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Journal of Ultrasound
https://doi.org/10.1007/s40477-018-0316-3
ORIGINAL ARTICLE
Ultrasound morphology ofcecal appendix inpet rabbits
AnnalisaNicoletti1 · NicolaDiGirolamo2· UlrichZeyen1· PaoloSelleri3· MarcoMasi3· PaoloFonti1
Received: 30 April 2018 / Accepted: 27 July 2018
© Società Italiana di Ultrasonologia in Medicina e Biologia (SIUMB) 2018
Abstract
Purpose Cecal appendix is the terminal part of cecum and is characteristic of rabbit, among domestic animals. The purpose
of this work is to evaluate its morphology upon ultrasound.
Methods A prospective study was planned for the duration of approximately 1year. Rabbits presented in the study period
for abdominal ultrasound with no clinically evident alterations of the gastrointestinal tract were eligible for inclusion in the
study. Abdominal ultrasound was performed under manual restrain with a high frequency linear probe (8–18MHz).
Results Cecal appendix was visualized in 40/42 rabbits (95.2%) with median or left paramedian views. The wall appeared
multilayered in accordance with normal bowel anatomy, and the luminal content showed in all cases an alimentary pattern.
Measurement of appendix wall thickness (AWT) was possible in all 40 rabbits in which the appendix was visualized while
measurement of the appendix diameter (AD) was possible in 39 rabbits. Reference intervals for AWT were 1.1–2.1mm, and
for AD were 3.9–8.8mm. There was a negative correlation between age and AWT (r = −0.35, P = 0.027) and a moderate
positive correlation between AWT and AD (r = 0.71, P < 0.001).
Conclusions Cecal appendix is recognizable via ultrasound in the vast majority of rabbits. We describe the normal morpho-
logical aspect of the appendix and we provide reference intervals for wall thickness and diameter of the appendix, in order
to aid in the diagnosis of disorders of the appendix. The negative correlation between age and AWT indicates lower values
of AWT associated with increasing age that could represent the physiological decrease in the immunitary function of the
appendix in aged rabbits.
Keywords Appendix· Rabbit, ultrasound· Appendicitis· Gastrointestinal stasis
Sommario
Scopo L’appendice cecale rappresenta la parte terminale del cieco e tra gli animali domestici è caratteristica del coniglio.
Lo scopo di questo lavoro è di valutare la sua morfologia in ecografia.
Metodi È stato pianificato uno studio prospettico della durata di circa 1 anno. I conigli presentati per ecografia addominale
nel periodo dello studio e senza alterazioni cliniche evidenti dell’apparato gastro-enterico sono stati inclusi. L’ecografia
addominale è stata effettuata tramite contenimento manuale utilizzando una sonda lineare ad elevata frequenza (8-18MHz).
Risultati L’appendice cecale è stata visualizzata in 40/42 (95,2%) animali utilizzando scansioni mediane e paramediane sinis-
tre. La parete appare pluristratificata in accordo con la normale anatomia intestinale ed il contenuto luminale è rappresentato
in tutti i casi da pattern alimentare. La misurazione dell’AWT è stata possibile in tutti i 40 conigli in cui l’appendice è stata
visualizzata mentre la misurazione dell’AD è stata possibile in 39 conigli. Gli intervalli di riferimento per AWT sono stati
di 1,1-2,1mm e per l’AD di 3,9-8,8mm. È stata evidenziata una correlazione negativa tra l’età e AWT (r = -0,35, P = 0,027)
ed una moderata correlazione positiva tra AWT e AD (r = 0,71, P < 0,001).
Conclusioni L’appendice cecale è un organo riconoscibile attraverso l’ecografia nella maggior parte dei conigli. Descriv-
iamo l’aspetto morfologico dell’appendice e forniamo parametri di riferimento per lo spessore parietale e il diametro
dell’appendice, con lo scopo di facilitare la diagnosi delle patologie dell’appendice. La correlazione negativa tra l’età e
* Annalisa Nicoletti
annalisa_nicoletti@virgilio.it
Extended author information available on the last page of the article
Journal of Ultrasound
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AWT indica valori più bassi di AWT associati all’aumento
dell’età, che potrebbe rappresentare la diminuzione della
funzione immunitaria dell’appendice nei conigli adulti.
