Document Type : Research Paper
Authors
College of Veterinary Medicine,University of Al Muthanna
Abstract
Canine tapeworm Taenia hydatigena larval stage is also called Cysticercus
tenuicollis (C. tenuicollis). This cystic stage was reported in domestic and wild
ruminants worldwide. It is one of the common parasites of small ruminants in
Iraq. The omenta, the mesenteries, and liver are the usual locations of C.
tenuicollis. This article tends to describe a case report of the uncommon locations
of the T. hydatigenacysticerci in pregnant goat. In this case, large (7 cm length X
5 cm width) C. tenuicollis cyst was found on the body surface of the 4 months
pregnant uterus of local goat as well as inside the fetal allantoic cavity (chorionallantoic
membrane). The cyst-like channels with a mass of fibrin and
erythrocytes were the most characteristic histopathological lesion THAT observed
on the uterine wall. However, slight degeneration changes seen on the fetus and
the C. tenuicollis vesicle located adjacent to the placentomes. In conclusion, this
study approved the deviant situation of C. tenuicollis cyst on fetus membranes
and over the pregnant uterus surface. These locations explain the probability of
larval migrations into the fetal body during pregnancy.
Keywords
Article Title [العربیة]
حویصلات الدودة الشریطیة المعدرة فی الارحام الحوامل والاجنة فی الماعز
Abstract [العربیة]
یسمى الطور الیرقی للدودة الشریطیة المعدرة(الشریطیة الھامشیة) للکلاب،بالکیسةالمذنبةالرقیقةالعنق.
وعالمیا ، تم تسجیل ھذا الطور الیرقی الکیسی فی المجترات الداجنة والبریة. وقد اعتبرت واحدة من
الطفیلیات الشائعة بالمتجرات الصغیرة فی العراق.ویعتبر الثرب ، الکبد والمساریق المواقع الشائعة
للکیسةالمذنبةالرقیقةالعنق. تھدف ھذه المقالة إلى وصف حالة تواجد غیرعادیة للکیسة المذنبة الرقیقة العنق
5 X فی رحم معزة حامل. وقد تم العثور على الکیسة المذنبة الرقیقة العنق وبحجم یصل الى ( 7 سم طول
سم عرض) على سطح جسم رحم المعزة المحلیة الحامل لمدة اربعة اشھر تقریبا وکذلک داخل جوف
السقائی المشیمائی . اھم الآفات التشریحیة المرضیة الأکثروضوحافی جدار الرحم ھی القنوات الشبیھة
بالکیس مع کتلة من الفبرین والکریات الدمویة الحمراء . ورغم ذلک ففد تم ملاحظة التغیرات التنکسیة
الطفیفةعلى الجنین ووجدت الکیسةالمذنبةالرقیقةالعنق بصورة متاخمة للمشام . فی الخلاصة، اثبتت ھذه
الدراسة الموقع الشاذ للکیسة المذنبة الرقیقة العنق داخل الأغشیة الجنینیة وعلى سطح الرحم
الحامل. ھذا التواجد یثبت احتمالیة ھجرة الطور الیرقی فی داخل ھیکل الجنین أثناءالحمل .
Basrah Journal of Veterinary Research,Vol.15, No.3,2016
Proceeding of 5th International Scientific Conference,College of Veterinary Medicine
University of Basrah,Iraq
45
Cysticercus tenuicollis VESICLE IN GOAT PREGNANT
UTERUS AND FETAL BODY: REPORT OF A CASE
Karima Al Salihi*; Samir Sabaa Rahee 1; Ali Husein Ali 1
College of Veterinary Medicine,University of Al Muthanna
Key words:C. tenuicollis, chorion-allantoic membrane, pregnant goat.
ABSTRACT
Canine tapeworm Taenia hydatigena larval stage is also called Cysticercus
tenuicollis (C. tenuicollis). This cystic stage was reported in domestic and wild
ruminants worldwide. It is one of the common parasites of small ruminants in
Iraq. The omenta, the mesenteries, and liver are the usual locations of C.
tenuicollis. This article tends to describe a case report of the uncommon locations
of the T. hydatigenacysticerci in pregnant goat. In this case, large (7 cm length X
5 cm width) C. tenuicollis cyst was found on the body surface of the 4 months
pregnant uterus of local goat as well as inside the fetal allantoic cavity (chorionallantoic
membrane). The cyst-like channels with a mass of fibrin and
erythrocytes were the most characteristic histopathological lesion THAT observed
on the uterine wall. However, slight degeneration changes seen on the fetus and
the C. tenuicollis vesicle located adjacent to the placentomes. In conclusion, this
study approved the deviant situation of C. tenuicollis cyst on fetus membranes
and over the pregnant uterus surface. These locations explain the probability of
larval migrations into the fetal body during pregnancy.
