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Bull. Mus. natn. Hist, nat., Paris, 4 sér., 8, 1986,


section A , n° 3 : 543-550.

Witenbergitaenia sinaica gen. n., sp. n. (Anoplocephalidae)


and other Cestodes from small Mammals
in Israel and in the Sinai Peninsula
by G u t a WERTHEIM, Gerald D. SCHMIDT and Zalman GREENBERG

Abstract. — Twelve species of Cestodes are reported from twenty species of small mammals reco-
vered in Israel and Sinai. Eight other adult Cestodes were identified to genus only. New host and
locality records are indicated in table 1 a n d in the text. Witenbergitaenia sinaica gen. n . , s p . n . ,
found in Acomys cahirinus in southern Sinai, differs from Markewitchitaenia and Tupaiataenia, the
only other genera in Anoplocephalidae with a hermaphroditic canal, in having two postovarian fields
of testes.
Résumé. — Witenbergitaenia sinaica n. g., n. sp. (Anoplocephalidae) et autres Cestodes parasites
de petits Mammifères d'Israël et de la péninsule du Sinaï. — Douze espèces de Cestodes o n t été trou-
vées chez vingt espèces de petits mammifères récoltés en Israël et dans la péninsule du Sinaï. Huit
autres Cestodes adultes ont été identifiés seulement j u s q u ' a u niveau générique. Les nouveaux hôtes et
les nouvelles localités sont indiqués dans le tableau 1 et dans le texte. Witenbergitaenia sinaica n. g.,
n. s p . , récoltée chez Acomys cahirinus dans le sud du Sinaï, diffère de Markewitchitaenia et de
Tupaiataenia, les seuls autres genres d'Anoplocephalidae possédant u n canal hermaphrodite, par la
présence de deux champs de testicules postovariens.

G . WERTHEIM, Laboratory of Helminthology, the Hebrew University-Hadassah Medical School, Jerusalem, Israel.
Temporary adress : Professeur Associée, Laboratoire de Zoologie (Vers) associé au CNRS, Muséum national
d'Histoire naturelle, 61, rue Buffon, F 75231 Paris, France.
G . D. SCHMIDT, Department of Biology, University of Northern Colorado, Greeley, Co. 80639, USA.
Z. GREENBERG, Laboratory of Helminthology, the Hebrew University-Hadassah Medical School, Jerusalem, Israel.
Present adress : Ministry of Health, Government Central Laboratories, P.O. Box 6115, Jerusalem, Israel.

INTRODUCTION

In a previous publication (SCHMIDT, GREENBERG and WERTHEIM, 1986) s u r v e y d a t a on


a v i a n C e s t o d e s w e r e r e p o r t e d a s well a s i n f o r m a t i o n o n c o l l e c t i o n sites a n d t e c h n i q u e s u s e d
in p r o c e s s i n g a n d m o u n t i n g t h e s p e c i m e n s . T h e p r e s e n t c o m m u n i c a t i o n d e a l s w i t h C e s -
todes recovered from small m a m m a l s , mostly r o d e n t s .
T h e earliest findings o n C e s t o d e s , published with t h e initiation o f helminthological stu-
die s in I s r a e l ( t h e n P a l e s t i n e ) , d e a l t w i t h t h e f a u n a o f d o m e s t i c a n d w i l d c a r n i v o r e s p o s s i b l y
b e c a u s e of t h e i m p o r t a n c e of these a n i m a l s as a s o u r c e of h u m a n infections. In stray dogs
a n d c a t s , W I T E N B E R G ( 1 9 3 2 , 1 9 3 3 , 1 9 3 4 a , b) f o u n d five s p e c i e s o f D i l e p i d i n a e , o n e s p e c i e s
o f M e s o c e s t o i d i d a e ( g e n u s Mesocestoides) a n d five species o f T a e n i i d a e , a m o n g t h e m Echi-
— 544 —

nococcus granulosus ( r e c o r d e d a l s o f r o m t h e j a c k a l Canis aureus). F r o m the presence of


