracted from o n e cyst.
Host: Cebus apella L., 1 7 5 8 ( C e b i d a e , Primates).
Site: o n e cyst located in the anterior pan o f the jejunum.
Geographical origin: French Guyana (Camopi), 7 august 1992.
Redescription
N e m a t o d e s with b o d y uncoiled. P r e s e n c e o f circular e x c r e t o r y furrow, not surrounded by cuticular e x p a n sions (Fig. 2 A, C). Excretory pore situated at s a m e level as furrow, deirids situated posterior to furrow (Fig. 2 C).
Head: Cephalic vesicle present. In apical view, rounded b u c c a l o p e n i n g surrounded b y two small amphids, six e x t e r n o lateral papillae and four c e p h a l i c papillae (Fig. 2 B ) .
Synlophe: (studied in o n e male and t w o females). In both s e x e s , cuticle bears uninterrupted ridges. Dorsal ridges and lateral ridges appearing posterior to cephalic- vesicle (Fig. 1 A), ventral ridges just posterior to e x c r e
tory pore (Fig. I B ) Ridges disappearing just anterior to caudal bursa in male and at caudal extremity in female (Fig. 2L)
Number o f ridges varying along body. In b o t h s e x e s , n u m b e r i n c r e a s i n g from s e v e n ( t h r e e dorsal, four lateral) posterior to cephalic vesicle (Fig. 1A) to 12 (five dorsal, four lateral, three ventral) at level o f deirids (Fig. I B ) to 14 (five dorsal, four lateral, five ventral) at level o f oesophago-intestinal junction. (Fig. 1C). In male, this n u m b e r remaining constant along first third o f b o d y (Fig. I D ) . T h e n , n u m b e r o f ridges reaching 16 (six dorsal, four lateral, six ventral) at mid-body (Fig. I E ) and remaining constant until level o f caudal bursa (Fig. I F ) . In female, posterior to level o f o e s o phago-intestinal junction, (Fig. 1 G ) , n u m b e r o f ridges varying a c c o r d i n g to the level b e t w e e n 18 ( s e v e n dorsal, s e v e n ventral, four lateral) within first third to 14 (five dorsal, five ventral, four lateral) at mid-body (Fig. 1H). B e t w e e n mid-body to vulva level, n u m b e r varying b e t w e e n 16 (five dorsal, s e v e n ventral, four lateral) to 17 with an extra dorsal ridge.
Ridges regularly s p a c e d e x c e p t t h o s e o p p o s i t e lateral fields which are close to o n e another. Ridges orien
tated perpendicularly to b o d y surface (Fig. 1A-H).
Males: 8. 9 ( 7 . 9 - 9 . 7 ) m m long and 168 ( 1 4 5 - 1 8 7 ) wide at mid-body; cephalic vesicle 4 4 ( 4 0 - 4 8 ) long by 5 6 ( 5 2 - 6 5 ) w i d e ; n e r v e ring, e x c r e t o r y p o r e and deirids situated at 2 1 4 ( 1 8 5 - 2 4 0 ) , 2 5 6 ( 2 3 0 - 2 8 5 ) and 287 ( 2 6 0 - 3 0 5 ) from apex, respectively; oesophagus 532 ( 4 6 0 - 5 9 5 ) long (Fig. 2A).
Symmetrical caudal bursa with pattern o f type 2-1-2, not spiny o n lateral l o b e s (Fig. 2 H ) . Rays 4 short with extremities at a b o u t s a m e distance as b e t w e e n t h o s e o f rays 3 and rays 5. Rays 8 arising from proximal third o f dorsal ray, shorter than latter. Dorsal ray divided into t w o b r a n c h e s at its distal extremity, e a c h giving rise to three small b r a n c h e s , firstly e x t e r n a l b r a n c h e s (rays 9 ) then phasmids and rays 10 (internal b r a n c h e s ) .
