Trematodes Recovered in the Small Intestine of Stray Cats in the Republic of Korea

Article information

Abstract

INTRODUCTION

The stray cat, Felis catus, is well established as a powerful predator in the wild natural ecosystem of the Republic of Korea. This highly adaptable predator actively consume the wide-ranged food stuff originated from the mammalian, avian, reptilian, amphibian, and piscine preys as well as invertebrates. Consequently, it has been known that the stray cat is infected with numerous parasites and act as an important reservoir host for parasites of medical or veterinary importance. On the other hand, surveys on the intestinal parasites of stray cats have been conducted in various regions of the world [1-6]. In the Republic of Korea, studies on helminthic infections of cats have been performed by several workers [7-13].

As trematodes of cats, a total of 10 species, i.e., Clonorchis sinensis, Paragonimus sp., Heterophyes nocens, Heterophyopsis continua, Pygidiopsis summa, Metagonimus yokogawai, Centrocestus sp., Pharyngostomum cordatum, Echinochasmus perfoliatus, and Echinoparyphium sp., were reported in the Republic of Korea until 2000 [7-10]. Subsequently, in 2005, more than 15 species were added to the trematode fauna of felines by Sohn and Chai [12], and Gymnophalloides seoi was found in the small intestines of 2 feral cats from Shinan-gun, Jeollanam-do in 2009 [13]. Among the trematode fauna reported by Sohn and Chai [12], 13 species (Procerovum varium, Stellantchasmus falcatus, Stictodora fuscata, Stictodora lari, Centrocestus armatus, Cryptocotyle sp., Echinostoma hortense, Echinostoma revolutum, Echinochasmus japonicus, Stephanoprora sp., Neodiplostomum sp., Plagiorchis muris, and Eurytrema pancreatitum) were new for cat parasites in Korea. However, no morphologic descriptions were made on these trematode species. Therefore, in the present study, we intended to provide morphologic details and characteristics of these 13 trematode species infecting cats.

MATERIALS AND METHODS

The trematode specimens were collected as previously described [12]. The collected worms were fixed with 10% neutral buffered formalin under a cover glass pressure, stained with Semichon's acetocarmine, and observed using a light microscope equipped with a micrometer (OSM-4, Olympus Co., Tokyo, Japan). All measurements are given in µm unless stated otherwise.

RESULTS

Morphology of worms first recorded in Korea [12]

Procerovum varium (Fig. 1)

Fig. 1

Procerovum varium adult (Semichon's acetocarmine stained and a drawing) recovered from the small intestine of a cat. Body small, 435×235 µm in average size, and having a muscular oral sucker (OS), a pharynx (P), a small ventral sucker with a long and thick-walled expulsor (E), a spherical ovary (O), single globular testis (T), and follicular vitellaria distributed in the post-ovarian fields.

Body small, pear-shaped, 435 (425-445 in range) long and 235 (230-240) wide (n=2), with greatest width at posterior 1/3 of the body. Oral sucker subterminal, 44 (41-46) by 47 (44-51). Prepharynx very short. Pharynx subglobular or elliptical, 37 (36-38) by 35 (33-36). Esophagus short, 53 (51-54) in length. Ceca bifurcating anterior 1/3 and terminating posterior 1/4, middle level of testis. Ventral sucker very small, 25 by 38, embedded in ventrogenital sac. Expulsor long and thick-walled, 156 (153-159) by 29 (26-33). Seminal vesicle saccular, 87 (82-92) by 51. Ovary spherical or subspherical, 44 (41-46) by 47 (46-49), preequatorial and slightly dextral to midline. One testis globular or subglobular, 102 (90-115) by 118 (102-133), lying in middle of hind-body. Vitellaria follicular, distributing in post-testicular fields near posterior extremity. Uterus with eggs occufying from anterior 1/3 to posterior end, most of hind-body. Eggs small, yellow, and 26 (24-28) by 13 (11-14).

Cryptocotyle concava (Fig. 2)

Fig. 2

Cryptocotyle concava adult (Semichon's acetocarmine stained and a drawing) recovered from the small intestine of a cat. Body small, 778×576 µm in average size, and having a muscular oral sucker (OS), a pharynx (P), a ventrogenital sac (VGS) with a small ventral sucker, a thick-walled seminal vesicle (SV), a spherical ovary (O), slightly lobulated 2 testes (T), and follicular vitellaria distributed along the extracecal margin from the preacetabular level to the posterior end of the body.