INTRODUCTION
Cysticercus tenuicollis is also called Cysticercosis. The tapeworm infectionhas
caused by embryonic stage of Taenia hydatigena,the canine alimentarycestode
and other untamed canids (1). Withal,omentum, mesentery, peritoneum are the
usual locations of the mature Cysticercus tenuicollis, while the pleura and
pericardium are, the less frequent. These tapeworm larvae are migrating
Basrah Journal of Veterinary Research,Vol.15, No.3,2016
Proceeding of 5th International Scientific Conference,College of Veterinary Medicine
University of Basrah,Iraq
46
commonly in the parenchyma of the liver and causing hepatitis in the young
animals (2). The most infected cases are chronic and asymptomatic which not
commonly recognized until slaughter (3). However, sheep are rarely affected by
the acute infection form and the internal organs cysticercosis in lambs are rare (4,
5). Very low mortality reported but the individual death of infected lambs
occurred in various countries of Asia content (6, 7).
In Iraq, the incidence of Cysticercosis (Tenuicollosis) reported in sheep at
Duhok abattoir (north of Iraq) (8). Besides, the number of infection was 31 (0.7%)
out of 4716 examined sheep. However, the cysts were absence in both goats and
cattle. Mesentery was the common site of the cysts with a percentage (29%)
followed by the uterus (16%) with few cases in other visceral organs. Ghaffar,
(2011) (8) also recorded the first findings associated with uncommon locations of
the cysts in the diaphragm, ovary and urinary bladder in Duhok region. Moreover,
the study reported that the only sheep play an insensible role in the dissemination
of the infection. In another previous study, on the genital system anomaly,
Smithet al., (1999) (9) found the presence of C. tenuicollis on the body of the
uterus and the large ligament of the ewes.Review of the literature revealed a
paucity information regardingC. tenuicollis cystdeviant situation in the
goat.Features of attached C. tenuicollis cyst on surface on the pregnant uterine
body of a goat and the fetal bodyis described for the first time in Iraq in this study.
CASE REPORT
In Al Muthanna abattoir and during the routine examination of four slaughtered
a pregnant goat, attached C. tenuicolliscyst found on the surface of the body of the
uterus. Later on, this pregnant uterus collected from the abattoir and examined.
The C. tenuicolliscyst also found on the allantoic cavity, neighboring to the
amniotic membrane. The owner of this goat was a butcher who bought it from
local livestock in Al Muthanna governorate, where the animals were grazedon the
field pastures. The goats and dogs supplied with anti-parasitic drug according to
the request of the owner. The uterus and fetal membranes samples were
Basrah Journal of Veterinary Research,Vol.15, No.3,2016
Proceeding of 5th International Scientific Conference,College of Veterinary Medicine
University of Basrah,Iraq
47
collected from affected area. The samples were preserved in (10%)neutral
buffered formalin. The tissue samples were processed routinely and3-5-μm thick
sections were done and stained with routine haematoxylin and eosin staining. The
other closer gross examination of the animal revealed numerous smallcysticerci
cyst (ranged between 2-4 cm in diameter) in the peritoneum. The uterus was
enlarged and distended and its horn consistent with a four months fetus. A 7 X 5
cm C. tenuicollis vesicle was attached to the surface of the uterine body. After
dissection of the uterine wall, the fetal and fetal membranes reached. A parasitic
cyst was seen inside the fetus allantoic (Figure. 1& 2). The cystic structure
revealed a colorless fluid surroundedwith a tiny membrane. Moreover,the anterior
end of a tapeworm that bearing suckers and hooks for attachment,indignant
vertically.The cystback features enabled its identification as C. tenuicollis. No
signs of union was seen between the cover of C. tenuicolliscysts and fetus sheath,
which located in parallel to amnions. The examination of uterine wall lesions by
microscopic revealed cyst-like channels with a mass of fibrin and erythrocytes.