s o m e o f t h e s e t a e n i i d s o n e c o u l d infer t h a t t h e i r l a r v a l f o r m s will b e f o u n d in r o d e n t s o r
other small m a m m a l s . This w a s later proven when extensive studies of these animals were
undertaken. C y s t i c e r c u s o f T. taeniaeformis, for e x a m p l e , w a s r e p o r t e d from rats ( W E R -
THEIM, 1 9 6 3 ) a n d f r o m Nesokia indica, Rodentia-Muridae (GREENBERG, 1 9 7 2 ) . Other
c e s t o d e s f r o m r o d e n t s , s o f a r r e p o r t e d i n c l u d e Megittina gerbilli, Hymenolepis diminuta and
Vampirolepis nana ( W E R T H E I M , 1 9 5 4 , 1 9 6 3 ) . Vampirolepis negevi (= Rodentolepis negevi),
Pseudandrya monardi a n d Mathevotaenia symmetrica ( r e p o r t e d a s M. rodentinum) (GREEN-
B E R G , 1 9 6 9 ) ; Sinaiotaenia witenbergi (WERTHEIM and GREENBERG, 1 9 7 1 ) and Paranoploce-
phala sp. (WERTHEIM and NEVO, 1971).
T h e present paper summarizes findings from examination of over t w o t h o u s a n d small
m a m m a l s a s well a s n e w h o s t a n d l o c a l i t y r e c o r d s . A l l l o c a l i t y r e c o r d s f r o m S i n a i a r e
new. I n t h e d a t a o n f o u r s p e c i e s o f C e s t o d e s f r o m r o d e n t s i n S i n a i p r e s e n t e d in a p r e v i o u s
report (WERTHEIM a n d GREENBERG, 1 9 7 0 ) only t h e hosts a r e listed.

RESULTS

C e s t o d e s i d e n t i f i e d in t h i s s t u d y , a s well a s d a t a o n h o s t s a n d l o c a l i t i e s , a r e s u m m a -
r i z e d in t a b l e 1 . C l a s s i f i c a t i o n f o l l o w s S C H M I D T ( 1 9 8 6 ) . M e a s u r e m e n t s a r e in m i c r o m e t e r s
unless otherwise stated. T h e letter n indicates t h e n u m b e r of m e a s u r e m e n t s m a d e . O n e
s p e c i e s is r e c o g n i z e d a s n e w a n d a s r e p r e s e n t i n g a n e w g e n u s . W e p l a c e it w i t h i n t h e L i n -
s t o w i i n a e b e c a u s e t h e eggs l a c k a p y r i f o r m a p p a r a t u s a n d t h e r e is o n l y o n e e g g p e r c a p s u l e .

DESCRIPTION

WITENBERGITAENIA gen. n.

DIAGNOSIS : Anoplocephalidae, Linstowiinae. Dorsoventrally flattened, becoming wider evenly


toward the gravid segments. Immature segments wider than long, mature segments about as long as
wide, gravid segments longer than wide. Scolex lacking rostellum, hooks or apical organ. Suckers
r o u n d , powerful, u n a r m e d . Neck present, narrower than scolex. Proglottids n u m e r o u s , slightly cras-
pedote. Osmoregulatory canals reticulated throughout proglottid. This canal system is identical with
that described for Atriotaenia procyonis (Chandler, 1 9 4 2 ) , by GALLATI ( 1 9 5 9 ) , to which the reader is
referred. Muscle bundles feebly developed. One set of reproductive organs per segment ; genital
pores irregularly alternating. Genital atrium well developed, lacking sphincter muscles, smaller than
cirrus pouch. Genital ducts dorsal to osmoregulatory canals. Testes in two lateral fields, mainly
postovarian, some lateral to ovary, between outer limits of osmoregulatory canals. Cirrus pouch
elongate, crossing outermost osmoregulatory canals, usually reaching poral edge of ovary. Cirrus
absent. Internal and external seminal vesicles absent. Ovary median, with bilateral wings subdivided
into slender lobes. Vitellarium with small lobes, posterior to ovary. Vagina posterior to cirrus
p o u c h . Distal end of vagina entering, with cirrus pouch, into c o m m o n hermaphroditic canal that
enters genital atrium. Seminal receptacle small, remaining discrete in gravid segments. Uterus deve-
— 545 —

lops as a thin-walled, reticular sac, which quickly fills and disappears, leaving abundant developing
eggs evenly scattered throughout the medullary parenchyma. Oncospheres each surrounded by a
single, thin-walled membrane ; pyriform apparatus absent.

