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Ultrasound and computed tomography of sacculitis and appendicitis in a rabbit

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Abstract

A 9-month-old neutered male rabbit was referred for lethargy, anorexia, and gastrointestinal stasis. Routine hematology, serum biochemistry, and diagnostic imaging were performed. Computed tomography revealed a wall thickening of the sacculus rotundus and appendix, which was further confirmed on abdominal ultrasound. Full thickness biopsies were collected with histopathology diagnosing a chronic multifocal heterophilic granulomatous sacculitis and appendicitis. The patient was treated medically and at 6 weeks follow-up, clinical signs and intestinal changes had completely regressed. Inflammation of the sacculus rotundus and appendix should be considered as a cause of gastrointestinal stasis in rabbits.
Received: 10 August 2017 Revised: 9 October 2017 Accepted: 31 October 2017
DOI: 10.1111/vru.12602
IMAGING DIAGNOSIS
Ultrasound and computed tomography of sacculitis
and appendicitis in a rabbit
Maurizio Longo Florence Thierry Kevin Eatwell Tobias Schwarz Jorge del
Pozo Jenna Richardson
Royal (Dick) School of VeterinaryStudies and
Roslin Institute, The University of Edinburgh,
Roslin, UK
Correspondence
Maurizio Longo, Royal (Dick) School of Veteri-
nary Studies and Roslin Institute, The University
of 7 Edinburgh, Roslin, EH25 9RG, UK.
Email: mlongo@exseed.ed.ac.uk
Abstract
A 9-month-old neutered male rabbit was referred for lethargy, anorexia, and gastrointestinal sta-
sis. Routine hematology, serum biochemistry, and diagnostic imaging were performed. Computed
tomography revealed a wall thickening of the sacculus rotundus and appendix, which was fur-
ther confirmed on abdominal ultrasound. Full thickness biopsies were collected with histopathol-
ogy diagnosing a chronic multifocal heterophilic granulomatous sacculitis and appendicitis. The
patient was treated medically and at 6 weeks follow-up, clinical signs and intestinal changes had
completely regressed. Inflammation of the sacculus rotundus and appendix should be considered
as a cause of gastrointestinal stasis in rabbits.
KEYWORDS
appendix, cecum, sacculus rotundus, typhilitis
1SIGNALMENT, HISTORY, AND CLINICAL
FINDINGS
A 9-month-old, male neutered, Lionhead rabbit was presented to the
Rabbit and Exotic Animal Department at the referral Hospital of the
University of Edinburgh for evaluation of a 4-day history of anorexia,
lethargy, and decreased fecal production consistent with gastrointesti-
nal stasis. The patient was neutered at 6 months of age by the refer-
ring veterinary surgeon and had no previous health concerns. The diet
offered included ad-libitum hay, with a small ration of complete com-
mercial pellet and mix of fresh green vegetables each day.
On physical examination, the patient was tachypnoeic, with a heart
rate of 200 beats/min and an elevated rectal temperature of 39.9C.
Body condition score was 2/5 and no abnormality was detected
on palpation of the abdomen. Gut sounds were absent on abdominal
auscultation. Complete blood count findings included a mildly elevated
white cell count of 13.1 ×109/l (reference range 5.2–12.5 ×109/l)
with left shift of the neutrophils. The patient was medically managed
with supportive care for 24 h including intravenous fluid therapy with
compound sodium lactate (Hartmann's solution, Aquapharm, Animal-
care Limited, UK) at 4 ml/kg/h divided into slow intravenous boluses.
Multimodal analgesia was provided with buprenorphine (Buprecare
[The copyright line for this article was changed on 5 March 2018 after original online publication.]