Body small, oval or spatulate, 778 (500-1,170) long and 576 (468-732) wide (n=20). Oral sucker subterminal, 75 (50-84) by 89 (70-105). Pharynx subglobular, 36 (28-49) by 43 (25-55). Esophagus slender, 114 (63-230) in length. Ventrogenital sac elliptical, 52 (35-88) by 65 (48-88), with small ventral sucker and genital pore. Seminal vesicle saccate, thick-walled, 270 (150-332) by 114 (75-153). Ovary spherical, 70 (38-133) by 76 (50-120), lyingy dextral to midline. Seminal receptacle elliptical and small, just behind of the left margin of ovary. Two testes slightly lobulated, closely located in posterior portion; right 182 (108-332) by 85 (50-161); left 169 (110-307) by 89 (50-197). Vitellaria follicular, distributing along extracecal margin from pre-acetabular level to posterior end of body. Eggs small, yellow, and 25.6 (23.0-28.1) by 13.2 (11.0-16.6).

Stephanoprora sp. (Fig. 3)

Fig. 3

Stephanoprora sp. adult (Semichon's acetocarmine stained and a drawing) recovered from the small intestine of a cat. Body elongated and 2,317×474 µm in average size, having a characteristic head crown with 22 collar spines, a muscular oral sucker (OS), a pharynx (P), a well developed ventral sucker (VS), a cirrus sac (CS), a spherical ovary (O), transversely elliptical 2 testes (T), and follicular vitellaria (V) distributed in the post-testicular fields.

Body elongated, somewhat attenuated at both ends, 2,317 (2,253-2,381) long and 474 (461-486) wide (n=2). BW (body width) to BL (body length) ratio about 20%. Head crown distinct, bearing total 22 collar spines in 1 row, and interrupted at the dorsal side of oral sucker, 135 (125-145) by 305 (300-310). Dorsal spines 45 (43-48) long and 14 broad at base, lateral spines 40 (39-41) by 12, the last one (33 by 11) of 2 end group spines smaller than the second one (38 by 12). Oral sucker subterminal, 105 by 113 (100-125). Prepharynx short. Pharynx subglobular, 133 (130-135) by 105 (100-110). Esophagus slender, 190 (175-205) in length. Ceca bifurcated at 513 (21-24% of body length) from anterior end. Ventral sucker large and well developed, 215 (205-225) by 230 (225-235), located at 713 (27-32% of body length) from anterior end. Cirrus sac well developed and contained saccular seminal vesicle, 225 (215-235) by 123 (110-135). Ovary spherical, submedian, 95 (80-110) by 120 (115-125). Two testes transversely elliptical, directly tandem near the middle portion of the body; anterior 125 (100-150) by 245 (215-275); posterior 140 (130-150) by 218 (200-235). Total testicular region 274 (about 12% of body length). Vitellaria follicular, occupying from 73 from posterior end of body to about middle of posterior testis. Eggs, a few in the uterus, operculated, yellow, 82 (77-92) by 65 (61-69).

DISCUSSION

Trematode infections in cats have been reported by several workers in Korea. In 1967, Kang [7] detected 2 trematode species, i.e., C. sinensis and Paragonimus sp., in cats from a western region of Gyeongsangnam-do. In 1979, Lee [8] reported 6 trematode species, namely, C. sinensis, H. nocens, M. yokogawai, Centrocestus sp., E. perfoliatus, and Echinoparyphium sp., in cats from Gyeongsangbuk-do [8]. Eom et al. [9] described heterophyid flukes, including H. continua, H. nocens, and P. summa, from cats purchased at Jungang Market in Seoul in 1985 [9]. Huh et al. [10] in 1993 found 2 trematode species, i.e., C. sinensis and P. cordatum, in cats purchased at a market in Seoul. Therefore, before 2005, a total of 10 trematode species (C. sinensis, Paragonimus sp., M. yokogawai, H. nocens. H. continua, P. summa, Centrocestus sp., E. perfoliatus, Echinoparyphium sp., and P. cordatum) were known among the trematode fauna of Korean cats [12].

