HELGOI.~NDER MEERESUNTERSUCHUNGEN
Helgol~inder Meeresunters. 37, 463-478
H e t e r o p h y i a s i s , an intestinal f l u k e i n f e c t i o n of m a n and
vertebrates transmitted by e u r y h a l i n e g a s t r o p o d s and
fish
H. T a r a s c h e w s k i
Universit~t Hohenheim, Abteilung Parasitotogie;
D-7000 Stuttgart 70, Federal Republic of Germany
ABSTRACT: Heterophyes heterophyes, a g e n t of h u m a n heterophyiasis in the Near East, is transmitted in marine lagoons a n d saline i n l a n d waters, w h e r e the e u r y h a l i n e i n t e r m e d i a t e hosts are
abundant. In Egypt, mullets, the p r e d o m i n a n t second i n t e r m e d i a t e hosts, are customarily c o n s u m e d
raw; thus m a n becomes infected easily. Symptoms of h u m a n infections are usually considered mild.
Mullets do not seem to b e affected by the m e t a c e r c a r i a e encysted in the muscles, w h e r e a s the
growth of the snail host Pirenella conica was found to b e e n h a n c e d due to the infestation by the
trematodes. In laboratory experiments, the flukes were found to b e well d e v e l o p e d in dogs, foxes
a n d cats, but failed to reach sexual maturity in several other potentially piscivorous m a m m a l s a n d
birds. In nature, dogs p r o b a b l y serve as t h e major reservoir hosts. Heterophyiasis is most p r e v a l e n t
in the Nile Delta, a h u g e b r a c k i s h w a t e r area w h i c h is d e n s e l y p o p u l a t e d by h u m a n s and,
consequently, also by dogs a n d cats. In the Far East, besides Heterophyes nocens, several other
heterophyids with marine or fresh-water life-cycles are k n o w n to infect humans.
INTRODUCTION
A t l e a s t 14 s p e c i e s of h e t e r o p h y i d t r e m a t o d e s a r e k n o w n f r o m t h e h u m a n i n t e s t i n e .
H u m a n s as d e f i n i t i v e h o s t s a r e a f f e c t e d a c c i d e n t a l l y , or o n a l a r g e s c a l e w h e r e f i s h is
c o n s u m e d r a w , s a l t e d , or i n s u f f i c i e n t l y c o o k e d ( c h i e f l y i n E a s t A s i a a n d i n S o u t h - E a s t
Asia).
A s t h e s e ' h u m a n " h e t e r o p h y i d s a r e t r a n s m i t t e d b y p r o s o b r a n c h g a s t r o p o d s of t h e
families Potamididae, Melaniidae, Pleuroceridae and Littorinidae - and subsequently
by fish with a similar habitat preference - several species are encountered along the
c o a s t s . Still, Cryptocotyle lingua, w h i c h w a s s h o w n to p a r a s i t i z e 6 % of t h e i n v e s t i g a t e d
E s k i m o s o n G r e e n l a n d ( B a b b o t e t al., 1961), is t h e o n l y s p e c i e s m a r i n e b i o l o g i s t s h a v e
p a i d a t t e n t i o n to a d e q u a t e l y .
Among the heterophyids with medical relevance the species most frequently
r e p o r t e d f r o m h u m a n s a r e l i s t e d i n T a b l e 1. A s h e t e r o p h y i d e g g s of d i f f e r e n t s p e c i e s m a y
b e v e r y s i m i l a r to e a c h o t h e r , i n f e c t i o n s c a n o f t e n b e d i a g n o s e d to t h e s p e c i e s l e v e l o n l y ,
b y m e d i c a l e x p u l s i o n of t h e f l u k e s or b y a u t o p s y . O n l y s u c h r e p o r t s a r e l i s t e d i n T a b l e 1.
M u l l e t s , Mugil cephalus for i n s t a n c e , a c t a s t h e m o s t i m p o r t a n t s e c o n d i n t e r m e d i a t e
h o s t s of Heterophyes s p p . , Pygidiopsis summa a n d Stellantchasmus falcatus ( T a b l e 1).
Metagonimus s p p . a n d Haplorchls yokogawal e n c y s t i n f r e s h w a t e r fish. A s m u l l e t s m a y
© Biologische Anstalt Helgoland, H a m b u r g
H. T a r a s c h e w s k i
464
Table 1. H e t e r o p h y i d a e most frequently reported from the h u m a n intestine
Fluke species
Snail hosts
H u m a n cases
reported from
Recent reports or reviews,
remarks
Heterophyes
heterophyes
(v. Siebold)
Stiles & Hassal
Near East:
Pirenella conica
(Potamididae)
H. nocens
Onji & Nishio
Cerithidea cingulata East Asia
( = Tympanotonus
micropterus]
(Potamididae)
Ito (1964); Yokogawa et al. (1965);
Seo et al. (1981). Often H, nocens
is considered a subspecies of
H. heterophyes
East Asia
Ito (1964); Yokogawa et al. (1965);
Seo et al. (1981)
Near East
v. Siebold (1852); Looss (1902);
Khalil (1937); Kuntz & C h a n d l e r
(1956a)
Pygidiopsis summa
Onji & Nishio
cingulata
Metagonim us
yokogawai
Katsurada
Semisulcospira
libertina
(Pleuroceridae)
Asia
Ito (1964); Yokogawa et al. (1965);
Seo et al. (1981}. Ito (1964): "The
incidence of Metagonimus in the
h u m a n body (in Japan) is
considered to b e ca 1%, a n d yet in
certain local areas the incidence
of tens percent is exhibited."