TYPE SPECIES : Witenbergitaenia sinaica sp. n.

W i t e n b e r g i t a e n i a sinaica s p . n .
( F i g . 1, A t o D )

MATERIAL STUDIED : O n e specimen found in 1 out of 152 host-animals examined.

DESCRIPTION

W i t h t h e c h a r a c t e r s o f t h e g e n u s , a s d e s c r i b e d a b o v e . S c o l e x ( f i g . 1A) a b o u t 4 8 0 l o n g
(measured t o posterior constriction of scolex), 640 greatest width. S u c k e r s r o u n d , 175 t o
2 0 0 w i d e . N e c k n a r r o w e r t h a n s c o l e x , a b o u t 1.0 m m l o n g . S t r o b i l a 71 m m l o n g
( a l t h o u g h a s m u c h a s o n e - f o u r t h m a y b e m i s s i n g i n t h e p r e p a r e d s l i d e ) , a b o u t 1.5 m m w i d e
in m a t u r e p o r t i o n , 2 . 0 m m w i d e i n g r a v i d s e g m e n t s . P r o g l o t t i d s slightly c r a s p e d o t e , a n a -
p o l y t i c . M a l e a n d f e m a l e g o n a d s (fig. I B ) m a t u r e a t s a m e t i m e . G e n i t a l d u c t s d o r s a l t o
o s m o r e g u l a t o r y canals (fig. 1 C ) .

Male genitalia : 41 t o 6 2 t e s t e s (n = 7) i n t w o fields o f 2 3 t o 2 9 ( p o r a l ) a n d 18 t o 3 3


( a p o r a l ) , m a i n l y p o s t e r i o r t o o v a r y . T e s t e s (n = 2 3 ) 6 0 t o 100 w i d e i n m a t u r e s e g m e n t s .
C i r r u s p o u c h (fig. 1 C ) (n = 7) e l o n g a t e , n a r r o w e d p r o x i m a l l y , u s u a l l y r e a c h i n g b u t n o t
exceeding poral margin of ovary, 240 t o 270 long, 60 greatest width. Internal a n d external
s e m i n a l vesicles a b s e n t . Ejaculatory duct a n d vas deferens coiled. Cirrus absent.

Female genitalia : Ovary m e d i a n , with bilateral wings subdivided into lobules ; n o t reach-
i n g m a i n l a t e r a l o s m o r e g u l a t o r y c a n a l s ; m a x i m u m size (n = 7) 3 4 5 t o 4 8 0 l o n g , 5 6 0 t o
6 8 0 w i d e . V i t e l l a r i u m (n = 7) p o s t e r i o r t o o v a r y , l o b a t e d , 160 t o 2 0 0 l o n g , 175 t o 255 g r e a -
test width. V a g i n a posterior t o cirrus p o u c h , u n a r m e d , proceeding directly t o seminal
r e c e p t a c l e , w h i c h lies b e t w e e n o v a r y a n d v i t e l l a r i u m . S e m i n a l r e c e p t a c l e (n = 7) a s i m p l e
s a c 120 t o 140 l o n g , 6 0 t o 9 0 w i d e in m a t u r e s e g m e n t s , s l e n d e r w i t h a single l o o p in g r a v i d
segments. Distal e n d of vagina joins h e r m a p h r o d i t i c duct with cirrus p o u c h before opening
into genital a t r i u m . A t r i u m ( n = 7) 7 0 d e e p , 2 0 t o 3 0 w i d e a t d i s t a l e n d , 10 w i d e a t b a s e ,
not exceptionally muscular or glandular. E g g s ( f i g . I D ) s u r r o u n d e d b y single m e m b r a n e ,
5 4 t o 6 4 w i d e (n = 10). O n c o s p h e r e s 3 0 t o 4 0 w i d e ; o n c o s p h e r e h o o k s 14 t o 16 l o n g .

[
TYPE HOST : Egyptian spiny mouse, Acomys cahirinus Desm., 1819. Rodentia, Muridae.
LOCATION : Small intestine.
LOCALITY : Wadi Atzvira (Southern Sinai).
TYPE SPECIMEN : M N H N (Museum national d'Histoire naturelle, Paris) holotype n° 641 H B .
ETYMOLOGY : T h e genus is named in h o n o r of the late Professor George WITENBERG, w h o pio-
neered in helminthology in Israel.