The Uterine cells mostly degenerated areas. Microscopic lesions of inflammation
were not visible inside the fetus, and the C. tenuicollis vesicle located adjacent to
the placentomes with slight degeneration of the epithelia and the uterine wall.
Basrah Journal of Veterinary Research,Vol.15, No.3,2016
Proceeding of 5th International Scientific Conference,College of Veterinary Medicine
University of Basrah,Iraq
48
Figure. 1. Shows the C. tenuicollis vesicleon the surface of the body of the gravid
Uterus.
Figure.2. ShowsC. tenuicollis vesicle is located adjacent to the placentomes.
DISCUSSION
In this case report, the uncommon location of C. tenuicolliscyst on wall of
uterus body and inside the pregnant uterus revealed that the possibility of blood
supply to transfer the parasite oncosphere to the uterus. This result is compatible
with the previous observation that mentioned the possibility of the migration of
the parasite oncosphere via the tiny capillaries of the cotyledonal area, via the
placental wallapproaching the allantoic membrane vascular network, and then
reaching the allantoic cavity (10, 11, 12). The histopathological changes that
observed on the attachment site of the C. tenuicollis vesicle revealed a mass of
fibrin, erythrocytes and degeneration of the uterine. Previous studies explain the
existence of cestode oncospheres and cysticerci that can escape theimmunological
reaction of the host,by using a passive fleemechanism orvia modulation of the
immune response that called immunomodulation (13, 14, 15). The viable
cysticerci of other cestode wrapped up by mild inflammatory cellsthat serve to kill
the parasite (16, 17). The existence of cysticercus on placenta enables itssmooth
crossingfromhost immunmechanisms.Moreover,in the gravidity, an advancement
in the osmolality and electrolyte concentrations of the allantoic fluid is also seen
Basrah Journal of Veterinary Research,Vol.15, No.3,2016
Proceeding of 5th International Scientific Conference,College of Veterinary Medicine
University of Basrah,Iraq
49
(18) and the contents of the allantoic fluid which are water and solutes may play a
role in the growth of this cysticercus. The previous studies revealed the existence
oflive and degenerative cysts on all parts of genital system of the infected
ewes(17, 19). Deviant location of C. tenuicollis cystwas documented for the first
time in Iraq in pregnant the goat in the present study.Seemingly, C. tenuicollis
existence was not harming the normal growth of the unborn young that owned
this cysticercus cyst.In addition,C. tenuicolliscyst existencebackwardsto the wall
of placenta might activate the possibility ofcrossingand reachof oncosphere
intomature embryo in gravid ewes.In conclusion, this study approved the aberrant
location of C. tenuicolliscyston the fetus membranes and on the surface of the
pregnant uterus of the goat. These locations explain the probability of larval
migrations and reaching the fetal body during pregnancy.
الخلاصة
یسمى الطور الیرقی للدودة الشریطیة المعدرة(الشریطیة الھامشیة) للکلاب،بالکیسةالمذنبةالرقیقةالعنق.
وعالمیا ، تم تسجیل ھذا الطور الیرقی الکیسی فی المجترات الداجنة والبریة. وقد اعتبرت واحدة من
الطفیلیات الشائعة بالمتجرات الصغیرة فی العراق.ویعتبر الثرب ، الکبد والمساریق المواقع الشائعة
للکیسةالمذنبةالرقیقةالعنق. تھدف ھذه المقالة إلى وصف حالة تواجد غیرعادیة للکیسة المذنبة الرقیقة العنق
5 X فی رحم معزة حامل. وقد تم العثور على الکیسة المذنبة الرقیقة العنق وبحجم یصل الى ( 7 سم طول
سم عرض) على سطح جسم رحم المعزة المحلیة الحامل لمدة اربعة اشھر تقریبا وکذلک داخل جوف
السقائی المشیمائی . اھم الآفات التشریحیة المرضیة الأکثروضوحافی جدار الرحم ھی القنوات الشبیھة
بالکیس مع کتلة من الفبرین والکریات الدمویة الحمراء . ورغم ذلک ففد تم ملاحظة التغیرات التنکسیة
الطفیفةعلى الجنین ووجدت الکیسةالمذنبةالرقیقةالعنق بصورة متاخمة للمشام . فی الخلاصة، اثبتت ھذه
الدراسة الموقع الشاذ للکیسة المذنبة الرقیقة العنق داخل الأغشیة الجنینیة وعلى سطح الرحم
الحامل. ھذا التواجد یثبت احتمالیة ھجرة الطور الیرقی فی داخل ھیکل الجنین أثناءالحمل .