M. takahashfi
Suzuki
Semisulcospira
libertina
East Asia
Sakai (1962); Ito (1964). In recent
years generally accepted as a
species different from
M. yokogawai (Saito, 1973)
Stellantchasmus
falcatus
Onji & Nishio
Tarebia granifera
a n d other m e l a n i i d
snails
Asia, O c e a n i a
Ito (1964); Kagei et al. (1964);
T a n t a c h a m r u m & Kliks (1978)
Haplorchis
yokogawai
Katsuta
Asia
Melanoides
tuberculatus a n d
other m e l a n i i d snails
Cerithidea
Ito (1964); M a n n i n g & Lertprasert
(1970); M a n n i n g et al, (1971).
Africa (1938): " . . . not only the
most frequently e n c o u n t e r e d in
m a n in this country (Philippines)
but also the most frequently
associated with cardiac failure."
f r e e l y m i g r a t e b e t w e e n t h e s e a a n d f r e s h w a t e r , m e t a c e r c a r i a e of t h e ' c o a s t a l s p e c i e s '
may be carried into fresh water as well.
T h e a i m of t h i s p a p e r is to s u m m a r i z e t h e i n f o r m a t i o n o n t h e b i o l o g y a n d e c o l o g y of
H e t e r o p h y e s h e t e r o p h y e s (Fig. 1), t h e a g e n t of h u m a n h e t e r o p h y i a s i s ,
HOST
RECORDS
Definitive
hosts
H e t e r o p h y e s h e t e r o p h y e s w a s f o u n d i n E g y p t i n t h e h u m a n i n t e s t i n e for t h e first
t i m e i n 1851 (v. S i e b o l d , 1852). L a t e r on, t h e n u m b e r of a u t o p s i e s m e n t i o n e d is o n l y
Heterophyiasis
465
Fig. 1. Heterophyes heterophyes from intestine of a cat taken by a scanning electron microscope, os
= oral sucker; vs = ventral sucker; gt = gonotyl (genital sucker)
s c a r c e (Looss, 1902; Khalil, 1937). H o w e v e r , t h e f l u k e h a s b e e n f r e q u e n t l y d i a g n o s e d b y
c o p r o l o g i c a l d i a g n o s i s (Khalil, 1937; W e l l s & B l a g g , 1956; N a g a t h y & Khalil, 1964;
C o b l e et al., 1968; S h e i r & E 1 - S h a b r a w y A b o u l - E n e i n , 1970; Rifaat et al., 1980). As t h e
p r e v a l e n c e of o t h e r h e t e r o p h y i d s in t h e a r e a in q u e s t i o n is l o w e r t h a n that of H.
heterophyes ( T a r a s c h e w s k i , 1984), in E g y p t this d i a g n o s i s c a n b e a c c e p t e d as fairly
reliable.
P o s i t i v e d i s s e c t i o n s of d o g s ( A b d e l A z i m , 1938; K u n t z & C h a n d l e r , 1956a; W e l l s &
R a n d a l l , 1956; F a h m y & S e l i m , 1959) a n d cats (Kuntz & C h a n d l e r , 1956a; W e l l s &
R a n d a l l , 1956) h a v e s h o w n t h a t this p a r a s i t e is not s p e c i f i c to h u m a n s .
A f e w w i l d m a m m a l s a n d b i r d s w e r e also f o u n d to b e i n f e c t e d : Vulpes vulpes, Canis
aureus, Fells chaus, Milvus migrans (Wells & R a n d a l l , 1956); Pelecanus onocrotalus
(Looss, 1902).
O u t s i d e E g y p t , t h e f l u k e h a s b e e n r e c o r d e d , in r e c e n t years*, o n l y in d o g s a n d to a
l e s s e r e x t e n t in cats. M e d i t e r r a n e a n area: W i t e n b e r 9 (1929); B a l o z e t & C a l l o t (1939);
• Witenberg (1932) also reported human cases from Palestine (Israel).
466
H. T a r a s c h e w s k i
M i m i o g l u et al. (1959}; D e i a n a (1961); H i m o n a s (1964, 1968, 1977); J e m e n : Kuntz &
C h a n d l e r (1956a); Iran: M a s s o u d et al. (1982); India, Sri Lanka: Rao & A y y a r (1932);
M a p l e s t o n e & B h a d u r i (1940); D i s s a n a i k e (1961); S e n (1965); Rao & A n a n t a r a m a n (1967);
R a j a s e k a r i a h et al. (1974); in I n d i a H. heterophyes is c o n s i d e r e d a n e x t r e m e l y rare
p a r a s i t e of m a n ( M a p l e s t o n e & Bhaduri, 1940); S o u t h - E a s t A s i a : S e g a l et al. (1968).
As t h e t a x o n o m i c a l status of Heterophyes nocens is not sufficiently s o l v e d yet, H.
heterophyes is s o m e t i m e s r e c o r d e d from East A s i a also. W h e n e v e r d e s c r i p t i o n s of the
f l u k e s in q u e s t i o n a r e a v a i l a b l e , h o w e v e r , it b e c o m e s c l e a r that H. nocens is meant.
Second intermediate
hosts
K h a l i l (1923) d e t e c t e d that m u l l e t s s e r v e as t h e s e c o n d i n t e r m e d i a t e hosts of H.
heterophyes. S e v e r a l s p e c i e s of M u g i l i d a e h a v e b e e n f o u n d i n f e c t e d since then (data
o n l y from E g y p t a n d Israel a v a i l a b l e ) . P a p e r n a & O v e r s t r e e t (1981) listed: Mugil
cephalus, M. capito, M. auratus, M. saliens, a n d M. chelo as b e i n g n a t u r a l l y infected.