1. In a previous publication (WERTHEIM and GREENBERG, 1 9 7 0 ) the Acomys from Sinai was temporarily
named A. dimidiatus. Professor WAHRMAN informs us (personal communication) that at a later date, it was
chosen, for the time being, to use the name A. cahirinus for all the chromosomal forms.
— 546 -

FIG. 1. — Witenbergitaenia sinaica sp. n. from Acomys cahirinus : A , scolex ; B , mature proglottid ; C, terminal
genital ducts ; D , egg.

DISCUSSION

T o d a t e t h e r e a r e t w o g e n e r a in t h e a n o p l o c e p h a l i d s u b f a m i l y L i n s t o w i i n a e w i t h a c o m -
m o n h e r m a p h r o d i t i c c a n a l a s in t h e p r e s e n t s p e c i e s : Markewitchitaenia Sharpilo and
K o r n y u s h i n , 1 9 7 5 , a n d Tupaiataenia S c h m i d t a n d F i l e , 1 9 7 5 . Tupaiataenia, from tree
s h r e w s , is u n i q u e in p o s s e s s i n g a c i r r u s a n d m u s c u l a r l a p p e t s o n t h e s u c k e r s .
T h e p r e s e n t s p e c i e s is m o s t s i m i l a r t o Markewitchitaenia b u t c l e a r l y d i f f e r s f r o m it i n
h a v i n g t w o l a t e r a l fields o f l a r g e t e s t e s , i n s t e a d o f a single field o f s m a l l t e s t e s .
— 547 —

B e c a u s e t h e p r e s e n c e o f t w o fields o f t e s t e s v e r s u s o n e field h a s t r a d i t i o n a l l y b e e n
a c c e p t e d a s a g e n e r i c c h a r a c t e r ( a s i n Kowalewskiella, Schizorchis, Cycloskrjabinia, Latero-
taenia a n d m a n y o t h e r s ) w e p r o p o s e o u r n e w species t o r e p r e s e n t a n e w g e n u s a n d n a m e it
Witenbergitaenia.
I n o r d e r t o s h o w t h a t W. sinaica is n o t a d e v i a n t M. rodentinum ( J o y e u x , 1927) — t h e
o n l y species in Markewitchitaenia — t h e f o l l o w i n g c o m p a r i s o n s a r e g i v e n : (1) t h e g r a v i d
s t r o b i l a o f M. rodentinum is a b o u t 4 4 m m l o n g b y 7 1 0 / u n g r e a t e s t w i d t h , c o m p a r e d w i t h
a t least 7 0 m m l o n g b y 2 . 0 m m g r e a t e s t w i d t h in W. sinaica ; (2) t h e c i r r u s p o u c h o f
M. rodentinum is 137 t o 154 / u n l o n g b y 33 t o 3 8 / u n w i d e a n d r e a c h e s t h e m i d l i n e level o f
t h e o v a r y , w h i l e t h a t o f W. sinaica is 2 4 0 / u n l o n g b y 6 4 / u n w i d e a n d b a r e l y r e a c h e s t h e
p o r a l e d g e o f t h e o v a r y ; (3) t h e t o t a l n u m b e r o f t e s t e s is 33 t o 4 7 ( u s u a l l y 3 8 t o 4 0 ) in
M. rodentinum, c o m p a r e d w i t h 4 1 t o 6 2 in W. sinaica. T h u s it is c l e a r t h a t t w o d i f f e r e n t
species a r e r e p r e s e n t e d .

Acknowledgments

The authors wish to express their gratitude to P r Y . SCHLEIN, Department of Parasitology, T h e


Hebrew University-Hadassah Medical School, for his help in collecting the animals. T h a n k s are d u e
to Mrs H e r m i n a ZYLBERMAN, M r s Simona R A D A I , M r M . MUALLEM a n d M r Y . GATTAS for technical
assistance.
G . W . , o n sabbatical leave from the Hebrew University, wishes t o express her appreciation t o t h e
Department of Biological Sciences, University of Northern C o l o r a d o , for its cooperation a n d hospita-
lity during the period of this research.

TABLE 1. — Cestodes from small mammals of Israel a n d Sinai.

HOST CESTODE LOCALITY *HUJP


Vaucher n o .