Introduction
In rabbits, the gastrointestinal tract is composed of a relatively
large stomach that has a well-developed cardiac sphincter that
prevents vomiting and a pyloric area. The small intestine,
divided in duodenum, jejunum and ileum, ends in a rounded
structure unique to the rabbit called sacculus rotundus. The
wall of the sacculus rotundus has abundant aggregations of
lymphoid tissue in the lamina propria and submucosa. The
rabbit cecum is very large and has a capacity roughly ten times
that of the stomach, constituting around 40% of the total gas-
trointestinal tract [1]. The cecum ends with a cecal appendix,
a thick-walled, blind-ended structure whose wall is rich in
lymphoid tissue. The cecal appendix represents a site for the
antibody diversification in young rabbits and has a secretory
function of water and bicarbonate throughout the life of the
animals. The cecum is followed by the colon, which originates
from an area defined ampulla coli and is divided into proximal
and distal colon by the fusus coli [2, 3].
The rabbit has been used as an experimental model to
study acute appendicitis in humans. In these studies, surgical
ligation of the appendix or the obstruction of the appendix
obtained through the placement of a balloon catheter intro-
duced via cecostomy induced ischemic necrosis or inflam-
matory changes of the organ. These modifications were stud-
ied for their similarity with spontaneous human appendicitis
and to evaluate the response to medical or surgical treatment
[4–6].
Recently, a case of appendicitis and sacculitis in a
9-month-old male rabbit, diagnosed by means of ultrasonog-
raphy and computed tomography, has been reported [7].
Although a previous study reported ultrasonographic
features and size of abdominal organs in healthy rabbits,
including cecal appendix [8], it included a limited number
of cases and no information about the diameter of the organ
and the luminal content was reported.
The purpose of our work is to demonstrate that in nor-
mal condition morphological and structural features of the
appendix are recognizable during basic abdominal ultra-
sonography and to provide reference size for appendix of
gastrointestinal healthy rabbits.
Materials andmethods
A prospective, reference interval, single-center study
was planned for the duration of approximately 1year
(19/12/2016–12/12/2017). All the rabbits that were pre-
sented in the study period for abdominal ultrasound and had
no history and no clinically evident alterations of the gastro-
intestinal tract were eligible for inclusion in the study. Rab-
bits included in the study had no ultrasonographic evidence
of gastrointestinal tract disease. All the rabbits were client-
owned animals. All animals underwent abdominal ultra-
sound examination performed with a GE logiq E9, equipped
with a linear multifrequency hokey stick probe 8–18MHz
with a small parts optimized setting. The animals were
prepared with trichotomy and application of a small quan-
tity of alcohol and ultrasonographic gel. The rabbits were
manually restrained for the duration of the ultrasonographic
examination. A complete abdominal ultrasonographic exam
was performed with the animal in both right and left lateral
recumbency. When possible, the appendix was visualized
in longitudinal and transversal views; wall measures were
taken in longitudinal view because in the authors’ experi-
ence the visibility of the organ and repeatability of measures
were higher. Measures were taken from the interface lumen-
mucosal layer to the serosal one obtaining the wall thickness
and from serosal to serosal layer obtaining the diameter of
the organ (Fig.1).
Statistical analysis
Summary statistics were compiled for measured variables.
Data were analyzed for normality by means of the Sha-
piro–Wilk test. In case appendix wall thickness (AWT)
and appendix diameter (AD) were normally distributed,
ninety percent reference intervals for the variables were
provided. Difference in appendix parameters (AD, AWT)
between male and female rabbits was evaluated by means
of Student t test since the distribution was normal. Corre-
lation between age and appendix parameters and between
Fig. 1 Rabbit, normal appendix, longitudinal view: mucous luminal
pattern. Wall measure from lumen-mucosa interface to sierosal layer
(measure 1). Measure of the appendix diameter (measure 2). The
blind-ended appearance can be noticed (arrows)
Journal of Ultrasound
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AD and AWT was evaluated by calculation of the Pearson
r statistic. Data were analyzed using commercial software
(SPSS statistics v22.0; IBM, Chicago, IL). Two tailed P
values of less than 0.05 were considered significant.
Results
Population summary
A total of 42 pet rabbits were included in the study. The
rabbits were of mixed breed, ranging between 0.5 and 2kg
in weight. Eighteen rabbits were males (9 neutered and
9 intact) and 24 females (17 neutered and 7 intact). The
median age was 54months (2–156).
Visualization andmorphology ofappendix
In two rabbits, it was not possible to identify cecal appen-
dix. In the remaining 40 rabbits, the appendix was visual-
ized and the ultrasonographic examination was allowed to
study wall structure and luminal content. In all cases, the
appendix was visualized through median and/or left para-
median views. The appendix was recognizable as a tubular
structure with a rounded, closed end and a multilayered
wall characteristic of the intestinal tract. In all cases, the
luminal content had an alimentary pattern (Figs.2, 3 and
4), and no appendix had evidence of fluid content. In one
rabbit, the shadow generated from the luminal pattern lim-
ited visualization of the distal wall of the appendix prohib-
iting measurement of AD. Therefore, 40 rabbits had meas-
urement of AWT and 39 rabbits had measurement of AD.