M a t u r e m e t a c e r c a r i a e of H. heterophyes w e r e also o b t a i n e d e x p e r i m e n t a l l y from Liza
subvlrldls a n d L. ramada ( T a r a s c h e w s k i & P a p e r n a , 1981}.
In a d d i t i o n to t h e s e M u g i l i d a e , m a n y s p e c i e s of other e u r y h a l i n e a n d m a r i n e fishes
w e r e r e c o r d e d as i n t e r m e d i a t e hosts: Epinephelus enaeus (Serranidae), Tilapia
(Sarotherodon) simonis (Cichlidae), Lichia amia, L. glauca ( C a r a n g i d a e ) , Barbus canis
( C y p r i n i d a e ) ( W i t e n b e r g , 1929), Tilapia (Sarotherodon) nilotica, T. zillii, Solea solea
(Soleidae), Sciaena aquilla ( S c i a e n i d a e ) (Wells & Randall, 1956).
H e t e r o p h y i d m e t a c e r c a r i a e , o b v i o u s l y of H. heterophyes, w e r e also found in Dicentrarchus labrax, D. punctatus, Sparus auratus, Argyrosoma regius ( P a p e r n a & Overstreet,
1981). N o n - m u g i l i d fishes w e r e also d e s c r i b e d as b e i n g s u s c e p t i b l e to e x p e r i m e n t a l
infections: Gambusia affinis (Poecilioidae) (Khalil, 1937), Fundulus parvipinnis (Cypr i n o d o n t i d a e ) (Kuntz & C h a n d l e r , 1956a) a n d Tilapia (Sarotherodon)mossambica
( T a r a s c h e w s k i , 1984).
U s u a l l y m u l l e t s s h o w t h e h i g h e s t i n t e n s i t i e s of Heterophyesinfections (Khalil, 1937;
W e l l s & Randall, 1956; P a p e m a & Overstreet, 1981). As yet, t h e r e is no information
a v a i l a b l e on w h e t h e r M u g i l i d a e are most s u s c e p t i b l e or w h e t h e r it is the h a b i t a t
p r e f e r e n c e of t h e s e fish w h i c h m a k e s t h e m t h e p r e d o m i n a n t i n t e r m e d i a t e hosts.
First intermediate
host
Khalil (1937) f o u n d the m u d s n a i l Pirenella conica Blainville to b e the first interm e d i a t e host of H. heterophyes. S i n c e t h e n P. conica n a t u r a l l y i n f e c t e d with H.
beterophyes h a v e b e e n m e n t i o n e d b y M a r t i n & Kuntz (1955); Kuntz & C h a n d l e r (1956al;
M a r t i n (1959); T a r a s c h e w s k i & P a p e r n a (1981, 1982). Q u a n t i t a t i v e d a t a on specific
p r e v a l e n c e of this f l u k e in different snail p o p u l a t i o n s h a v e b e e n c o l l e c t e d by Taras c h e w s k i (Fig. 2, T a b l e 2). C o n t r a r y to the d i s t r i b u t i o n of t h e s e c o n d i n t e r m e d i a t e hosts,
d i s t r i b u t i o n of P. conica is l i m i t e d to t h e e a s t e r n a n d s o u t h e r n M e d i t e r r a n e a n , Red Sea
a n d the P e r s i a n Gulf ( T a r a s c h e w s k i & P a p e r n a , 1981). As no other p o t a m i d i d gastropod
is k n o w n from t h e M e d i t e r r a n e a n , it can b e c o n c l u d e d that this s p e c i e s acts as the only
snail host in the M e d i t e r r a n e a n . In India, h o w e v e r , Cerithidea cingulata (syn. Tympanotonus micropterus), the host of H. (heterophyes) nocens in East A s i a (Asada, 1928)
Heterophyiasis
467
p r o b a b l y is the first i n t e r m e d i a t e host. A c c o r d i n g to Evans et al. (1973), both p o t a m i d i d
snails occur in the P e r s i a n Gulf. T h u s in this area too, further i n v e s t i g a t i o n into the
i n t r a m o l l u s c a n part of the life cycle is desired.
MEDITERRANEAN SEA
~--8
4~"{ ~
•
h
RED SEA
Fig. 2. Populations of Pirenella conica examined for prevalence of Heterophyes heterophyes, For
explanations see Table 2. B = Bardawil Lagoon; S = Siwa Oasis
ENVIRONMENT OF TRANSMISSION
As shown by Seo et al, (1981), in Korea p r e v a l e n c e of tTeterophyes n o c e n s and
laygidiopsis s u m m a in h u m a n s is c o n c e n t r a t e d a l o n g the coast, w h e r e Cerithidea cingulata thrives in l a g o o n s a n d estuaries, w h i l e M e t a g o n i m u s y o k o y a w a i is the d o m i n a n t
h e t e r o p h y i d inland. A c c o r d i n g to Vohra (1970), C. cingulata occurs in a v a r i e t y of w a v e
sheltered {subsequently soft sediment) habitats 'from b r a c k i s h w a t e r to s u p e r s a l t e d
fishponds with a salinity r a n g e of 15-45 %°', usually in h i g h p o p u l a t i o n densities. In
Japan, e n v i r o n m e n t a l conditions such as t h e s e are chiefly found a r o u n d the ' I n l a n d Sea'
b e t w e e n the major islands, w h e r e p r e v a l e n c e of H. n o c e n s in that country is a c c o r d i n g l y
highest (Ito, 1964).