Acomys cahirinus Desm., 1819 Hymenolepis diminuta (Rudolphi, Bar Giyora, Zova 1943
1819)
Witenbergitaenia sinaica gen. n . , t Wadi Atzvira S140
sp. n.
***Mathevotaenia symmetrica (Bay- Elat, t Sharm el Sheikh, S211
lis, 1927) f W a d i Azvira, t Wadi
Latai, t Wadi Ajar
Mathevotaenia sp. Timna 2025
Pseudandrya monardi F u h r m a n n , Jerusalem, **Bet Alpha, 232
1943 Ein F a r ' a
Tetrathyridium Jerusalem, Zova, Dimona,
Ein Hussub, t Mitla
Pass, t Monastery of
St. Catherine, t Wadi
Kid, t Wadi Abu G'eada
Vampirolepis nana (Siebold, 1852) Jerusalem, t Monastery of S275
St. Catherine
— 548 —

HOST CESTODE LOCALITY *HUJP


Vaucher n o .

Vampirolepis negevi (Greenberg, Elat, Yotvata, Wadi Mé- 2039


1969) nayeh, t Dahab | E 1
Tur, t Ras Nusrani,
f Wadi Isla, t Wadi Kid
Acomys russatus W a g n e r , Tetrathyridium Masada
1840
Apodemus mystacinus Danf. Paranoplocephala sp. **Ein Hemed 524A
and Alst., 1877
Taenia taeniaeformis (Batsch, 1786) """Jerusalem, **Ein He-
strobilocercus med
Gerbillus (Dipodillus) dasyu- Meggittina gerbilli (Wertheim, 1954) **Elat, " J e r u s a l e m , f Ge- 1956
rus Wagner, 1842 bel A b u Z a r u b , t M o -
nastery of St. Cathe-
rine, t Wadi A b u G'ea-
da
Sinaiotaenia witenbergi Wertheim t Gebel Yi'allaq S486
and Greenberg, 1971
Taenia sp. coenurus Ein Hazeva
Tetrathyridium t Gebel Yi'allaq
Gerbillus allenbyi T h o m a s , ***Raillietina (R.) trapezoides (Ja- **Herzliya, **Caesarea 854A
1918 nicki, 1904)
Gerbillus gerbillus Olivier, Mathevotaenia symmetrica t A b u Rudeis, f El T u r , S53
1801 tNabq
***Meggittina gerbilli **Be'er S h e v a , t M i t l a 2203
Pass
***Raillietina (R.) trapezoides **Be'er Sheva
Sinaiotaenia witenbergi t Wadi Nafk
***Taenia pisiformis (Bloch, 1780) f A b u Zenima, t Bir Gaf- S65
cysticercus gafa
Gerbillus pyramidum Geof- ***Mathevotaenia symmetrica t Ras Sudar, t Sharm el S386
froy, 1825 Sheikh
Meggittina gerbilli Be'er Sheva, Holon, **Pal- 862
m a c h i m , **Rishon le
Ziyon, t Bir Gafgafa
***Raillietina (R.) trapezoides Be'er Sheva, **Hadassim,
**Holon, **Palmachim,
**Rishon le Ziyon
Taenia taeniaeformis strobilocercus **Holon 81
Jaculus jaculus L., 1758 ***Raillietina (R.) trapezoides t Sabkhet el Bardawil, S489
t El'Arish
Meriones crassus Sund., 1842 ****Hymenolepis sp. Wadi Taiyiba S288
***Meggittina gerbilli t Mitla Pass S470
***Raillietina (R.) trapezoides **Nizana 1608
Sinaiotaenia witenbergi t Mitla Pass, t Wadi Ak- S470
dar
***Taenia sp. polycephalus cyst **Ein Yahav
Tetrathyridium t Mitla Pass
Meriones sacramenti Thomas, Hymenolepis diminuta Holo n 857
1922
***Raillietina (R.) trapezoides H o l o n , Palmachim, **Ne- 858
bi Rubin
— 549 —

HOST CESTODE LOCALITY *HUJP


Vaucher n o .