Subsequently, in 2005, Sohn and Chai [12] detected 23 trematode species which included C. sinensis, Paragonimus westermani, Eurytrema pancreatitum, P. cordatum, Metagonimus spp., H. nocens, P. summa, H. continua, Stictodora fuscata, S. lari, Acanthotrema felis, Stellantchasmus falcatus, Centrocestus armatus, Procerovum varium, Cryptocotyle sp., Echinostoma revolutum, Echinostoma hortense, Echinochasmus japonicus, Stephanoprora sp., Plagiorchis muris, Neodiplostomum sp., unidentified echinostome larvae, and a diplostomulum (mesocercaria of Diplostomum sp.) in 438 stray cats from a wholesale house of animals located in Gupo, Buk-gu, Busan Metropolitan City, Korea. Among them, 13 species were newly recorded as cat intestinal flukes [12]; 10 species (S. falcatus, S. fuscata, S. lari, C. armatus, E. hortense, E. revolutum, E. japonicus, N. seoulense, P. muris, and E. pancreatitum) were new fauna of cats and 3 species (P. varium, C. concava, and Stephanoprora sp.) were new fauna of not only cats but also all animal hosts in Korea. There was a necessity to provide morphologic details of these trematodes. Therefore, in the present study, we intended to record the morphologic details of these 13 new fauna of cats.

With regard to cat trematode parasites, Scholz et al. [1] reported 5 species (Opisthorchis viverrini, Haplorchis pumilio, Haplorchis taichui, Haplorchis yokogawai, and S. falcatus) in domestic cats from Vientiane province, Lao PDR. In several regions of Egypt, Kuntz and Chandler [14] detected 14 trematode species (Heterophyes heterophyes, Heterophyes aequalis, H. pumilio, H. taichui, H. yokogawai, S. falcatus, Pygidiopsis genata, Phagicola longicollis, P. ascolonga, Stictodora sawakinensis, Echinochasmus liliputanus, Stephanoprora denticulatoides, Mesostephanus appendiculatus, and Cynodiplostomum namrui) from domestic cats. Most of these trematode species detected from cats are zoonotic and transmitted via eating raw flesh of freshwater or brackish water fish. Therefore, it is suggested that stray cats may play an important role as a reservoir host in endemic areas of zoonotic trematodes.

The genus Procerovum is a small trematode group of the family Heterophyidae, and characterized by possessing a single testis and a large prominent seminal vesicle modified into an expulsor. Infections by these flukes have been recorded mainly in birds and occasionally in mammals, including humans from China, Japan, the Philippines, Vietnam, India, and Australia [15,16]. Only 3 species, namely P. varium, P. calderoni, and P. cheni, are recognized to be valid by morphologic differences, including the extent of ceca and size of the expulsor. Our specimens are characterized by the presence of a saccular seminal vesicle with thick-walled chambers and an expulsor less than 160 µm long. Meanwhile, P. calderoni has a very long expulsor measuring longer than 200 µm, and P. cheni has a bipartite seminal vesicle with thin-walled chambers and an expulsor shorter than 100 µm long [15]. Moreover, our specimens were morphometrically very similar with P. varium from Vietnam which was described by Chai et al. [16]. Accordingly, it is confirmed that our specimen is identical to P. varium, and this species is indigenously distributed in Korea.

Trematodes of the genus Cryptocotyle (Heterophyidae) are intestinal parasites of fish-eating birds and mammals, and they are widely distributed throughout the world. Among 11 species recorded, Cryptocotyle lingua is known from various species of birds and mammals, including cats, Felis catus. This species was also found from herring gulls (Larus argentatus vegae), stray dogs (Canis familiaris), and red foxes (Vulpes vulpes schrencki) in Japan [17]. However, our specimens were morphologically compatible with C. concava, rather than C. lingua. The body shape is usually elongated in C. lingua, while it is somewhat oval or spatulated in C. concava which was consistent with our specimens [18]. The shape of testes, slightly lobed or severely lobed, is somewhat obscure as a differential point between C. lingua and C. concava. The location of 2 testes is side by side in C. concava and in our specimens, while it is slightly oblique in C. lingua. The distribution of vitellaria, extending anteriorly to mid-point between the ventral sucker and intestinal bifurcation, is commonly revealed in C. lingua, C. concava, and also our specimens, unlike in C. jejuna in which vitellaria extending to the level of the anterior edge of the ventral sucker. The egg size in our specimens was more or less smaller than those of C. lingua and C. concava (Table 1). Based on the aforementioned morphologic characters, our specimens were almost idendical with C. concava except in the size of eggs.