Pirenella conica is also a d a p t e d to l a g o o n e n v i r o n m e n t (Fig. 3) ( T a r a s c h e w s k i &
Paperna, 1981, 1982); h o w e v e r , salinity t o l e r a n c e also i n c l u d e s the h y p e r s a l i n e range,
468
H. Taraschewski
T a b l e 2. P r e v a l e n c e rate of Heterophyes heterophyes in Pirenella conica in E g y p t a n d S u d a n
Sampling
site
Site No.
(see
Fig. 2)
D a t e of
sampling
No. of
snails
examined
No. of
snails
shedding
H, hetero-
Prevalence
rate
(%)
Habitat type
b r a c k i s h w a t e r lake; rural
e n v i r o n m e n t ; 10 k m e a s t of
Alexandria
phyes
LakeIdku
1
April
1982
400
27
7
Lake
Burullus
2
April
1982
150
57
38
h u g e b r a c k i s h w a t e r lake;
sampling station on black mud
off a s m a l l t o w n ; p r e v a l e n c e of
o t h e r t r e m a t o d e s in P. conica
v e r y low
Lake
Menzaleh
3
Sept.
1981
Sept.
1981
Sept.
1981
Sept.
1981
295
10
3
225
10
4
200
27
14
h u g e b r a c k i s h w a t e r lake;
important fishery ground;
d i s t a n c e to t h e city of Port Said
d e c r e a s i n g from Station 3 to
S t a t i o n 6; S t a t i o n 6 at t h e
o u t s k i r t s of t h e city
500
~ 80
16
4
5
6
Lake
Timsah
7
Sept.
1981
375
1
Lake
Qarun
8
April
1982
650
15
Suez
beach
9
Sept.
1981
April
1982
250
1
540
~ 10
2
9
0.3
s a l i n e i n l a n d l a k e in t h e S u e z
C a n a l ; o n l y o n e p o p u l a t i o n of
P. conica o n t h e b a t h i n g b e a c h
of I s m a e l i a
2
s a l i n e i n l a n d lake; rural
environment; only few
p o p u l a t i o n s of P. conica
0.4
n o r t h e r n e n d of G u l f of Suez;
d e n s e p o p u l a t i o n of P. conica
on black mud; high
p r e v a l e n c e of o t h e r
heterophyids
Hurghada
harbor
10
April
1982
623
~ 12
2
f i s h e r y h a r b o r of H u r g h a d a ;
only a few human settlements
in vicinity; h i g h p r e v a l e n c e of
other heterophyids
Sinai
Mangrove
11
April
1980
April
1981
Febr.
1982
500
-
-
630
~ 3
0.5
200
1
0.5
marine lagoon fringed by a
m a n g r o v e thicket; no h u m a n
s e t t l e m e n t s in vicinity;
a b u n d a n c e of w a t e r birds;
h i g h p r e v a l e n c e of
Heterophyes aequaHs a n d
other heterophyids
11
11
Sudan
Mangrove
12
Dec,
1980
400
mangrove thicket on
uninhabited island near
S u a k i n ; a b u n d a n c e of w a t e r
birds; o t h e r h e t e r o p h y i d s v e r y
prevalent
Heterophyiasis
469
~
.
~
~~
~
.....
Fig. 3. Pirenella conica (dark dots) on intertidal mud flat (after Taraschewski & Paperna, 1981)
obviously due to the arid c l i m a t e of the N e a r East. It has b e e n s h o w n by field observations and laboratory e x p e r i m e n t s that this g a s t r o p o d was a b l e to tolerate a salinity r a n g e
of 15-80 %0. P. conica also occurs in s a l i n e i n l a n d w a t e r s with an a t h a l a s s i o h a l i n i c ion
composition such as Lake Q a r u n and l a k e s of the Siwa Oasis (Fig. 2) ( T a r a s c h e w s k i &
Paperna, 1981).
A l o n g the M e d i t e r r a n e a n Coast, the N i l e Delta is the m a j o r c e n t r e of a b u n d a n c e of
P. conica; d e n s e p o p u l a t i o n s are found in e a c h of the great b r a c k i s h w a t e r l a k e s (Fig. 2).
N u m e r o u s d e n s e p o p u l a t i o n s of P. conica also exist a l o n g the s h e l t e r e d shore of the
northern Red Sea. In the N i l e Delta, h o w e v e r , the a c c u m u l a t i o n of first a n d s e c o n d
i n t e r m e d i a t e hosts and d e f i n i t i v e hosts creates a u n i q u e e p i d e m i o l o g i c a l situation. T h e
eutrophic lakes serve as nursery and f e e d i n g g r o u n d s for m u l l e t s and other fishes of
c o m m e r c i a l i m p o r t a n c e (e.g. Tilapia [Sarotherodon] nilotica) (Khalil, 1937; P a p e r n a &
Overstreet, 1981). Most of the p r e s e n t - d a y 43 m i l l i o n E g y p t i a n s live in the d e l t a
s u r r o u n d e d by l a r g e n u m b e r s of stray d o g s and cats. In addition, - contrary to other
M e d i t e r r a n e a n countries like Tunisia, w h e r e it is u n u s u a l to c o n s u m e r a w fish (Balozet &
Callot, 1939) - fresh salted m u l l e t 'fessikh' is c o n s i d e r e d a d e l i c a c y by m a n y E g y p t i a n s
(Khalil, 1937; Rifaat et al., 1980) and is thus p r o b a b l y the most i m p o r t a n t source of
infection to man. A c c o r d i n g to Khalil (1937), m e t a c e r c a r i a e inside m u l l e t put on ice
470
H. T a r a s c h e w s k i
(2-4 °C) w e r e found still a l i v e a n d i n f e c t i v e after 13 days, in salted fish for a m a x i m u m of
7 days.