Reference ranges forappendix wall thickness
andappendix diameter
Both AWT and AD were normally distributed (Shap-
iro–Wilk: P = 0.58 and P = 0.91, respectively). On aver-
age, AWT measured 1.5mm (SD: 0.3; range 0.8–2.2).
Male had a mean AWT of 1.53 ± 0.29mm and females of
1.48 ± 0.32mm. The mean difference between male and
female was 0.05mm (95% CI −0.14 to 0.25) and not statis-
tically significant (P = 0.59). Reference intervals for AWT
were 1.1 to 2.1mm. The mean AD was 6.1mm (SD: 1.4;
range: 2.6–9.2). Male had a mean AD of 6.07 ± 1.39mm and
Fig. 2 Rabbit, normal appendix: alimentary luminal pattern. The state
of repletion can be variable and the wall (w) shows an attenuated
echogenicity
Fig. 3 Rabbit, normal appendix in longitudinal (a) and transversal (b)
views: alimentary luminal pattern. The state of repletion can be vari-
able in normal conditions and the wall (w) shows an attenuated echo-
genicity, sierosa is visible as a hyper-echoic linear structure (arrows)
Fig. 4 Rabbit, normal appendix in longitudinal view. In this case,
the appendix shows a higher state of repletion compared to previous
images and the luminal content creates a posterior acoustic shadow
(arrows)
Journal of Ultrasound
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females of 0.07 ± 1.53mm. The mean difference between
male and female was −0.004mm (95% CI −0.96–0.95)
and not statistically significant (P = 0.99). Reference inter-
vals for AD size were 3.9–8.8mm. There was no corre-
lation between age and AD (r = 0.01, P = 0.94) but there
was a weak negative correlation between age and AWT
(r = −0.35, P = 0.027), indicating lower values of AWT
associated with increasing age, and a moderate positive cor-
relation between AWT and AD (r = 0.71, 95% CI 0.53–0.83;
P < 0.001) (Table1).
Discussion
Gastrointestinal stasis is a common condition in rabbits; it is
not related exclusively to pathologies of the gastrointestinal
tract but could be the expression of several problems. As
in other animals as dogs and cats, abdominal ultrasonog-
raphy is an important evaluation in the clinical practice; it
provides useful clinical and operative information in a non-
invasive way. It consents to differentiate mechanical stasis to
functional ones, allowing to detect foreign bodies or indirect
signs of mechanical ileus, as segmental fluid or gas accumu-
lation within the stomach or part of the intestinal tract, and to
individuate signs of inflammatory bowel disease [3, 9, 10].
In our opinion, the evaluation of the appendix has always to
be included in abdominal ultrasound, because pathologies
of the organ are reported [7, 11]. In human medicine, the
visualization of normal appendix on sonography is reported
to appear advantageous in reducing the percentage of false-
negative cases of appendicitis. Moreover, ultrasonography
is considered a readily available, inexpensive, non-invasive
test with a reported sensitivity of 80–94% in the detection
of acute appendicitis [12] and it is the preferred imaging
modality in pregnant woman and in children suspected of
acute appendicitis, because radiation exposure is an impor-
tant concern in managing this kind of patients [13, 14]. Con-
sidering published works in human and veterinary medicine
and the authors’ experience, abdominal ultrasound probably
can help to detect morphological changes that involve the
wall structure and the luminal pattern in course of appendix
diseases. This work wants to focus on the ultrasonographic
features of the appendix in condition of normality; further
studies are necessary to establish the ultrasonographic
changes of the appendix in course of appendicitis. In the
present study, we found a negative correlation between
age and AWT. In young rabbits, the appendix represents
an important site for development of the primary antibody
repertoire. Although the rabbit appendix does not involute,
it changes in appearance, possibly in function, and partially
atrophies with age [15]. We suggest that probably lower val-
ues of AWT associated with increasing age could be related
to the physiological decrease in the immunitary function of
the appendix in aged rabbits.
Conclusions
Based on our study, cecal appendix is recognizable via
ultrasound through median and/or left paramedian views
in the vast majority of rabbits. We describe the normal
morphological aspect of the appendix and we provide ref-
erence intervals for wall thickness and diameter, in order
to aid in the diagnosis of disorders of the appendix. We
found a weak negative correlation between age and AWT
that suggests that lower values of AWT are associated with
increasing age, hypothesis that has to be confirmed with
further studies. We also found a moderate positive cor-
relation between AD and AWT. We suspected that AD is
positively related with the repletion state of the organ and
that can be variable in the same individual. However, fur-
ther research with multiple monitoring of the same rabbits
at different times is required to prove this hypothesis. We
also describe the normal luminal content of the appendix
that in all cases was represented by the alimentary pattern.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval All procedures performed in studies involving animals
were in accordance with the ethical standards of the institution or prac-
tice at which the studies were conducted. This article does not contain
any studies with human participants performed by any of the authors.