Table 1.

Comparison of Cryptocotyle sp. morphometrics with those of previous studies

The genus Stephanoprora (Echinostomatidae) is a group of echinostomatid flukes, and mainly found in birds and rarely in mammals. Among the species described, S. denticulatoides was found in dogs from Crimea and cats from the Mediterranean coast of Egypt [14,19]. Isaichikoff [19] recorded this echinostome as a new species based on some morphological differences from a close species, S. denticulata. He regarded following characters as differential points from S. denticulata; large collar spines, larger body, suckers, ovary, and testes, and more anterior extending of the vitellaria [19]. However, Stephanoprora species are difficult to distinguish on the basis of adult morphology alone. Since this fluke groups have been described from birds and mammals of wide geographical ranges, they can differ in important morphologic characters, i.e., measurements of the body and internal organs, shape and location of internal organs, shape and arrangement of collar spines, and distribution of vitelline glands, according to the age (maturity) of worms recovered and host species. Moreover, the quality of worm specimens can affect the species identification. Accordingly, the more solid index is needed for the definitive identification of Stephanoprora species.

It has been known that more than 13 species have the following morphologic characters like S. denticulata; a total of 22 collar spines, an unlobed ovary, and the anterior limits of the vitelline glands fluctuating between the anterior limits of the anterior testis and the testicular junction [20]. Among them, 2 species recovered from mammalian hosts, S. denticulatoides and S. denticulata, were compared with our specimens from cats (Table 2) [14,20]. Our specimens (about 20% of BW/BL ratio) are somewhat stouter than S. denticulatoides (about 10%) and S. denticulata (about 15%). However, the sucker ratio, diameter of the oral sucker to the ventral sucker, 1:2.07-2.13, is nearly equal with those of 2 species. The arrangement pattern of 22 collar spines is nearly the same, but the size of each spines is more or less smaller than those of the 2 species. The egg size was somewhat larger in our specimens. On the other hand, from the standpoint of some morphologic characters, such as the anterior limits of the vitelline glands, smaller size of the eggs than the ovary, uterine extent, diameter of suckers, sucker ratio, and having 2 corner spines on each side of the pharynx, about 10 species, including S. denticulatoides are regarded as the synonyms of S. denticulata [20]. Conclusively, based on the aforementioned comparative morphologies, it is suggested that our specimens, tentatively called Stephanoprora sp., should be considered identical with S. denticulata although there are minor differences between them and lacking enough number of our specimens.

Table 2.

Comparison of Stephanoprora sp. morphometrics with those of previous studies

The remaining 10 species (S. falcatus, S. fuscata, S. lari, C. armatus, E. revolutum, E. hortense, E. japonicus, N. seoulense, P. muris, and E. pancreatitum), newly recorded as cat flukes in Korea, are all zoonotic trematodes, and their infections to humans and animals have been sporadically reported [21]. With the exception of humans and cats, a few animal species have been recorded as natural definitive hosts of these flukes in Korea. For example, adults of C. armatus were recovered from egrets [22], E. revolutum from rats [23], E. hortense from rats, dogs, and mice [24-27], E. japonicus from egrets, ducks, and shrews [22,27,28], and N. seoulense and P. muris from rats and mice. Before the present study, N. seoulense and P. muris were described only from rodent hosts (Rattus norvegicus and Apodemus agrarius), and they were somewhat smaller than our specimens [24,25,29,30].

E. pancreaticum normally parasitizes the biliary and/or pancreatic duct of ruminants, such as cattle, sheep, goat, and rabbit. However, sometimes this fluke accidentally infects humans. In Korea, human infections by this fluke were reported by detecting eggs in stool examinations [31,32]. Adult worms were found at a human autopsy case in Japan [33]. The specimens from this human were about 10.5 mm in length and 6 mm in width, having the oral sucker (2.0 mm in diameter) larger than the ventral sucker (1.5 mm in diameter) and characteristic dark brown eggs (av. 47 by 30 µm in size) [33]. Although our specimen is partly broken and somewhat smaller than those from a human case, morphologic characteristics, including convoluted ceca, lobed ovary, 2 lobed testes, and operculated dark brown eggs, were identical with that of the previous study [33].

Article information Continued