Open accessarticle ultrasonographic diagnosis of urachal anomalies in cats and dogs retrospective st

veterinary sciences Article

Ultrasonographic Diagnosis of Urachal Anomalies in Cats and Dogs: Retrospective Study of 98 Cases (2009–2019) Francesca Perondi 1 , Caterina Puccinelli 1 , Ilaria Lippi 1, *, Daniele Della Santa 2 , Michelangelo Benvenuti 2 , Tommaso Mannucci 1 and Simonetta Citi 1 1

2

*

Department of Veterinary Sciences, University of Pisa, Via Livornese Lato Monte, 56121 Pisa, Italy; f.perondi87@gmail.com (F.P.); caterina.puccinelli@phd.unipi.it (C.P.); tommy.mannucci@gmail.com (T.M.); simonetta.citi@unipi.it (S.C.) Vet Hospital H24, 50142 Firenze, Italy; danieledellasanta@yahoo.it (D.D.S.); miche-sportster.hd@libero.it (M.B.) Correspondence: ilaria.lippi@unipi.it; Tel.: +39-0502210100

Received: 8 May 2020; Accepted: 25 June 2020; Published: 2 July 2020

Abstract: This retrospective study investigated the prevalence of different urachal anomalies (UA) in cats (n = 60) and dogs (n = 38) and their association with clinical symptoms and urinalysis alterations.

Among UA, the vesicourachal diverticulum was the most prevalent UA diagnosed in both cats (96.7%) and dogs (89.5%): the intramural vesicourachal diverticulum was diagnosed in 76.7% of cats and 71.1% of dogs, followed by extramural vesicourachal diverticulum (20.0% and 18.4% respectively).

In both cats and dogs, bladder wall diffuse or regional thickening was the most prevalent alteration.

The most common alterations of the urinary bladder content were urolithiasis sediment in cats (33.3%) and in dogs (31.6%). Dogs with UA were more often asymptomatic (p = 0.01). No difference was found in cats. Stranguria, hematuria, and urethral obstruction were the most frequently reported clinical signs, while hematuria and leukocyturia were the most prevalent abnormalities at urinalysis.

In conclusion, our study confirmed UA as uncommon, and often incidental findings, with a high prevalence of animals without clinical signs.

Keywords: dog; cat; urachal anomalies; vesicourachal diverticula; ultrasound

1. Introduction The urachus is a fetal connection allowing urine to pass between the developing urinary bladder and the placenta [1–3]. Urachal anomalies (UA) result from failure of the urachus to undergo complete atrophy by the time of birth: at this time it should be nonfunctional and typically look like a fibrous connective tissue remnant connecting the bladder vertex with the umbilicus [4,5]. The factors responsible for incomplete closure and atrophy of the urachus have not yet been defined [5]. UA are relatively uncommon congenital diseases of the lower urinary tract of dogs and cats [3,4,6].

Four different UA have been described in dogs and cats: patent urachus, urachal cysts, vesicourachal diverticula, and urachal sinus (Figure 1) [3,4,6].

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from the bladder apex [3,4]. Vesicourachal diverticula may be classified as intramural or extramural based on their anatomical extent [4,8]. A urachal sinus occurs when the distal part of the urachus remains patent and communicates with the umbilicus. This is often asymptomatic and rarely Vet. Sci. 2020, 7, 84 2 of 12 recognized [4].

Figure 1. Illustration of the different types of urachal anomalies. (a) Normal bladder with a completely atrophied urachus; (b) urachal sinus: the distal part of the urachus remains patent and communicates with the umbilicus; (c) patent urachus: the urachal canal remains patent and connects the bladder to the Figure 1. Illustration the different types ofofurachal anomalies.