Spicules alate, 178 ( 1 7 2 - 1 8 0 ) long, with handle sligthly shorter than blade. B l a d e divided first into three bran
c h e s : o n e e x t e r n o lateral b r a n c h a n d t w o internal b r a n c h e s . T h e externo-lateral b r a n c h is thickest and longest. T h e three b r a n c h e s sharp and inclused in m e m b r a n e (Fig. 2 D - F ) . C o n e genital very discret with two small papillae 7. Papilla zero not observed. Guber- naculum rectangular in s h a p e in ventral view, sligthly curved in lateral view with proximal h o o k , 111 ( 1 0 8 - 1 1 5 ) long and 10 wide (Fig. 2I-K).
Females: 11.6 ( 1 0 . 0 - 1 2 . 3 ) mm long and 167 ( 1 4 0 - 1 9 5 ) wide at mid-body; c e p h a l i c vesicle 4 4 ( 4 0 - 4 5 ) long by 57 ( 5 0 - 6 5 ) wide; nerve ring, e x c r e t o r y p o r e and dei
rids situated at 2 0 8 ( 1 8 5 - 2 5 0 ) , 251 ( 2 3 5 - 2 9 0 ) , 2 9 3 ( 2 7 5 - 3 4 0 ) from apex, respectively; oesophagus 545 ( 4 6 0 - 6 3 0 ) long.
Mémoire Parasite, 2001, 8, 53-60
54.
MOULINEUS TORULOSUS: NEW MORPHOLOGICAL AND HISTOLOGICAL DATA
Fig. 1. - Molineus lorulosus (Molin, 1861) in Cebus apella. Synlophe. A-F, Male 8.5 mm long. A. at excretory pore level. B . at left deirid level. C. at oesophhago-intestinal junction. D. at 3.2 mm from head. E, at mid-body. F. at 1.2 mm above caudal bursa. G. H. Female 11.7 mm long. G, at oesophago-intestinal junction. H, at mid-body.
The transversal sections are orientated as A.
Abbreviations: d = dorsal side; de : deirid ; g = left side.
Scales: A-C, 30 um ; D-F, 50 um : G. H. 100 um.
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D U R E T T E - D E S S E T M . - C , F R I B O U R G B L A N C L A . & V U O N G P . N .
Fig. 2. - Molineus toralosus (Molin, 1861) in Cebus apella . A, male, anterior extremity, ventral view. B, male, head, apical view. C, male, detail of the furrow, the exretory pore and the deirids, ventral view. D-F, male, right spicule, D. ventral view, E, dorsal view, F, interno- lateral view. G, female, ovejector, left lateral view. H, male, caudal bursa, ventral view. I-K, gubernaculum. 1. right lateral view, J . ventral view, K, left lateral view. L, female, tail, right lateral view.
Abbreviations: de = deirid; elb: externo-lateral branch; idb: interno-dorsal branch; ivb: interno-ventral branch.
Scales: A, 100 um ; B, 10 um ; C . H . 50 um; D-F, I-K, 30 um ; G, 150 vim ; L, 75 um.
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MOLINEUS TORULOSIS: NEW MORPHOLOGICAL AND HISTOLOGICAL DATA
Didelphic: vulva at 2.5 ( 2 . 2 - 2 . 9 ) from caudal extremity.
Vagina vera: 4 6 ( 4 2 - 5 0 ) long, divided vestibule into t w o equivalent parts; vestibule, 1.3 ( 1 . 2 - 1 . 4 ) m m long;
anterior sphincter and infundibulum 4 6 ( 3 5 - 6 5 ) and 3 6 ( 2 0 - 4 5 ) long, respectively; p o s t e r i o r s p h i n c t e r and infundibulum 4 5 ( 3 5 - 6 0 ) and 3 6 ( 2 0 - 4 5 ) long, r e s p e c tively (Fig. 2 G ) . Anterior uterine b r a n c h 1.6 ( 1 . 4 - 1 . 8 ) . Posterior uterine branch 1.5 ( 1 . 3 - 1 . 7 ) long. Each ute
rine b r a n c h with 5 0 to 1 0 0 eggs, morula stage 64 ( 5 8 - 7 5 ) long b y 3 4 ( 2 6 - 4 0 ) wide. Tail 129 ( 1 1 0 - 1 6 0 ) long with caudal spine 2 0 ( 1 5 - 2 8 ) l o n g ) (Fig. 2L).