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the original work is properly cited.
c
2018 The Authors. Veterinary Radiology & Ultrasound published by Wiley Periodicals, Inc. onbehalf of American College of Veterinary Radiology
0.3 mg/ml, Animalcare Limited, UK) at 0.03 mg/kg subcutaneously
every 6 h alongside a nonsteroidal anti-inflammatory drug, meloxicam
(Metacam 1.5 mg/ml, Oral Suspension, Boehringer Ingelheim, Ger-
many) at 0.6 mg/kg per every 12 h. Gastrointestinal prokinetic therapy
was provided with ranitidine (Zantac 15 mg/ml, GlaxoSmithKline, UK)
at 4 mg/kg per os every 12 h and cisapride (Cisapride 5 mg/ml, Summit,
UK) at 0.5 mg/kg per os every 12 h. Assisted feeding with an herbivore
critical care food (Critical Care Herbivore, Oxbow Animal Health,
USA) 25 ml was provided per os every 4 h.
2IMAGING FINDINGS, DIAGNOSIS,
AND OUTCOME
To investigate causes of gut stasis, a helical-64-slice whole body
computed tomographic (CT) study (Somatom Definition AS Siemens,
Erlangen, Germany) was performed without sedation, and with
restraint provided by a VetMouseTrap (Universal Medical Systems
Inc, Solon, USA). Scan settings included a pitch of 1.5, tube potential
of 120 kVp, reference tube current of 160 mA, slice thickness of
1.5 mm, matrix 512 ×512, and reconstruction with low and high fre-
quency algorithms. Scan tube current was modulated by an automatic
Vet Radiol Ultrasound. 2018;1–5. wileyonlinelibrary.com/journal/vru 1
2LONG O ET AL.
FIGURE 1 Postcontrast computed tomographic image of the sacculus rotundus (*) and appendix (arrowhead) in transverse (A) and dorsal plane
(B). B-mode ultrasound image of the sacculus rotundus (C) (8 MHz, wall thickness 0.8 cm), with anechoic and gas content, and of the appendix (D)
(14 MHz, wall thickness 0.6 cm) showing multifocal mucosal speckles and thickened wall (between callipers) [Correction added on 5 March 2018
after first online publication: the position of figures 1 and 2 have been reversed in the text. They were originally published out of order and with
incorrect captions.]
exposure control system (Care Dose 4D, Siemens Medical Solutions,
International). Postcontrast images were acquired within 1 min after
contrast injection and reconstructed with a low frequency algorithm.
A bolus of 740 mg Iodine/kg of nonionic iodinated contrast medium
(Iopamiro, Bracco, Manno, Switzerland) was manually injected through
an auricular angiocatheter followed by 1.5 ml of saline solution flush.
On postcontrast images, a round fluid-filled structure delineated by
a contrast-enhancing wall was detected in the right caudoventral
abdomen along the lesser curvature of the cecum (Figure 1A and B).
This saccular structure contained a small amount of gas and its lumen
projected into the cecal lumen, which was consistent with the location
of the sacculus rotundus. Its wall was markedly thickened (0.77 cm).
Within the left mid-ventral abdomen, an elongated and thickened
(wall thickness 0.4 cm, Figure 1A and B) blind-ending tubular structure
was visible connected to the cecum, consistent with the appendix.
Mild peritoneal effusion and moderate mesenteric lymphadenopathy
(1.2 cm in width) were also identified. The presumptive CT diagnosis
was sacculitis and appendicitis, with associated reactive local lym-
phadenopathy and mild inflammatory peritoneal effusion. Abdominal
B-mode ultrasound was performed (MyLab Twice Esaote, Genova,
Italy) with microconvex (SC 3123) and electronic linear (LA 435) array
probes, with frequencies ranging between 8–14 MHz. Ultrasound
examination confirmed the markedly thickened wall of the sacculus
rotundus (0.8 cm) located dorsal to the cecum, without loss of wall
layering (Figure 1C). A distinct inner mucosal layer was detected, how-
ever heterogeneously hyperechoic and markedly thickened, while the
outer layer was hypoechoic (Figure 1C). Moreover, the appendix had a
moderately thickened wall (0.6 cm) containing numerous hyperechoic
speckles (Figure 1D). At this stage, an inflammatory noninfectious or
infectious sacculitis and appendicitis was suspected, while neoplastic
infiltration was considered less likely due to the extension of the
infiltration and the young age of the animal. Considering the ongoing
anorexia, with lack of response to medical treatment and the high risk
of dysbiosis, an exploratory laparotomy was recommended.