Normalpersistent; bladder with a completely umbilicus; (d) urachalofcyst: a focal segment the patent urachus(a) remains (e) vesicourachal atrophied urachus; (b) urachal the distal of thelocated urachusatremains patentvertex and communicates diverticulum (extramural): thesinus: portion of thepart urachus the bladder fails to close, with the umbilicus; (c) patent urachus: the urachal remains patent andbladder; connects bladder to resulting in a blind diverticulum protruding beyond canal the serosal surface of the (f)the vesicourachal the umbilicus; (d) urachal cyst: a focal segment of the patent urachus remains persistent; (e) diverticulum (intramural): in this case the blind diverticulum is limited to the thickness of the vesicourachal bladder wall. diverticulum (extramural): the portion of the urachus located at the bladder vertex fails to close, resulting in a blind diverticulum protruding beyond the serosal surface of the bladder; (f) A patent (ordiverticulum persistent) (intramural): urachus occurs theblind urachal canal remains patent vesicourachal in thiswhen case the diverticulum is limitedfunctionally to the thickness between bladder of thethe bladder wall.and the umbilicus. It is characterized by inappropriate urine loss through the

umbilicus and can also be associated with omphalitis and urinary tract infection [3,4]. Urachal cysts UA when are often conditions that be found incidentallybut at imaging.

Associated develop the under-diagnosed umbilical and bladder ends of themay urachus are obliterated, a focal segment of a clinicalurachus signs may be attributed to [4,7]. urinary tract infectiondiverticulum (UTI) and may be indistinguishable from patent remains persistent A vesicourachal occurs when a portion of the other acquired of lowervertex urinary diseases (LUTD) affected patientsthat canprotrudes be completely urachus locatedcauses at the bladder failstract to close, resulting in a or blind diverticulum from asymptomatic [5,7,9]. the bladder apex [3,4]. Vesicourachal diverticula may be classified as intramural or extramural based In human medicine, the reported incidence urachal anomalies is relatively low, approximately on their anatomical extent [4,8].

A urachal sinusofoccurs when the distal part of the urachus remains one in 5000 for adults (lesswith among TheThis most type of urachal anomaly reported[4]. is a patent and communicates the infants). umbilicus. is common often asymptomatic and rarely recognized patent (47%), followed by urachal cystthat (30%), (18%),incidentally and, least at commonly, UAurachus are often under-diagnosed conditions may sinus be found imaging. vesicourachal diverticulum [7]. In veterinary medicine, the(UTI) prevalence is be unknown, because Associated clinical signs may (3%) be attributed to urinary tract infection and may indistinguishable there are only few studies reviews [3,8,10] case reports [11–13]. from other acquired causes and of lower urinary tractor diseases (LUTD) or affected patients can be completely Although [5,7,9].

UA can be diagnosed by different imaging techniques (ultrasonography, contrast asymptomatic cystography, cystoscopy) is of theurachal most commonly because of its widespread In humanormedicine, the ultrasonography reported incidence anomaliesused, is relatively low, approximately availability absence of among ionizinginfants). radiation exposure [3,6,7,14–16]. one in 5000 and for adults (less The most common type of urachal anomaly reported is a The purposes offollowed the present retrospective study are(18%), to determine the prevalence of the patent urachus (47%), by urachal cyst (30%), sinus and, least(1) commonly, vesicourachal different types of urachal anomaliesmedicine, in cats and (2) the association UA with urinary clinical diverticulum (3%) [7]. In veterinary thedogs prevalence is unknown,ofbecause there are only few signs and urinalysis abnormalities. studies and reviews [3,8,10] or case reports [11–13].

Although UA can be diagnosed by different imaging techniques (ultrasonography, contrast cystography, or cystoscopy) ultrasonography is the most commonly used, because of its widespread availability and absence of ionizing radiation exposure [3,6,7,14–16].

The purposes of the present retrospective study are to determine (1) the prevalence of the different types of urachal anomalies in cats and dogs (2) the association of UA with urinary clinical signs and urinalysis abnormalities.

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2. Materials and Methods Medical records (n = 28,174) of the Veterinary Teaching Hospital of the Department of Veterinary Science (University of 61 Pisa, Italy) and Veterinary Clinical Practice “Vet Hospital H24” (Florence, Italy) between July 2009 and July 2019 were retrospectively reviewed for client-owned dogs and cats with an ultrasonographic diagnosis of urachal anomalies.

