Abdominal secondary ectopic pregnancy in a free-roaming cat

Selda Curtseit1, Elvira Condrut1, Mihai Ciprian Stoicea2, Alexandru Ciuca3, Ozana
Ciulei3
1
Synevovet, Veterinary Diagnostic Laboratory, 25 Industriilor Street, 077040 Chiajna,
Romania
2
Synevo, Diagnostic Laboratory, 81 Pache Protopopescu Blvd. 021408 Bucharest,
Romania
3
Teravet, Small Animal Practice, 72-86 Giurgiului Street, Bucharest, 040673, Romania
Correspong author: Selda Curtseit, 25 Industriilor Street, 077040 Chiajna, Romania
+40 723 474 225, selda.curtseit@gmail.com
Introduction
Ectopic, or extrauterine pregnancy denotes a pregnacy that occurs elsewhere than in the
uterine cavity. According to the location of the fetus, ectopic pregnancy is considered to
be (1) Tubal pregnancy occurs when the fetus is located in the oviduct. This category is
further divided in three subtypes: fimbrial, ampullar and isthmic. (2) Abdominal
pregnancy occurs when the fetus is located in the peritoneal cavity. Based on the causes,
the latter is divided in two subtypes: primary abdominal pregnancy occurs when an
oocyte is fertilized in the peritoneal cavity or when the already fertilized ova is lost from
the oviduct and ends in the peritoneal cavity, where it becomes attached to the abdominal
viscera or peritoneum. Secondary abdominal pregnancy follows the rupture of an oviduct
or of the uterus. Three mechanisms lead to this: (a) the fetus is located in the abdominal
cavity, but the placental attachments are retained through the breach in the uterine wall
(Lederer & Fisher, 1960), (b) the fetus develops further in the abdominal cavity due to
the complete reimplantation of the placenta in the abdominal cavity (Bunte &
Hildebrandt, 1975) or (c) an internal abortion may occur in witch the fetus is lost in the
abdominal cavity along with the loss of the placental attachments (Madani & Tirgari,
1984). Three other types of ectopic pregnancies are reported, but to lesser frequency:
cornual, ovarian and cervical.
Ectopic pregnancies in animals were reported in dogs (Lederer & Fisher 1960, Peck &
Badame 1967, Shamir & Shahar 1996, Buergelt & Russell 2004, Eddey 2012, Scholten et
al. 2013), rabbits (Arvidsson 1998, Beddow 1999, Segura et al. 2004, Smith et al. 1989),
ewes (Davies 1982, Madani & Tirgari 1984, Mitchell 1989), guinea pigs (Araujo 1964,
Hong & Armstrong 1978), laboratory mouse (Bloch 1962), cow (Botcherby 1980),
hamsters (Peters 1982, Buckley & Caine 1979), mare (Freytag 1972), monkeys (Jerome
& Hendrickx 1982, Bunte & Hilebrandt 1975, Bosu & Barker 1980), squirell (McClure &
Chang 1975), rat (Gosden & Russell 1981, Polzenhagen et al. 1983), baboon (SchlabritzLoutsevitch et al. 2004).
In the last 40 years 17 cases of abdominal pregnancy in cats were reported in
international literature (Linzell, 1951; Carrig et al., 1972; Fry & Jones, 1973; Hansen,
1974; Crownover & Yeargan, 1976; Bodle 1979, De Nooy, 1979; Johnson et al., 1983;
Palmer, 1989; Knott, 1989, Forbes 1989, Ristic & Raijmakers 1997, Nack 2000, Thilagar
et al. 2000, Rosset et al., 2011, Oros 2012, Cetin et al. 2014).
Case presentation
A 4-year-old European Shorthair intact female was referred to a private clinic with
lethargy, anorexia, anuria and constipation. The cat was free-roaming and there was no
available information or history relating to the cats life. The person bringing the cat to