PREVALENCE OF INFECTION
Snails
A s u r v e y of different habitats of Pirenella conica in E g y p t a n d S u d a n (Taraschewski,
1984) (Fig. 2) r e v e a l e d , that p r e v a l e n c e of Heterophyes heterophyes was h i g h e s t in the
N i l e D e l t a (Table 2). At L a k e Burullus, 38 % of the snails e x a m i n e d * s h e d c e r c a r i a e of/-/.
heterophyes* *. At Lake M e n z a l e h on t h e outskirts of Port Said, a b o u t 16 % infection was
noted. P r e v a l e n c e rates d e c r e a s e d w i t h i n c r e a s i n g d i s t a n c e to the city of Port Said (Fig. 2,
T a b l e 2). At t h e i n l a n d saline l a k e s Q a r u n a n d Timsah, p r e v a l e n c e rates w e r e l o w e r than
in the Delta, also on t h e s c a r c e l y p o p u l a t e d coast of t h e Red Sea, w h e r e only a f e w snails
w e r e f o u n d i n f e c t e d by H. heterophyes. At the Red S e a two o t h e r Heterophyes spp. (H.
aequafis, H. dispar], w h i c h h a v e a m o r e sylvatic c y c l e are a b u n d a n t (Taraschewski,
1984).
Fish
S e c o n d i n t e r m e d i a t e hosts are h e a v i l y p a r a s i t i z e d by m e t a c e r c a r i a e of H. heterophyes t h r o u g h o u t t h e D e l t a a n d t h e s u r r o u n d i n g S e a (Khalil, 1937; W e l l s & Randall,
1956; P a p e r n a & O v e r s t r e e t , 1981). In the 1950s, p r e v a l e n c e rates of Mugil cephalusand
M. capito of Lake M e n z a l e h (Fig. 2) w e r e f o u n d to be 100 % or almost 100 % (Wells &
Randall, 1956); t h e s e a u t h o r s r e p o r t e d s i m i l a r l y h i g h p r e v a l e n c e rates of H. heterophyes
in fish from t h e i n l a n d Lake Q a r u n (Fig. 2), w h e r e only a f e w snails w e r e found to be
i n f e c t e d in 1982 (Table 2).
As to the intensity, t h e r e is only o n e report a v a i l a b l e from B a r d a w i l l a g o o n (Fig. 2),
east of the S u e z Canal. A b o u t 10 y e a r s ago, up to 6000 h e t e r o p h y i d m e t a c e r c a r i a e w e r e
r e c o r d e d p e r g r a m m of m u s c l e in Mugil capito a n d up to a b o u t 1000 in M. cephalus
(Paperna & O v e r s t r e e t , 1981). Probably, t h e s e e n o r m o u s p a r a s i t e b u r d e n s w e r e o b t a i n e d
in the a d j a c e n t N i l e Delta, as the e n v i r o n m e n t of B a r d a w i l l a g o o n is almost u n i n h a b i t e d .
This a s s u m p t i o n is s u p p o r t e d by t h e fact that y o u n g fish of t h e l a g o o n w e r e p r e d o m i n antly i n f e c t e d by Heterophyes aequalis a n d Stictodora sawakinensis, both of w h i c h are
s h o w n to b e t r a n s m i t t e d in a sylvatic k i n d of e n v i r o n m e n t (Taraschewski, in prep.) such
as that at B a r d a w i l lagoon. A c c o r d i n g to r e c e n t spot c h e c k s by P a p e r n a (pets. comm.)
a n d by T a r a s c h e w s k i (unpubl.), it s e e m s that the i n t e n s i t y of i n f e c t i o n in m u l l e t of that
l a g o o n has b e e n d e c r e a s i n g . East of B a r d a w i l lagoon, on the Israeli coast, w h e r e only
o n e e p i d e m i o l o g i c a l l y i s o l a t e d p o p u l a t i o n of P, conica exists, H. heterophyes is also
s o m e t i m e s f o u n d in l a r g e m u l l e t s (Paperna & O v e r s t r e e t , 1981), w h i c h p r o b a b l y b e c a m e
i n f e c t e d in the N i l e Delta. H e t e r o p h y i d infections in y o u n g - o f - t h e - y e a r m u l l e t mostly
c o n s i s t e d of Stellantchasmus falcatus (Paperna & Overstreet, 1981). C e r c a r i a e of this
s p e c i e s w e r e s h o w n to h a v e the best v i a b i l i t y at salinities r a n g i n g from 4.5-9.0 %0 S (Lee
* Only snails :> 6 mm in length were collected, as no infection was noted in snails below that
minimal size (Taraschewski & Paperna, 1981, 1982).
* * Actual prevalence was probably higher, as not all infected snails will have released cercariae
after experimental treatment.
Heterophyiasis
471
& C h e n g , 1970). So t h e s e infections, o b t a i n e d in the low salinity e s t u a r i e s of the Israeli
coast, could b e autochthonous.
Definitive hosts
As to the d e f i n i t i v e hosts, the first q u a n t i t a t i v e data on h u m a n infections b e c a m e
a v a i l a b l e in 1937, At that time, up to 90 % of the school c h i l d r e n i n v e s t i g a t e d and 22 %
of the adults n e a r Lake M e n z a l e h (Fig. 2) d e f e c a t e d 'Heterophyes e g g s ' (Khalil, 1937)
(Fig. 4). Wells & B l a g g (1956) found Heterophyes e g g s in the stools of 36 % of the school
children of Baltim at Lake Burullus (Fig. 2). N a g a t h y & Khalil (1964) r e p o r t e d about 10 %
of the persons i n v e s t i g a t e d n e a r Lake M e n z a l e h to b e infected. F i n a l l y Rifaat et al. (1980)
found an a v e r a g e of 2.5 % infection in the s a m e area. Thus, like other intestinal h e l m i n t h
diseases of h u m a n s the p r e v a l e n c e of h e t e r o p h y i a s i s s e e m s to be d e c l i n i n g .