Basrah Journal of Veterinary Research,Vol.15, No.3,2016
Proceeding of 5th International Scientific Conference,College of Veterinary Medicine
University of Basrah,Iraq
50
REFERENCE
1. Taylor MA, Coop RL, Wall RL (2015). Veterinary parasitology. Wiley-
Blackwell; 4 edition: PP. 585.
2. Blazek K, Schramlova J and Hulinska D. (1985).Pathology of migration
phase of Taenia hydatigena(Pallas 1766) larvae.Folia Parasitol.32:127-
137.
3. Christodoulopoulos G, Theodoropoulos G. & Petrakos G. (2008)
Epidemiological survey of cestode-larva disease in Greek sheep flocks.
Veterinary Parasitology. 53:368–373.
4. Livesey CT, Herbert IV, Willis JM & Evans WT. (1981). Acute
cysticercosis in housed sheep. Veterinary Record. 109:217.
5. Koutsoumpas A, Psychas V, Papadopoulos E, Panousis N, Karatzias H&
Giadinis ND. (2013). Acute visceral cysticercosis in feed-lot lambs. Revue
de Me´dicine Ve´terinaire. 164:425–428.
6. Radfar MH, Jajalli M & Jalalzadeh M. (2005). Prevalence and
morphological characterization of cysticerci from sheep and goats in Iran.
Veterinarski Arhiv. 75:469–470.
7. Nourani H, Pirali Kheirabadi KH, Rajabi H & Banitalebi A. (2010). An
unusual migration of Taenia hydatigena larvae in a lamb. Tropical
Biomedicine. 27: 651–656.
8. Ghaffar M Nacheervan. (2011). Tenuicollosis in slaughtered sheep at
duhok abattoir- kurdistan region of Iraq. Bas J Vet Res. 10(1):1-15.
9. Smith KC, Parkinson TJ, Long SE (1999). Abattoir survey of acquired
reproductive abnormalities in ewes. Vet Rec. 144:491–496.
10. Payan-Carreira R, Silva F, Rodringues M and Dos Anjos Pires M. (2008).
Cysticercus tenuicollis in fetal structures: Reprod.Domest.Anim. 43
(6):764-766. DOI: 10.1111/j.1439-0531.2007.01014.x · Source: PubMed.
11. Cheng TC (1986). Eucestoda: the true tapeworms. General Parasitology.
2nd edn., Academic 8Press, pp. 387–444.
Basrah Journal of Veterinary Research,Vol.15, No.3,2016
Proceeding of 5th International Scientific Conference,College of Veterinary Medicine
University of Basrah,Iraq
51
12. Heath DD. (1971). The migration of oncospheres of Taenia pisiformes, T.
serialis and Echinococcus granulosus within the intermediate host. Int J
Parasitol. 1:145–152.
13. Terrazas LI, Bojalil R, Govezensky T, Larralde C. (1998). Shift from an
early protective Th1-type immune response to a late permissive Th2-type
response in murine cysticercosis (Taenia crassiceps). J Parasitol. 84: 74–
81.
14. Molinari JL, Mejia H, White AC Jr, Garrido E, Borgonio VM, Baig S,
Tato P, 2000: Taenia solium: a cysteine protease secreted by metacestodes
depletes human CD4 lymphocytes in vitro. Exp Parasitol 94, 133–142.
15. Pe´rez-Torres A, Ustarroz M, Constantino F, Villalobos N, deAluja AS
(2002): Taenia solium cysticercosis: lymphocytes in the inflammatory
reaction in naturally infected pigs. Parasitol Res. (88):150–152.
16. Chi HS, Chi JG (1978). A histopathological study on human cysticercosis.
Korean J Parasitol. 16:123–133.
17. Sanchez Acedo C. (1999). Cisticercosis bovina; Cisticercose de los
pequen˜ os ruminantes. In: del Campillo C, Va´ zquez R (ed),
Parasitologia Veterinaria. McGraw-Hill-Interamericana10de Espan˜ a,
SAU, pp. 350–362.
18. Faichney GJ, Fawcett AA, Boston RC, 2004: Water exchange between the
pregnant ewe, the foetus and its amniotic and allantoic fluids. J Comp
Physiol [B] 174, 503–510.