the veterinarian reported that she had been lethargic and anorexic in the last two days.
Physical examination revealed the cat was normothermic (38.5C). Examination of her
cardiac and respiratory systems was unremarkable. Routine palpation of the abdomen
demonstrated intense abdominal pain and one palpable mass present in the abdominal
cavity. The urinary bladder was distended. Serum biochemical profile and a complete
blood count (CBC) were performed. Mild elevation in serum glucose (140 mg/dl; range
61 - 124 mg/dl), alanin aminotrasferase (63 u/L; range 8.3 53 u/L), blood urea nitrogen
(36 mg/dl; range 15 31 mg/dl) and cholesterol (170 mg/dl; range 71-161 mg/dl) and a
mild decrease in serum calcium (6 mg/dl; range 7.9 - 10.9 mg/dl) were recorded. The
CBC showed reticulopenia (5.7 K/L; range 15-81 K/L), neutrophilia (90.6%; range
29.5-74.5%), lymphopenia (5%; range 20-61.2 %) and eosinopenia (0.6%; range 3.411.4%). The cell morphology was normal. Abdominal ultrasonography revealed a mass
attached to greater omentum. General anesthesia was induced by intramuscularly
administred acepromazine (Sedam, Pasteur Institute, Bucharest, Romania) followed by
intramuscularly administration of ketamine (Ketamidor, Richter Pharma AG, Wels,
Austria). A mid-line laparatomy was performed. The mass was embedded, and adherent
to the omentum which showed only small dark firm areas of hematomas near the fetus.
The uterine horns were involuted and near the distal end of the left uterine horn an oval
firm mass 1,5 cm long could be identified. It was supposed to be a uterine fetus and no
attempt of extraction was made. No scar or tear was visible on the uterus. The mass was
dissected together with its omental wrapping with a 1 cm additional margin. An
ovariohisterectomy was then performed. The ovarian vessels and ligament on both sides
and the uterine body were ligated cranial to the cervix and severed. In the next days
following surgery the general status of the cat improved dramatically and she made a full
recovery.
The mass and its omental attachments were submitted to the laboratory for gross and
histopathologic examination.
Results
Gross examination
Grossly, the mass had 5.5 x 5.0 x 2.0 cm, was globular and wrapped in the greater
omentum (fig.1). The regions of the body were not demarked except for a limb missing
the distal portion emerging the lateral side of the fetus. Longitudinal sections revealed
that one of the poles of the fetus was similar to a cranial vault with brain tissue
underneath (fig.) and that the skin folded deeply into the fetus, forming cavities lined by
haired skin. Some of the body regions, organs and tissues were recognizable on gross
examination (cranial vault, brain, ribs, spinal canal and spinal cord, muscle, cartilage) but
the general arrangement was chaotic (fig.). No placenta or major blood vessels were
observed in connection with the fetus. The mass was suspected to be a mature teratoma or
ectopic pregnancy.

Fig. 1 Fetus wrapped in omentum. Several Fig. 2 One of the poles of the fetus resembled a
hematomas on the omentum covering the fetus. cranial vault sheltering brain tissue underneath.

Fig. 3 The cut section of the fetus (A and B halves). The A half: appendix resembling a limb
missing the distal part (arrow). The B half: The spinal canal containing the spinal cord (arrow) and
the cartilaginous structure of a developing limb are visible in the upper third; the middle third
contains cartilaginous ribs arranged in an approximate row; in the lower third the haired skin folded
deeply into the fetus.
The tissue samples were decalcified and fixed in 10% phosphate-buffered formalin and
processed routinely for light microscopic examination.
Histopathology
Histologically, the fetus was composed of numerous types of tissue with ectodermal,
endodermal and mezodermal origin. The autolysis and decalcification effaced the cellular
details but the general architecture was still well discernable. The fetus was covered by
multilayered cornified epithelium with well-developed hair follicles (fig.) except for the
areas where the omentum was attached to the fetus (fig.). The brain had well developed
gyri and was covered by meninges (fig.). The spinal canal contained the spinal cord and
dorsal root ganglions (fig.). The developing limbs contained cancellous bone going
through endochondral ossification (fig. and fig.). The digestive tract was identified based
on its tubular shape, layered wall and folded mucosa containing numerous goblet cells
(fig.). The fetus had teeth present in alveolar bone (fig.) and a multilobular glandular
3

organ, supposedly a salivary gland (fig.). In the atelectatic lung parenchyma there were
bronchi surrounded by cartilaginous rings (fig.).

Fig. Multilayered cornified haired Fig. The attachment of the fetus to the
epithelium covering the fetus. Striated omentum. The fibrous tissue of the
muscle is also visible in this section. HE, omentum continues directly with the fetus.
10x
HE, 4x

Fig. Mature brain with well developed Fig. Spinal cord and dorsal root ganglion in
gyri. HE, 4x
the spinal canal. HE, 4x

Fig. Two parallel long bones containing

cancellous
bone,
going
through
endochondral
ossification.
Striated
muscles are attached to the bones. HE, 4x

Fig. Digestive tract. The muscular layer and

the folded mucosa typical for the intestine
are clearly visible. Numerous goblet cells
are present in the mucosa. HE, 4x.

Fig. Teeth present in alveolar bone of the Fig. Salivary gland with
jaw. HE, 4x.
architecture. HE, 4x.