HISTOLOGY
Grossly, the cystic formations w e r e o f variable size, the greatest m e a s u r i n g 0.7 c m in diameter, d e v e l o p e d alongside the external aspect o f the small intestine. His
tologically, the cysts d e v e l o p e d in the outermost part o f the intestinal wall, carved in the muscular layer and uplifting the intestinal serosa (Fig. 3 ) . In s o m e areas, the cysts c o m m u n i c a t e d with the intestinal lumen by a small channel. T h e cystic lumen presented an irregular contour. It was lined with inflammatory tissue made up o f numerous inflammatory cells: neutrophil leukocytes interspersed with lymphocytes and histiocytes (Figs 3, 4 ) . S o m e cysts contained adult w o r m s entsheathed in fibrinous material leading to Splendor Hoepli p h e n o m e n o n (Fig. 5 ) . According to the predominant inflam
matory cells in the wall, there w e r e three types o f cysts:
1°) Newly-formed cysts containing predominantly neu
trophils leukocytes. T h e cystic lumen was centered by a dozen intertwined worms. 2 ° ) Advanced cysts contai
ning fewer neutrophil leukocytes, more m o n o c y t e s and lymphocytes (Fig. 6). Adult worms w e r e less numerous.
Fibrotic strands starting at the periphery, penetrated the cyst lumen (Fig. 7 ) . 3°) Chronic old cysts having a lumen almost completely sealed by fibrotic tissue and devoid o f w o r m s (Fig. 8 ) . In the mesentery, s o m e veins displayed fibrinous thrombosis clogging the lumen with infiltration o f inflammatory cells in the surroun
ding adipose tissue (Fig. 9 ) .
DISCUSSION
F
our s p e c i e s b e l o n g i n g to the g e n u s Molineus w e r e parasites o f Neotropical primates: M. elegans (Travassos, 1 9 2 1 ) , o f Saimiri sciurea from Brazil;M. midas Durette-Desset & Corvione, 1 9 9 8 , o f Sangui- nus midas from F r e n c h G u y a n a a n d M. torulosus (Molin, 1 8 6 1 ) o f Cebus capucinus from Brazil w e r e found in the small intestine. M. vexillarius Dunn, 1 9 6 1 , a parasite o f Tamarinus nigricollis from Peru w a s found in the stomach.
T h e n e m a t o d e s described b e l o w can easily b e identi
fied with Molineus torulosus sensu Molin, 1861 nec
Cameron, 1 9 2 3 , redescribed by Travassos in 1937: the caudal bursa lacks spiny lateral lobes; the length o f rays 4 is about 4 0 % o f that o f rays 3 versus m o r e than 55 % in the o t h e r three s p e c i e s ; rays 8 are longer than the dorsal ray. In addition, M. tondosus is the sole spe
cies to have a location in the cysts. T h e host-spectrum is m a d e u p o f only s p e c i e s o f Cebus distributed throu
ghout the septentrional part o f South America: Cebus capucinus from Brazil, region not precised (Molin, 1 8 6 1 ) , Mato grosso (Travassos, 1 9 3 7 ) , S. J o a o , Mato Grosso, Rio de J a n e i r o ( R e g o & Schaeffer, 1987); Cebus apella from Brazil, Mato G r o s s o (Travassos, 1 9 3 7 ) , Salobra, Mato grosso, Linhaeres, Esperito Sancto ( R e g o
& Schaeffer, 1 9 8 7 ) F r e n c h Guyana (this w o r k ) ; Cebus apella from Argentina, C h a c o B o r e a l (Mazza, Parodi &
Brian, 1930 ; Cebus olivaceus from French Guyana (this w o r k ) ; Cebus sp. from Brasil, Manaus, A m a z o n a s . B r a c k et al. ( 1 9 7 3 ) , B r a c k ( 1 9 7 6 ) studied the lesions o f M. torulosus in Cebus apella but they did not spe
cify the geographical origin o f the m o n k e y s .