LONG O ET AL.3
FIGURE 2 Intraoperative picture of the appendix (arrow) and sacculus rotundus (asterisk) (A). Histological presentation of the appendix, with
multifocal necrotic granulomas (B, scale bar =1000 𝜇m, Hematoxylin & Eosin). Intraoperative picture of the multifocal wall microabscesses visible
at the level of the appendix (C). Appendix granuloma with necrotic core, a rim of macrophages and neutrophils (D, scale bar =50 𝜇m, Hematoxylin
& Eosin) [Correction added on 5 March 2018 after first online publication: the position of figures 1 and 2 have been reversed in the text. They were
originally published out of order and with incorrect captions.]
At surgery, the segmental thickening was confined to both the sac-
culus rotundus and appendix, with no evidence of wall defect (Fig-
ure 2A and C). Multifocal micro-abscesses were spread throughout
the wall (Figure 2A and C). Full thickness biopsies were taken from
the sacculus rotundus and appendix walls. A firm, pedunculated, irreg-
ular nodule extending into the sacculus rotundus lumen was also
excised. Samples were sent for bacteriology and histopathology. Cul-
ture of the biopsied tissues was negative for specific fungal or bacte-
rial growth, but rather a light, mixed bacterial growth with no predom-
inant organism was identified at the level of the appendix (nonspecific
growth). On histopathology, multifocal, 500–2000 𝜇m wide, round to
oval lesions were scattered in the submucosa of the sacculus rotun-
dus and appendix (Figure 2B and D). These lesions had a large, central
area of lytic necrosis, with loss of cellular detail, hypereosinophilia, and
accumulation of cytoplasmic and nuclear debris. Around the necrotic
core, there was a poorly defined, thick rim of infiltration by large num-
bers of macrophages, with very rare bi-nucleated forms and scattered
neutrophils. The gut-associated lymphoid tissue was diffusely promi-
nent (lymphoid hyperplasia). There was moderate diffused infiltration
of the lamina propria by lymphocytes and plasma cells, and there was
trans-epithelial transmigration of the mucosal epithelium by small to
moderate numbers of heterophils. This presentation led to a histo-
logical diagnosis of severe, chronic, multifocal granulomatous sacculi-
tis, and appendicitis with necrotic heterophilic granuloma formation.
Warthin Starry (silver) and Ziehl Neelsen stains did not reveal specific
infectious agents, and bacterial infection was considered a possible dif-
ferential diagnosis.
Supportive treatment was continued, and additional oral antibi-
otics with trimethoprim sulphate (Sulfatrim 96 mg/ml, Virbac, UK) at
15 mg/kg per os every 12 h and metronidazole (200 mg/5ml, Lexon,
UK) at 20 mg/kg per os every 12 h, were added to the previous
medical therapy. The patient recovered uneventfully from surgery,
with normal gut sounds within 24 h and was discharged after 48
h. At 5 days postdischarge, the owner reported progressive return
to spontaneous eating and normal defecation. At 4 weeks follow-up,
complete regression of the clinical signs was obtained and complete
blood counts were within normal limits. A follow-up abdominal ultra-
sound revealed a moderate decrease in wall thickness of the sacculus
4LONG O ET AL.
rotundus (0.56 cm), although a focal heterogeneous area most likely
consistent with the previous biopsy site was detected. The appendix
appeared partially evaluable and gas-filled. At 6 weeks ultrasono-
graphic follow-up, the wall of the sacculus rotundus (0.3 cm) and
appendix were markedly reduced in thickness, with normal wall layer-
ing and echogenicity.