For each case with diagnosis of UA, data regarding signalment, history, physical examination and urological clinical findings (hematuria, pollakiuria, stranguria or urinary incontinence), abdominal ultrasound, and urinalysis findings (bacteriuria, leukocyturia, hematuria and crystalluria) were collected from the medical record when available. Patients were considered symptomatic in case at least one of the following signs of lower urinary tract disease was present: hematuria, pollakiuria, stranguria, urinary incontinence. In case none of the symptoms was present, patients were defined as asymptomatic. All cases with uncertain ultrasonographic diagnosis have been excluded.

Ultrasonography was performed using a Toshiba Aplio 400 (Canon Medical Systems Europe B.V., Zoetermeer, The Netherlands), and General Electrics Logiq E, Logiq E R6 and logiq E R7 equipped with 3,5-10 MHz microconvex (8C-RS), 4,5-13 MHz (12L) and 6,7-18 (L8-18i-RS) linear probes; patients were scanned in lateral recumbency.

Ultrasonographic records, images, and videos were reviewed for each patient with urachal anomalies. Data regarding ultrasound appearance of the wall and the content of the urinary bladder were also recorded for each patient. Urachal anomalies were then classified as follows: patent urachus, defined as a fluid-filled tubular structure, extending from the cranioventral bladder wall to the umbilicus; urachal cyst, defined as a thin-walled, fluid-filled structure, cranial to the bladder; vesicourachal diverticulum defined as a fluid filled structure extending from the bladder cranioventrally as a convex out-pouching of the lumen, subclassified as intramural (limited to the thickness of the bladder wall) or extramural (protruding beyond the serosal surface of the bladder) [3,17–19].

Moreover, the presence of other urinary bladder anomalies was also recorded: bladder anomalies were then divided into content anomalies and wall anomalies. Content anomalies were classified as the presence of calculi (intraluminal mobile structures, of variable size, number and shape, with a hyperechoic interface and forming distal shadow); sediment (intraluminal material of variable echogenicity, which layers in the dependent portion of the bladder and suspends with agitation of the urinary bladder); hyperechoic bands (multiple intraluminal suspended hyperechoic strips, compatible with necrotic, fibrinous and haemorrhagic material); and blood clot (free intraluminal nonshadowing structure, of variable size, shape, and echogenicity) [17,18,20]. Wall anomalies were defined as the presence of wall thickening and were classified as diffuse or regional thickening and focal thickening (wall mass extending into the bladder lumen) [17,18].

Urine samples were collected and analyzed within 12 h from collection (IDEXX VetLab UA Analyzer and Idexx UA Strips, Idexx, Milan, Italy). Urinary sediment reports were reviewed to check for the presence of bacteriuria, leukocyturia, hematuria, and crystalluria.

The D’Agostino and Pearson normality test was used to test data for normality using Graphpad Prism 4 (Graph Pad, San Diego, CA, USA). Chi-squared test was used to compare the prevalence of asymptomatic and symptomatic dogs and cats in relation to different urachal anomalies.

3. Results During the study period, 28,174 abdominal ultrasounds (6450 cats and 21,724 dogs) were performed for different clinical indications, resulting in an ultrasonographic diagnosis of UA in 98 cases (60 cats and 38 dogs). The prevalence of UA was 0.93% in cats and 0.18% in dogs.

Most of the cats were of mixed lineage (n = 56, 93.3%), four cats were reported as pure breed represented breed include Persian Cats (2 cats, 3.3%), Ragdoll and Norwegian Forest Cat (one cat each, 1.6%). Forty-six cats (76.7%) were male (6/46 intact male and 40/46 were castrated male) and 14 cats (23.3%) were female (3/14 were intact female and 11/14 spayed female). The median age was 5 years (ranging from 4 months to 15 years), 95% of cats were >1 years. Dogs were represented by