Meriones tristrami T h o m a s , Hymenolepis diminuta **Mishmar H a ' E m e k 19


1892 ****Hymenoiepis sp. Mishmar H a ' E m e k 465
***Raillietina (R.) trapezoides **Mishmar H a ' E m e k 37
***Vampirolepis nana **Mishmar H a ' E m e k 16
***Taenia pisiformis Cysticercus **Mishmar H a ' E m e k 8
Tetrathyridium Akko
Microtus guentheri Danf. and ****Andrya sp. Mishmar H a ' E m e k 105
Alst., 1880
Mus musculus L., 1758 Vampirolepis nana Mishmar H a ' E m e k 290
Catenotaenia pusilla (Goeze, 1782) **Aminadav 511A
Nesokia indica G r a y and Hymenolepis diminuta Jericho 2204
H a r d w . , 1832 Taenia taeniaeformis strobilocercus Jericho
Procavia capensis Pallas, 1766 ****Inermicapsifer sp. Gilboa 1657
Psammomys obesus Cretzmar, ***Raillietina (R.) trapezoides **Jericho
1828
Rat tus rat tus L., 1758 Hymenolepis diminuta Tel Aviv, **Rosh Pina 1642
Vampirolepis nana **Rosh Pina
Rat tus norvegicus Berk, 1769 Hymenolepis diminuta Haifa, Tel Aviv (ports)
Taenia taeniaeformis strobilocercus Tel Aviv
Vampirolepis nana Haifa, Tel Aviv (ports)
Sekeetamys calurus T h o m a s , ****Hymenolepis s p . Gebel Abu Zrur S382
1892 Hymenolepis sp. (juv.) t Gebel Sorbal S66
Sinaiotaenia witenbergi t Gebel el Tin, t Wadi el
Sheikh
***Taenia pisiformis Cysticercus **Wadi Milhek, t Gebel
Abu Zrur S382
Spalax ehrenbergi Nehring, ****Paranoplocephala sp. Kuneitra N24
1898

*HUJP : Hebrew University Jerusalem, Parasitológica! Collection,


t A site in the Sinai peninsula.
**New locality record in Israel.
***New host record.
****To be discussed in a later publication as it may represent a new species.

LITERATURE CITED

GALLATI, W. W . , 1959. — Life history, morphology and taxonomy of Atriotaenia (Ershovia) pro-
cyonis (Cestoda : Linstowiidae), a parasite of the raccoon. J. Parasit., 4 5 : 363-377.
GREENBERG, Z . , 1969. — Helminths of mammals and birds of Israel. I. Helminths of Acomys spp.
(Rodentia, Murinae). Israel J. Zool., 18 : 25-38.
— 1973. — Helminths of birds and mammals from Israel. IV. Helminths from Nesokia indica
Gray and Hardwicke, 1832 (Rodentia, Muridae). Israel J. Zool., 21 : 63-70.
SCHMIDT, G. D . , 1986. — H a n d b o o k of T a p e w o r m identification. C R C Press, Boca R a t o n , 675 p .
SCHMIDT, G. D . , and S . FILE, 1977. — Tupaiataenia quentini gen. et sp. n. (Anoplocephalidae : Lin-
stowiinae) and other tapeworms from the c o m m o n tree shrew, Tupaia glis. J. Parasit., 63 : 473-
475.
— 550 —

SCHMIDT, G . D . , Z. GREENBERG, and G . WERTHEIM, 1986. — Raillietina {Raillietina) a lectori sp. n.


e
and other avian Cestodes from Israel and Sinai. Bull. Mus. natn. Hist, nat., Paris, 4 ser., 8,
section A, (1) : 101-109.
SHARPILO, V. P . , and V. U. KORNYUSHIN, 1975. — A new genus of cestodes : Markewitchitaenia
gen. nov. (Cestoda, Linstowiidae). Parazity i Parazitozy Zhivotnych i Cheloveka, Kiev, USSR
« N a u k o v a D u m k a » : 217-222.
WERTHEIM, G . , 1954. — A new anoplocephalid cestode from the gerbil. Parasitology, 44 : 446-449.
— 1963. — Helminth parasites of the rat Rattus norvegicus from Haifa and Tel-Aviv. Bull. Res.
Coun. Israel, 10 E : 125-129.
WERTHEIM, G . , and Z. GREENBERG, 1970. — Notes on Helminth parasites of m y o m o r p h rodents from
Southern Sinai. J. Helminth., 44 : 243-252.
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