Human and animal rights statement All the described animal-related
procedures were conducted according to the Directive 2010/63/EU
of the European Parliament and of the Council of September 22nd
2010 on the protection of animals used for scientific purposes (Art.1,
Par.1, letter “b”), which does not require any approval by the competent
Authorities.
Informed consent Informed consent was obtained from all individual
participants included in the study.
Table 1 Summary of measurements of appendix wall thickness
(AWT) and appendix diameter (AD) obtained in 40 and 39 rabbits,
respectively
Both variables were normally distributed (Shapiro–Wilk > 0.05)
AWT (mm) AD (mm)
Mean 1.51 6.07
Standard Deviation .30 1.45
Minimum .80 2.60
Maximum 2.20 9.20
Journal of Ultrasound
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References
1. Jenkins J (1999) The veterinary clinics of North America. Exotic
animal practice. WB Saunders, Philadelphia
2. Quesenberry KE, Carpenter JW (2012) Ferrets, rabbits and
rodents. Clinical medicine and surgery, 3rd edn. Elsevier/Saun-
ders, section2
3. Selleri P, Di Girolamo T, Collarile T (2017) Medicina e chirur-
gia degli animali esotici, vol 415. Poletto Editore, MI Italia, pp
386–387
4. Nunes FC, Silva AL (2005) Acute ischemic appendicitis in rab-
bits: new model with histopathological study. Acta Cir Bras
20(5):399–404
5. Pieper R, Kager L, Tidefeldt U (1982) Obstruction of appendix
vermiformis causing acute appendicitis. An experimental study
in the rabbit. Acta Chir Scand 148(1):63–72
6. Simsek G, Servinc B, Onlu Y, Hasirci I, Kurku H, Karahan O
(2016) Effect of medical treatment on histological findings in
rabbits with acute appendicitis. Ulus Travma Acil Cerrahi Derg.
22(6):516–520
7. Longo M, Thierry F, Eatwell K, Schwarz T, Pozo JD, Richardson
J (2018) Ultrasound and computed tomography of sacculitis and
appendicitis in a rabbit. Vet Radiol Ultrasound 1–5. https ://doi.
org/10.1111/vru.12602
8. Banzato T, Bellini L, Contiero B, Selleri P, Zotti A (2015)
Abdominal ultrasound features and reference values in 21 health
rabbits. Vet Rec 176:101
9. Penninck D, D’anjou MA (2008) Atlas of small animal ultra-
sonography, 1st edn. Wiley-Blackwell, Ames IA, p 287
10. Baez JL, Hendrick MJ, Walker LM, Washabau RJ (1999) Radio-
graphic, ultrasonographic and endoscopic findings in cats with
inflammatory bowel desease of the stomach and small intestine:
33 cases (1990–1997). J Am Vet Med Assoc 215(3):349–354
11. Fujiwara H, Uchida K, Takahashi M (1987) Occurrence of granu-
lomatous appendicitis in rabbits. Jikken Dobutsu. 36:277–280
12. Rioux M (1992) Sonographic detection of the normal and abnor-
mal appendix. AJR 158:773–778
13. Kazemini A, Reza Keramati M, Fazeli MS, Keshvari A, Khaki S,
Rahnemai-Azar A (2017) Accuracy of ultrasonography in diag-
nosing acute appendicitis during pregnancy based on surgical
findings. Med J Islam Repub Iran. 31:48
14. Sola R Jr, Theut SB, Sinclair KA, Rivard DC, Johnson KM,
Zhu H, St Peter SD, Shah SR (2018) Standardized reporting of
appendicitis-related findings improves reliability of ultrasound in
diagnosing appendicitis in children. J Pediatr Surg. 53(5):984–987
15. Dusso JF, Obiakor H, Bach H, Anderson AO, Mage RG (2000) A
morphological and immunohistological study of the human and
rabbit appendix for comparison with the avian bursa. Dev Comp
Immunol 24:797–814
Aliations
AnnalisaNicoletti1 · NicolaDiGirolamo2· UlrichZeyen1· PaoloSelleri3· MarcoMasi3· PaoloFonti1
1 Diagnostica perimmagini, Centro Veterinario Specialistico,
via S. Giovannini 51-53, 00137Rome, Italy
2 Tai Wai Small Animal andExotic Hospital, 69-75 Chik Shun
street, Tai Wai, Shatin, ShaTin, HongKong
3 Clinica peranimali Esotici, Centro Veterinario Specialistico,
via S. Giovannini 51-53, 00137Rome, Italy