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following dogs, Vet. Sci. breeds: 2020, 7, 84 mixed breed (12 dogs, 31.5%), Boxer (6 dogs, 15.8%), Golden Retriever4 (4 of 12 10.5%), Newfoundlander, English Cocker Spaniel, Labrador Retriever (2 dogs each, 5.3%) and Beagle, German Shepherd dog, Dalmatian, Papillon, American Staffordshire Terrier, Dogue de Bordeaux, the following breeds: mixed breed (12 dogs, 31.5%), Boxer (6 dogs, 15.8%), Golden Retriever (4 dogs, ShihTzu, Jack Russell Terrier, Rottweiler, and Poodle (one dog each, 2.6%). Thirty-one dogs (81.6%) 10.5%), Newfoundlander, English Cocker Spaniel, Labrador Retriever (2 dogs each, 5.3%) and Beagle, wereGerman male (25/31 were castrated male and 6/31 were intact male) and seven (18.4%) were intact Shepherd dog, Dalmatian, Papillon, American Staffordshire Terrier, Dogue de Bordeaux, female.

The median age was 8.5 years (ranging from 2 months to 15 years) and 18% were <1 years ShihTzu, Jack Russell Terrier, Rottweiler, and Poodle (one dog each, 2.6%). Thirty-one dogs (81.6%) old. were male (25/31 were castrated male and 6/31 were intact male) and seven (18.4%) were intact female.

Vesicourachal diverticulum was the most prevalent diagnosed in this studyold. in both cats The median age was 8.5 years (ranging from 2 months to 15 UA years) and 18% were <1 years Vesicourachal diverticulum (96.7%) and dogs (89.5%) (Table 1). was the most prevalent UA diagnosed in this study in both cats (96.7%) and dogs (89.5%) (Table 1).

Table 1. Prevalence of the different type of Urachal Anomalies.

Table 1. Prevalence of the different type of Urachal Anomalies.

Urachal Anomalies Urachal Anomalies diverticulum Vesicourachal

Cats (n = 60)

Cats (n58=(96.7%) 60)

Vesicourachal diverticulum Intramural vesicourachal diverticulum 58 (96.7%) 46/60 (76.7%) IntramuralExtramural vesicourachal diverticulum 46/60 (76.7%) vesicourachal diverticulum 12/60 (20.0%) Extramural vesicourachal diverticulum 12/60 (20.0%) Urachal cysts 2 /60 (3.3%) Urachal cysts 2 /60 (3.3%) Patent urachus 0 Patent urachus 0 Urachal sinus 0 Urachal sinus 0

Dogs (n = 38) Dogs (n = 38) 34 (89.5%) 34 (89.5%) 27/38 (71.1%) 27/38 7/38 (18.4%)(71.1%) 7/38 (18.4%) 3/38 (7.9%) 3/38 (7.9%) 1/38 (2.6%) 1/38 (2.6%) 0 0

Intramural vesicourachal diverticulum was the most prevalent UA diagnosed in both cats (76.7%), and dogs (71.1%).

Thesediverticulum varied in size, thinprevalent anechogenic lines perpendicular to the wall, Intramural vesicourachal wasfrom the most UA diagnosed in both cats (76.7%), in the ventro-cranial portion of the bladder, to formations greater width, up to wall, 0.4–0.5 cm. Its and dogs (71.1%). These varied in size, from thin anechogenicof lines perpendicular to the in the ventro-cranial portion of the bladder, formations of greater width, up toto 0.4–0.5 cm. Its content was content was variable, from anechoic totoslightly corpuscular, in relation the bladder corpuscularity variable, (Figure 2). from anechoic to slightly corpuscular, in relation to the bladder corpuscularity (Figure 2).

Figure 2. Longitudinal ultrasound imageofofthe the urinary urinary bladder showing thethe presence of a of a Figure 2. Longitudinal ultrasound image bladderinina adog, dog, showing presence small (<1 cm diameter), well-defined, fluid-filled, anechoic structure in the cranioventral bladder wall, small (<1 cm diameter), well-defined, fluid-filled, anechoic structure in the cranioventral bladder wall, consistent with intramural vesicourachal diverticulum. consistent with intramural vesicourachal diverticulum.