From the pathological standpoint, the morphological patterns o f the cysts w e r e very similar to those pre
viously described by other authors in Capucin mon
k e y s (Schwartz, 1 9 2 8 , Brack, 1 9 7 6 , R e g o & Schaeffer, 1 9 8 7 ) . T h e s e cysts w e r e d e e p l y carved in the outer
most part o f the muscular layer and the serosa o f the small intestine. Identical findings w e r e also recorded in gazelles with Gazellostrongylus lerouxi, Y e h , 1 9 5 6 (Khalil & Ingram, 1 9 8 1 ) .
In our opinion, the turn out o f the cyst walls corres
p o n d e d to the three-staged inflammatory reaction:
acute, sub-acute and chronic. T h e larvae penetrated the intestinal wall and induced cyst formation alongside the external part o f the muscular layer or at the junction o f the muscular layer and the serosa. T h e s e cavities c o m m u n i c a t e d with the intestinal lumen through a n a r r o w c h a n n e l . T h e mature larvae b e c a m e adult worms, copulated and laid eggs. Adult w o r m s w e r e assumed to reside permanently in the cyst lumen as their p r e s e n c e had n e v e r b e e n e v i d e n c e d in the intes
tinal lumen. Only laid eggs w e r e released in the intes
tinal lumen through the channel w h o s e diameter might b e t o o small to let the adult w o r m s pass through. Free eggs h a t c h e d and p r o m o t e d the developmental cycle.
S p l e n d o r e Hoepli p h e n o m e n o n e v i d e n c e d in cysts containing w o r m s was a camouflage mechanism o f the parasites against the host i m m u n e reaction. This phe
n o m e n o n was not specific to Molineus as it had also b e e n noted in other parasitic diseases. ( V u o n g et al., 1993, 1 9 9 4 , 1 9 9 6 ) . With time, the inflammatory reac
tion w a n e d and the lesion underwent scarring. T h e cystic wall b e c a m e less cellular and m o r e fibrotic.
Mature worms degenerated and died w h e n the c o n n e c tive tissue sealed the cystic lumen. T h e s e s c h a n g e s w e r e similar to the findings noted in gazelles (Khalil
Parasite, 2001, 8, 53-60
Mémoire 57
DURETTE-DESSET M.-C, FRIBOURG BLANC L.A. & VUONG P.N.
Fig. 3. - Cyst carved alongside the external part of the intestinal wall. Arrow head: adult worms. L: intestinal lumen. S: serosa. Haema- toxylin-Eosin-Saffron (HES).
Fig. 4. - Adult worms surrounded by neutrophil leukocytes. HES.
Fig. 5. - Fnsheathed adult worms in fibrinous debris (asterisk) among the inflammatory infiltrate containing neutrophil leukocytes. HES.
Fig. 6. - Advanced cysts with starting fibrosis (star) developed at the periphery. HES.
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MOLINEUS TORULOSUS: NEW MORPHOLOGICAL AND HISTOLOGICAL DATA
Fig. 7. - Advanced cyst with fibrosis strands (stars) pene
trating the cyst lumen. HES.
Fig. 8. - Cyst sealed by fibrotic tissue (star). HES.
Fig. 9. - Mesenteric veins (arrow) displaying occluding thrombosis and phlebitis. HES.
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Mémoire 59
DURETTE-DESSET M.-C, FRLBOURG BLANC L.A. & VUONG P.N.
& Ingram, 1 9 8 1 ) . Vascular c h a n g e s m a y also o c c u r around the cysts o r in the mesentery. T h e e g g s acci- dentaly laid inside the capillaries and t h e veins sur- rounding the cysts c o u l d probably induce t h r o m b o - phlebitis o b s e r v e d in m e s e n t e r i c veins.
AKNOWLEDGEMENTS
T
h e authors are grateful to the ethnologists Drs.F r a n ç o i s e G r e n a n d (CNRS) a n d Pierre G r e n a n d ( I R D ) , Guyana Indian specialists for their help in the field.
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Reçu le 6 octobre 2000 Accepté le 13 janvier 2001
60 Mémoire Parasite, 2001, 8, 53-60