From the area of the saline i n l a n d lakes, snails of w h i c h h a v e b e e n e x a m i n e d by
T a r a s c h e w s k i (Fig. 2, T a b l e 2), and the Red Sea, n o t h i n g is k n o w n about the p r e v a l e n c e
of H. heterophyes in humans. From the Siwa Oasis, h o w e v e r , a b o u t 300 k m inside the
Libyan Desert (Egypt), of 42 p e r s o n s i n v e s t i g a t e d , one d e f e c a t e d Heterophl/es e g g s
(Coble et al., 1968). A l t h o u g h two p o p u l a t i o n s of P. conica h a v e b e e n r e p o r t e d from the
Siwa D e p r e s s i o n (Crawford, 1948; Ibrahim, 1975), it is u n c e r t a i n w h e t h e r the case
reported by C o b l e et al. can be c o n s i d e r e d autochthonous.
C o n c e r n i n g the other v e r t e b r a t e hosts in Egypt, all q u a n t i t a t i v e data are older than
25 years. In addition, e i t h e r the three E g y p t i a n Heterophyes spp. are not t r e a t e d
s e p a r a t e l y and data of different g e o g r a p h i c a l origin are p o o l e d (Wells & Randall, 1956),
or statements are very g e n e r a l (Kuntz & Chandler, 1956a), Proportionally l a r g e n u m b e r s
Fig. 4. Embryonated eggs of Heterophyes heterophyes inside the uterus of a fluke
472
H. T a r a s c h e w s k i
of t h e c a t a n d d o g p o p u l a t i o n w e r e i n f e c t e d . A c c o r d i n g to r e c e n t r e p o r t s f r o m G r e e c e
( H i m o n a s , 1968, 1977), 16 % (n: 186) of t h e e x a m i n e d s t r a y d o g s a n d 6 % (n: 123) of s t r a y
c a t s of t h e c i t y of T h e s s a l o n i k i w e r e f o u n d to b e i n f e c t e d b y H . h e t e r o p h y e s .
CONCLUSIONS
L a b o r a t o r y e x p e r i m e n t s w i t h 16 d i f f e r e n t d e f i n i t i v e h o s t s ( T a r a s c h e w s k i , i n p r e p . )
h a v e s h o w n ( T a b l e 3) t h a t ( b e s i d e s h u m a n s ) p r o b a b l y o n l y C a n i d a e a n d c a t s a r e
s u s c e p t i b l e t o H e t e r o p h y e s i n f e c t i o n ; i n t h e s e a n i m a l s t h e f l u k e s r e a c h a life s p a n of
T a b l e 3. Susceptibility of different definitive hosts to infection by H e t e r o p h y e s h e t e r o p h y e s
Hosts
No. of animals Flukes reach
sacrificed sexual maturity
Days of
life span
Recovery rates
(%) (3-25 d p.i.)
I2
< 16
< 18
< 8
~ 60
> 23
-- 60
60-120
0-15
0-94
0-71
0-29
61-83
66-93
55-91
32-81
0
M a c a c a irus
2
--
Ra ttus n o r v e g i c u s
R. tiomanicus
R. rattus
Canis farniliaris
Alopex lagopus
Vulpes vulpes
Felis catus
M e l e s rneles
M u s t e l a p u t o r i u s furo
M a r t e s foina
Sus scrofa
Egretta gularis
A r d e o l a ibis ×
N y c t i c o r a x nycticorax
Larus argentatus
L ridibundus
5
7
5
----
5
4
+
+
7
14
+
+
1
4
1
---
< 6
<
3
< 6
2
--
< 14
0-12
2
--
< 3
0
--
<
9
0
1
1
--
<
4
--
< 9
0-30
0
3
--
< 3
0
a b o u t 2 to 4 m o n t h s . C o n s i d e r i n g t h e l a r g e r s i z e a n d g r e a t e r a m o u n t of u t e r i n e e g g s ,
C a n i d a e t u r n e d o u t to b e b e t t e r h o s t s t h a n cats. I n a l l t h e o t h e r h o s t s u t e r i n e e g g s d i d n o t
b e c o m e e m b r y o n a t e d a n d l i f e s p a n d i d n o t e x c e e d 14 d a y s .
A s f l u k e s f r o m t h e h u m a n i n t e s t i n e w e r e f o u n d to h a v e a s i m i l a r s i z e t o t h o s e f r o m
d o g s ( K u n t z & C h a n d l e r , 1956 a), h u m a n s c a n b e c o n s i d e r e d s u i t a b l e h o s t s .
Besides dogs and cats, Canis aureus, Vulpes vulpes, Felis chaus and Milvus migrans
may also act as reservoir hosts (these species besides dogs and cats were found naturally
i n f e c t e d b y W e l l s & R a n d a l l , 1956). H o w e v e r , p r o b a b l y o n l y d o g s s e r v e a s i m p o r t a n t
reservoir hosts. Cats do not defecate on wet substrate and, as the Egyptian human
population rapidly increases, wild animals are becoming rare.