3DISCUSSION
This case highlights the important roles of CT and ultrasound as com-
plementary modalities for investigating gut stasis in rabbits. Presump-
tive sacculitis and appendicitis was diagnosed on CT based on focal
wall thickening of a saccular structure connected to the cecum. To the
authors’ knowledge, the CT appearance of the sacculus rotundus and
appendix has never been described in the veterinary literature. More-
over,only a single old reference describing the presence of granuloma-
tous appendicitis in rabbits was found.1
Further ultrasonographic examination of the abdomen provided
important additional information confirming the exact location and
nature of the lesion, affecting both the sacculus rotundus and the
appendix. In this patient, the wall thickening of the appendix and saccu-
lus rotundus measured more than twice the normal limits reported on
ultrasound.2Furthermore the diffuse thickening, preserved layering,
and mucosal speckles prompted the presumptive diagnosis of inflam-
matory or infectious disease. A neoplastic process, such as round cell
tumor, was considered less likely because of the young age of the
patient and extensive intestinal infiltrative changes without loss of
wall layering. As previously reported in cats, abnormalities detected on
ultrasonography or endoscopy at the levelof the ileocecocolic junction
should encourage histology for further evaluation. Histopathology was
performed in this case to confirm the imaging diagnosis.3
Due to the lack of information in the literature on the normal CT
appearance of the sacculus rotundus and appendix, ultrasonography
was a crucial complementary tool to confirm the nature of the lesion.
Both structures are small and challenging to detect on B-mode abdom-
inal ultrasound. They can be located in the mid-ventral abdomen at
the level of the umbilical region; however, the proximity of the cecum
hinders identification of these structures due to the distal acoustic
shadowing and gas reverberation from the adjacent cecal content. In
a previous study of 21 healthy mixed-breed dwarf rabbits, the saccu-
lus rotundus was detected in 14/21 patients, while the appendix was
always visible.2In the authors’ experience, the location of the saccu-
lus rotundus on CT is similar in most rabbits in the right caudoventral
abdomen along the lesser curvature of the cecum and it remains visible
in most of animals, while a normal appendix is often more challenging
to identify.
The rabbit cecum is a highly developed and differentiated organ,
compared to the cecum of other species, such as dogs and cats.4–7
The sacculus rotundus is an ampullar distension of the intestine rep-
resenting the distal end of the ileum, located on the first haustral-like
pouch of the corpus ceci. The appendix is located at the caudal tip
of the cecum, similar to humans.8–11 In Angora rabbits, the sacculus
rotundus is described to have a thick wall with a wide lumen, short
thick villi, large amount of crypts, and numerous lymphoid follicles.5
Moreover, on histopathology it differed from other parts of the diges-
tive system and was considered a novel lymphoid organ, because of
its high dense lymphoid accumulation.5,11 The ‘vermiform’ appendix of
the rabbit plays a fundamental role for development of the primary
(preimmune) antibody repertoire. It partially atrophies with age in this
species however it is fundamental for the immunological development
of gut-associated lymphoid tissues.11
Despite representing one of the most common surgical diseases in
children, to the authors’ knowledge, spontaneous sacculitis and appen-
dicitis in rabbits has only been reported once before.12,13 A previous
old publication described the histopathological findings in 25 with
rabbits affected by granulomatous appendicitis, with similar findings in
the sacculus rotundus.1In a more recent publication, an experimental
model of appendicitis was created by ligating the appendix of rabbits
in view of measuring blood markers of acute appendicitis.14 Medical
treatment is commonly included as a suitable alternative in humans
in nonacute and nonperforated cases of appendicitis.3In the rabbit
of this case report, the clinical signs of gastrointestinal stasis and
anorexia were believed to be secondary to the disease. This was
further supported by the prompt response to medical treatment
postsurgical diagnostic biopsies and the complete regression of clinical
and ultrasonographic abnormalities 6 weeks after diagnosis.