19. Smith KC, Parkinson TJ, Long SE (1999). Abattoir survey of acquired
reproductive abnormalities in ewes. Vet Rec. 144:491–496.
Blackwell; 4 edition: PP. 585.
2. Blazek K, Schramlova J and Hulinska D. (1985).Pathology of migration
phase of Taenia hydatigena(Pallas 1766) larvae.Folia Parasitol.32:127-
137.
3. Christodoulopoulos G, Theodoropoulos G. & Petrakos G. (2008)
Epidemiological survey of cestode-larva disease in Greek sheep flocks.
Veterinary Parasitology. 53:368–373.
4. Livesey CT, Herbert IV, Willis JM & Evans WT. (1981). Acute
cysticercosis in housed sheep. Veterinary Record. 109:217.
5. Koutsoumpas A, Psychas V, Papadopoulos E, Panousis N, Karatzias H&
Giadinis ND. (2013). Acute visceral cysticercosis in feed-lot lambs. Revue
de Me´dicine Ve´terinaire. 164:425–428.
6. Radfar MH, Jajalli M & Jalalzadeh M. (2005). Prevalence and
morphological characterization of cysticerci from sheep and goats in Iran.
Veterinarski Arhiv. 75:469–470.
7. Nourani H, Pirali Kheirabadi KH, Rajabi H & Banitalebi A. (2010). An
unusual migration of Taenia hydatigena larvae in a lamb. Tropical
Biomedicine. 27: 651–656.
8. Ghaffar M Nacheervan. (2011). Tenuicollosis in slaughtered sheep at
duhok abattoir- kurdistan region of Iraq. Bas J Vet Res. 10(1):1-15.
9. Smith KC, Parkinson TJ, Long SE (1999). Abattoir survey of acquired
reproductive abnormalities in ewes. Vet Rec. 144:491–496.
10. Payan-Carreira R, Silva F, Rodringues M and Dos Anjos Pires M. (2008).
Cysticercus tenuicollis in fetal structures: Reprod.Domest.Anim. 43
(6):764-766. DOI: 10.1111/j.1439-0531.2007.01014.x · Source: PubMed.
11. Cheng TC (1986). Eucestoda: the true tapeworms. General Parasitology.
2nd edn., Academic 8Press, pp. 387–444.
Basrah Journal of Veterinary Research,Vol.15, No.3,2016
Proceeding of 5th International Scientific Conference,College of Veterinary Medicine
University of Basrah,Iraq
51
12. Heath DD. (1971). The migration of oncospheres of Taenia pisiformes, T.
serialis and Echinococcus granulosus within the intermediate host. Int J
Parasitol. 1:145–152.
13. Terrazas LI, Bojalil R, Govezensky T, Larralde C. (1998). Shift from an
early protective Th1-type immune response to a late permissive Th2-type
response in murine cysticercosis (Taenia crassiceps). J Parasitol. 84: 74–
81.
14. Molinari JL, Mejia H, White AC Jr, Garrido E, Borgonio VM, Baig S,
Tato P, 2000: Taenia solium: a cysteine protease secreted by metacestodes
depletes human CD4 lymphocytes in vitro. Exp Parasitol 94, 133–142.
15. Pe´rez-Torres A, Ustarroz M, Constantino F, Villalobos N, deAluja AS
(2002): Taenia solium cysticercosis: lymphocytes in the inflammatory
reaction in naturally infected pigs. Parasitol Res. (88):150–152.
16. Chi HS, Chi JG (1978). A histopathological study on human cysticercosis.
Korean J Parasitol. 16:123–133.
17. Sanchez Acedo C. (1999). Cisticercosis bovina; Cisticercose de los
pequen˜ os ruminantes. In: del Campillo C, Va´ zquez R (ed),
Parasitologia Veterinaria. McGraw-Hill-Interamericana10de Espan˜ a,
SAU, pp. 350–362.
18. Faichney GJ, Fawcett AA, Boston RC, 2004: Water exchange between the
pregnant ewe, the foetus and its amniotic and allantoic fluids. J Comp
Physiol [B] 174, 503–510.
19. Smith KC, Parkinson TJ, Long SE (1999). Abattoir survey of acquired
reproductive abnormalities in ewes. Vet Rec. 144:491–496.