A c c o r d i n g t o Ito {1964), i n J a p a n M e t a g o n i m u s y o k o g a w a i is f o u n d m o r e f r e q u e n t l y
in d o g s t h a n in h u m a n s . For H. heterophyes this o b s e r v a t i o n c a n b e c o n f i r m e d in r e s p e c t
to t h e p r e v a l e n c e of t h i s f l u k e i n I n d i a o r i n G r e e c e for i n s t a n c e . I n E g y p t , h o w e v e r , it is
uncertain whether dogs or humans act as the predominant definitive hosts.
Heterophyiasis
473
mm
25-
n:~:556
20-
~"'!~"
~5-
10-
"":
4-6
z._w.
zz.zvz..
"i-zzzH:
.11z.iz
7-9
£-
I0-12
!~~ !
~
.
!
13-15
16-18
19-2!
mm
Fig. 5. Growth of P. conica naturally infected by heterophyids (H. heterophyes, H. aequalis,
Stictodora sawakinensis) within 2 months. Ordinate: snail length in ram; abscissa: initial length of
snails in ram; base column: initial length; undotted column: growth of uninfected snails (Zn: 297);
dotted column: growth of infected snails (Zn: 259)
Host-parasite relations
Little i n v e s t i g a t i o n has b e e n c o n d u c t e d on the q u e s t i o n of h o w i n t e r m e d i a t e a n d
d e f i n i t i v e hosts of H. heterophyes are affected by the fluke.
Snails
After the snails h a v e i n g e s t e d the fluke eggs, the e m b r y o n i c d e v e l o p m e n t of H.
heterophyes is p r e s u m a b l y similar to that of H. aequalis, d e s c r i b e d by Kuntz & C h a n d l e r
(1956b). Rediae, p r o d u c i n g cercariae, w e r e found i n s i d e the d i g e s t i v e g l a n d s (Taras c h e w s k i & Paperna, 1981). From growth e x p e r i m e n t s with snails n a t u r a l l y i n f e c t e d with
h e t e r o p h y i d s (H. heterophyes, H. aequalis, Stictodora sawakinensis), it b e c o m e s conspicuous that b e l o w 10 m m initial size, g r o w t h of i n f e c t e d and of u n i n f e c t e d s p e c i m e n s
was about the s a m e (Fig. 5). A b o v e 10 m m initial length, i n f e c t e d snails s h o w e d
e n h a n c e d growth w h e n c o m p a r e d to the u n i n f e c t e d snails (Taraschewski, 1980). T h u s it
can be s u s p e c t e d that h e t e r o p h y i d t r e m a t o d e s h a v e some d e t r i m e n t a l i n f l u e n c e on
r e p r o d u c t i o n of Pirenella conica, as was s h o w n in other r e l a t i o n s h i p s b e t w e e n snails and
flukes.
Fish
N o t h i n g is k n o w n about the p a t h o g e n i c i t y of H. heterophyes i n s i d e the s e c o n d
i n t e r m e d i a t e hosts. T h e r e is only one i n v e s t i g a t i o n a v a i l a b l e on Stellantchasmus falcatus infections in MugiI cephalus (Lee & C h e n g , 1970). T h e s e authors r e p o r t e d that " t h e
p r e s e n c e of the parasite, e v e n w h e n u n e n c y s t e d , results in the n e c r o t i c d e g e n e r a t i o n of
474
H. T a r a s c h e w s k i
the s u r r o u n d i n g m u s c l e cells, e s p e c i a l l y those s i t u a t e d at the anterior or posterior ends of
the parasite. Large, v a c u o l a t e d fat c e l l s . . , are u s u a l l y found filling the spaces v a c a t e d by
n e c r o t i c m u s c l e cells" (Lee & C h e n g , 1970).
As those m u l l e t s h i g h l y i n f e c t e d with Heterophyes m e t a c e r c a r i a e , r e p o r t e d by
P a p e r n a & O v e r s t r e e t (1981), w e r e still found alive, one m a y c o n c l u d e that the viability
of m u l l e t s is not m u c h a f f e c t e d by the p r e s e n c e of the Heterophyes m e t a c e r c a r i a e in their
muscles. Still, i n v e s t i g a t i o n on the p a t h o g e n i c i t y of Heterophyes heterophyes in different fish hosts is n e e d e d .
M e t a c e r c a r i a e in e x p e r i m e n t a l l y i n f e c t e d Gambusia affinis (Khalil, 1937) and
Tilapia (Sarotherodon) mossambica (Taraschewski, 1984) b e c a m e infective about 20
days post i n f e c t i o n e m .
Fig. 6. Heterophyes spec. in small intestine of a cat. Big arrow: ventral sucker clinging to host
mucosa; small arrow: oral sucker feeding on host tissue
Heterophyiasis
475
Definitive hosts
I n s i d e e x p e r i m e n t a l l y i n f e c t e d d e f i n i t i v e hosts, m e t a c e r c a r i a e of H. heterophyes
w e r e s h o w n (dogs: Khalil, 1937; cats: T a r a s c h e w s k i , 1984) to e x c y s t a b o u t 4 h after oral
a p p l i c a t i o n . E x c y s t m e n t t o o k p l a c e in t h e u p p e r s m a l l i n t e s t i n e ( T a r a s c h e w s k i , 1984) or
in t h e d u o d e n u m (Khalil, 1937). F r o m 14. heterophyes ( H a m d y & N i c o l a , 1981),
Metagonimus J/okogawai (Ito, 1964) a n d Haplorchis yokogawai (Africa et al., 1940) it h a s
b e e n d e s c r i b e d t h a t after e x c y s t m e n t , t h e j u v e n i l e f l u k e s p e n e t r a t e into t h e i n t e s t i n a l
g l a n d s or into t h e t i s s u e of t h e m u c o s a . A f t e r a f e w d a y s t h e y n o r m a l l y r e t u r n to t h e
i n t e s t i n a l l u m e n , w h e r e t h e y a d h e r e to t h e m u c o s a b y t h e i r v e n t r a l s u c k e r (Fig. 6). By
m e a n s of t h e i r o r a l s u c k e r t h e y f e e d o n t h e h o s t ' s m u c o s a l t i s s u e (Fig. 6).