The authors speculate that the presence of intramural microab-
scesses is supportive of a potential infectious process as the trigger
of the inflammation. Despite specific stains, no infectious agents were
identified, and culture yielded a light mixed growth, but no specific
prominent organism. A bacterial cause was considered a possibility
given the biopsy results, pyrexia, and neutrophilia. Clostridiosis was
highly unlikely due to the atypical localization of the lesions and lack
of necrohemorrhagic lesions.
In conclusion, granulomatous sacculitis and appendicitis should be
included among the potential causes of gastrointestinal stasis in rab-
bits. In the authors’ opinion, the sacculus rotundus and appendix
should always be assessed during CT or ultrasonographic abdominal
examinations of the rabbit, especially in young patients presenting for
gastrointestinal stasis.
LIST OF AUTHOR CONTRIBUTIONS
Category 1
(a) Conception and Design: Longo M, Thierry F, Richardson J,
Schwarz T
(b) Acquisition of Data: Longo M, Thierry F, Richardson J, Eatwell
K, Pozo Jd
(c) Analysis and Interpretation of Data: Longo M, Thierry F,
Eatwell K, Schwarz T, Pozo Jd, Richardson J
Category 2
(a) Drafting the Article: Longo M
(b) Revising Article for Intellectual Content: Longo M, Thierry F,
Eatwell K, Schwarz T, Pozo Jd, Richardson J
Category 3
(a) Final Approval of the Completed Article: Longo M, Thierry F,
Eatwell K, Schwarz T, Pozo Jd, Richardson J
LONG O ET AL.5
ACKNOWLEDGMENT
The authors would like to thank Dr. Emma Keeble for her kind assis-
tance with the case.
ORCID
Maurizio Longo http://orcid.org/0000-0002-6838-8430
Florence Thierry http://orcid.org/0000-0003-4175-4397
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How to cite this article: Longo M, Thierry F, Eatwell K, Schwarz
T, Pozo Jd, Richardson J. Ultrasound and computed tomography
of sacculitis and appendicitis in a rabbit. Vet Radiol Ultrasound.
2018;1–5. https://doi.org/10.1111/vru.12602
... In addition to its functional purpose, the stomach serves as a reservoir for ingesta, containing 15% of the alimentary tract content. The gastric cardia sphincter has a welldeveloped musculature, which makes rabbits unable to vomit [4,14,15,[18][19][20][21][22][23]35,36]. The small intestine is shorter in rabbits than in other mammal species (around 12% of total gastrointestinal tract volume) and the cecum occupies almost the entire ventral abdominal cavity. ...
... The small intestine is shorter in rabbits than in other mammal species (around 12% of total gastrointestinal tract volume) and the cecum occupies almost the entire ventral abdominal cavity. The cecum starts from the sacculus rotundus, where there is abundant lymphatic tissue, making its wall thicker than the rest of cecum; and it ends in a finger-like, thick-walled, and pale sac, named the "vermiform" appendix [2,15,16,23,24]. The cecum is spiral-shaped and thin-walled comprising around 50% of the digestive tract volume and it is the primary site of digestible fiber fermentation. ...
... In rabbits, GI tract diseases are frequent causes of morbidity and mortality. The proximal duodenum and terminal portion of the ileum are common sites of obstruction due to luminal narrowing [4,6,9] 10, 15,18,[20][21][22][23]. Rabbit Gastrointestinal Syndrome (RGIS) [7,8] is a term that describes a range of clinical signs and concurrent pathologic conditions that affect the digestive system. ...
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... Unlike the examined hamsters and other CLRs, rabbits have ampulla coli as an enlargement of the beginning of the ascending colon (proximal colon). Such an anatomical feature may cause sacculitis and appendicitis in rabbits [99]. ...
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