multilobular

Fig. Atectatic lung with bronchi Fig. Inflammatory infiltrate. Moderate

surrounded by cartilaginous tissue. HE, 4x. numbers of inflammatory cells consist of
eosinophils and lymphocytes are present in
the omentum. HE, 4x.
Discussion
Ectopic pregnancy is an important pathology in human medicine. In veterinary medicine,
ectopic pregnancy has been reported in a number of species but with a striking lower
frequency and to a different outcome in comparison to human medicine. The cats were
mainly affected and all the reported cases were ectopic abdominal secondary pregnancies.
Interestingly, clinical signs were absent in the majority of cases of ectopic pregnancy in
cats (Carrig et al 1972, Crownover & Yeargan 1976, Forbes 1989, Knott 1989, Godfrey
1997, Nack 2000). When present, they were caused by other infections (Hannon 1981) or
necrosis of the ectopic tissue (Johnson 1986). In our case, the clinical signs (lethargy,
decreased appetite, anuria, constipation, abdominal pain) were considered to be the result
of mechanical interference with abdominal organs due to its relatively large size. Anuria
was a response to the stress induced by confinement, resulting in accumulation of the
urine in the urinary bladder, which caused additional pressure on abdominal organs and
subsequent abdominal pain.
The previous reported cases of ectopic abdominal pregnancies in cats were considered to
be secondary and our case most likely falls in the same category. Ectopic secondary
pregnancy occurs when the uterus ruptures and the fetus is lost in the abdominal cavity.
In our case, the cat was free-roaming and uterine rupture caused by trauma is a likely
event in a cat living in these conditions. Thus, attacks by dogs or blunt trauma caused by
cars or humans with no other evident lesions except for the uterine rupture are constant
dangers. Literature reports a case of dog attack which resulted in multiple traumas

including rupture of the uterus and fall of the fetus in abdominal cavity (Kumru et al.
2007). Furthermore, for the abdominal pregnancy to be truly primary, placentation must
exist on the peritoneal or omental surface (Peters 1982). No signs of placentation were
observed in our case. Finally, the absence of evidence of uterine rupture does not
necessarily rule out the occurrence of this event. Other reports with no uterine scarring
(Fry & Jones 1973, Tirgari 1986, Max et al. 2013) but also with uterine scarring (Tigari
1986, Findik 1998, Rosset et al. 2011) It is known that the myometrium can regenerate,
leaving little or no cicatricial tissue (Buhimschi et al. 2010).
Unlike previous reports (Tirgari 1986, Findik 1998, Rosset et al. 2011) in which the
presence of placenta, umbilical cord, fetal membranes and blood vessels was noted, in
this case, no such structures were noticed. This led us to believe that the fetus was lost
shortly before the clinical signs manifested and the cat was referred to the veterinarian,
within a time range which permitted the healing of the uterus and the autolysis of the
fetus but not the installment of fetal modifications commonly reported in other studies:
encapsulation due to peritoneal reaction (Fry & Jones 1973, Tirgari 1986, Max et al.
2013), maceration (Bodh et al. 2014) or mummification (Tirgari 1986, Godfrey 1997,
Rosset 2011, Oros et al. 2012). The short duration of the ectopic pregnancy before
diagnosis is further demonstrated by the minimal peritoneal reaction, limited to a
moderate infiltration with mononuclear cells and polimorphonuclear eosinophils.
It is not possible to determine the precise time of the event but the mineralization of the
bones would place the age of the fetus at a minimum of 40 days.
The lump on the left uterine horn could have been the place of prior attachment of the
fetus before complete resolution or a fetus in the early stage of a new pregnancy. Term
pregnancies occurring subsequent to and in conjunction with extrauterine fetuses are
documented in other species (Hong & Armstrong, 1978; Peters, 1982). The exact nature
of the lump is impossible to be assessed in the absence of proper gross examination of the
cut surface.
Clinical signs (abdominal distension and pain, palpable mass) and gross characteristics of
the fetus (globular mass covered by haired skin) were also reported in cases of mature
teratomas in cats (Gruys et al. 1976, Basaraba et al. 1998). The differential diagnosis was
possible based on microscopic examination. Teratomas originate most often from the
ovary or testicle because of their germ cell origins, but extragonadal neoplasms have been
reported (Gruys et al. 1976, Homer & Riggs 1991, Lambrechts & Pearson 2001, Wong et
al. 2007, Arora & Iyer 1969, Ober et al. 2013). Although no case of omental teratoma in
the cat has yet been reported in English written literature, several reports exist in human
medicine, including proposed mechanisms of apparition, appliable for animal organisms
as well (Abdelmounaim et al. 2009, Mandal & Badhe 2012, Hardesty et al. 2012, Hegde
2014). Mature teratomas are composed of well differentiated tissues with ectodermal,
endodermal and mezodermal origin, but these tissues are haphazardly oriented
throughout the tumor and they fail to be organized in organs (Basaraba et al., 1998;
Gruys et al., 1976; Ober et al., 2013; Miyoshi et al., 2001).
The deformities of the fetus would not have permitted survival even if a laparatomy had
been carried out at a suitable moment. Furthermore, survival of fetuses in abdominal
pregnancy is a very rare or unknown in domesticated and laboratory species, even in
normally developed fetuses (Gosden & Russel, 1981). In the only reported case of a
viable fetus in an abdominal pregnancy it seems that the survival of the kitten was

possible due to the proximity of the uterine rupture and laparatomy (Hansen et al. 1974).
In contrast, ectopic pregnancy has been regularly reported to be compatible with full-term
development in humans (Zhang & Sheng, 2008; Dahab et al., 2011).
Conclusion
Ectopic pregnancy is readily diagnosed during surgery, but severe malformation of the
extrauterine fetus and attachment to the omentum can lead to confusion with omental
neoplasia, particularly mature teratoma. The differentiation can be made by microscopic
examination.
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