F r o m t h e d a t a o n 14. heterophyes, it s e e m s t h a t t h e p l a c e of p r i m a r y a t t a c h m e n t to
the m u c o s a is in t h e s a m e p a r t of t h e s m a l l i n t e s t i n e as t h e p l a c e of e x c y s t m e n t w h e r e t h e
flukes are still f o u n d o n e or t w o m o n t h s l a t e r (in s u i t a b l e hosts) ( T a r a s c h e w s k i , 1984).
W h e n t h e site of a t t a c h m e n t of j u v e n i l e f l u k e s 3 d p.i. (days p o s t i n f e c t i o n e m ) is
c o m p a r e d to that of s e x u a l l y m a t u r e f l u k e s 1 0 - 1 2 0 d p.i. it a p p e a r s t h a t - d u e to t h e
i n t e s t i n a l m o t i l i t y - t h e y a r e j u s t p a s s i v e l y c a r r i e d s l i g h t l y b a c k w a r d s (Fig. 7). I n d e p e n d e n t of t h e s p e c i e s of host, 14. heterophyes g e n e r a l l y p r e f e r s t h e m i d d l e p a r t of t h e s m a l l
i n t e s t i n e (Fig. 7).
In s o m e cases, s e x u a l l y m a t u r e h e t e r o p h y i d s w e r e f o u n d s t u c k in t h e i n t e s t i n a l w a l l ,
from w h e r e t h e i r e g g s c o u l d b e i n f i l t r a t e d i n t o d i f f e r e n t o r g a n s b y w a y of t h e b l o o d
s t r e a m or l y m p h a t i c s y s t e m (see r e v i e w b y Ito, 1964). In J a p a n , w h e r e Metagonimus
yokogawai is t h e m o s t p r e v a l e n t h e t e r o p h y i d s p e c i e s , n o t h i n g is k n o w n a b o u t fatal
h u m a n c a s e s d u e to s u c h e g g s (Ito, 1964). In t h e P h i l i p p i n e s , h o w e v e r , w h e r e Haplorchis
yokogawai is t h e m o s t p r e v a l e n t s p e c i e s in h u m a n s , A f r i c a et al. (1940) e s t i m a t e d t h a t
15 % of t h e fatal h e a r t c a s e s r e s u l t e d f r o m h e t e r o p h y i d m y o c a r d i t i s . In a s e r i e s of p a p e r s ,
iq
200-
100
m
10
15
Fig. 7. Distribution of juvenile and mature Heterophyes heterophyes throughout the small intestine
of experimentally infected definitive hosts. Ordinate: n flukes; abscissa: 16 segments of small
intestine. Narrow striped bars = Juvenile flukes (3 d p.i., n: 358 from 9 cats and 3 foxes), Broad
dotted bars = Mature flukes (10-120 d p.i., n: 862 from 9 cats and 3 foxes)
1
5
476
H. T a r a s c h e w s k i
s u m m a r i z e d i n 1940, t h e s e a u t h o r s r e p o r t e d m a n y f i n d i n g s of h e t e r o p h y i d e g g s i n t h e
t i s s u e s of h u m a n b e i n g s a u t o p s i e d i n t h e P h i l i p p i n e s .
O n l y i n t w o c a s e s w e r e e g g s , a s s i g n e d to I-t. heterophyes, f o u n d e n c a p s u l a t e d i n t h e
h u m a n b r a i n ( C o l l o m b e t al., 1960). In a n o t h e r c a s e , a n e g g a t t r i b u t e d to t-I. nocens w a s
d e t e c t e d i n s i d e a t u m o r of a n i n f l a m e d a p p e n d i x (Ito, 1964).
S y m p t o m s of i n t e s t i n a l h e t e r o p h y i a s i s s e e m to b e - a s u s u a l - d e p e n d e n t o n t h e
i n t e n s i t y of i n f e c t i o n . H e a v y i n f e c t i o n s , a c c o r d i n g to K h a l i l (1937), a r e a c c o m p a n i e d b y
abdominal discomfort, nausea, headache, vomiting, diarrhea, and sometimes dysentery.
S i m i l a r s y m p t o m s a r e d e s c r i b e d for h u m a n i n f e c t i o n s b y M e t a g o n i m u s yokogawai,
w h e r e t h e l i t e r a t u r e is m u c h m o r e c o m p r e h e n s i v e (Ito, 1964).
E x p e r i m e n t a l l y i n f e c t e d d o g s s t a r t e d d e f e c a t i n g e g g s (Fig. 4) of H. h e t e r o p h y e s 8 d
p.i. ( W i t e n b e r g , 1929); e x p e r i m e n t a l l y i n f e c t e d c a t s o n d a y 9 (Khalil, 1937). A s s u m a b l y
t h e p r e p a t e n t p e r i o d a l s o i n h u m a n s w i l l b e a b o u t 7 d a y s , w h i l e f l u k e s m a y h a v e a life
s p a n of 1 to 4 m o n t h s , a s s h o w n f r o m i n f e c t e d C a n i d a e a n d c a t s ( T a b l e 3).
Acknowledgement. Thanks are due to Prof. B. Loos-Frank for critical revision of the manuscript and
reading the proofs.
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