Extramural vesicourachal diverticulum was diagnosed in 20.0% of cats and 18.4% of dogs. Four out

Extramural diverticulum in 20.0% of catsofand ofbladder dogs. Four of 19 were of vesicourachal large dimensions and extendedwas 1 todiagnosed 2 cm cranially to the serosa the18.4% urinary out of 19 were of large dimensions and extended 1 to 2 cm cranially to the serosa of the apex; 3/19 appeared 0.5–1 cm in diameter, while 12/19 were smaller than 0.5 cm. The wall appearedurinary as bladder apex; 3/19 appeared cm inwas diameter, were smaller than 0.5 cm. The wall a thin hyperechoic line and 0.5–1 the content similar towhile that of12/19 the bladder (Figure 3). appeared as a thin hyperechoic line and the content was similar to that of the bladder (Figure 3).

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Figure 3. Longitudinal ultrasound image of the urinary bladder in a cat, showing the presence of a Figure 3. Longitudinal ultrasound image image ofofthe urinary bladder in a cat, the presence of athe small small (<1 diameter),ultrasound well-defined, fluid-filled, anechoic structure, protruding beyond serosal Figure 3. cm Longitudinal the urinary bladder in ashowing cat, showing the presence of a cm diameter), well-defined, fluid-filled, anechoic structure, protruding beyond thebeyond serosal surface surface of the cranioventral bladder wall, consistent with extramural vesicourachal diverticulum.

The small(<1 (<1 cm diameter), well-defined, fluid-filled, anechoic structure, protruding the serosal of the cranioventral bladder wall, consistent with extramural vesicourachal diverticulum.

The bladder bladder a moderate, diffuse, thickening the extramural wall, with an irregular mucosal surface.

A surface ofpresents the cranioventral bladder wall, consistentofwith vesicourachal diverticulum.

The presents a moderate, diffuse, thickening of the wall, with an irregular mucosal surface. A moderate moderate amountaofmoderate, echogenicdiffuse, sediment is present lumen. material bladder presents thickening of in thethe wall, withShadowing an irregularhyperechoic mucosal surface.

A amount of echogenic sediment is present in the lumen. Shadowing hyperechoic material adhered to the adhered the ventral bladdersediment wall mucosa is also observed, may hyperechoic represent congealed moderatetoamount of echogenic is present in the lumen. which Shadowing material ventral bladder wall mucosa is also observed, which may represent congealed mineralized sediment. mineralized sediment. adhered to the ventral bladder wall mucosa is also observed, which may represent congealed mineralized Urachalsediment. cyst: only five patients (two cats and three dogs) had this UA. Urachal cysts appeared Urachal cyst: only five patients (two and three dogs) had this UA. Urachal cysts as round structures in continuity with cats the bladder wall, with thin and hyperechoic wallsappeared and as round structures inItcontinuity with(two the bladder thin and hyperechoic walls and regular regular margins. was different size,cats from 0.2wall, to 0.5with cm and the content always anechoic Urachal cyst: only fiveof patients and three dogs) had this UA. was Urachal cysts appeared (Figure 4). margins. was of different size, from 0.5 cmwall, and the content was always anechoic (Figure 4). as round It structures in continuity with 0.2 the to bladder with thin and hyperechoic walls and regular

margins. It was of different size, from 0.2 to 0.5 cm and the content was always anechoic (Figure 4).

Figure 4. Longitudinal ultrasound imageofofthe the cranioventral cranioventral part urinary bladder in ain cat,a cat, Figure 4. Longitudinal ultrasound image partofofthe the urinary bladder showing the presence ultrasound of (<1image cm diameter), round, anechoic formation, showing presence ofa asmall small (<1 cmofdiameter), well-defined, thin-walled, anechoic Figure 4. the Longitudinal the well-defined, cranioventral partthin-walled, ofround, the urinary bladder in a cat, cranial to the bladder apex, consistent with urachal cyst.

The urinary bladder is empty. formation, cranial to theof bladder apex, with urachal cyst. Theround, urinary bladder is empty. showing the presence a small (<1consistent cm diameter), well-defined, thin-walled, anechoic

formation, thepresent bladderinapex, consistent with urachal The of urinary bladder is empty.

Patent cranial urachustowas only one mixed-breed dog of 6cyst. months age. The urachal presented

only one mixed-breed dog of the 6 months of age.

The urachal aPatent tubularurachus structurewas and present anechoicin content.

The formation began from bladder and ended at the presented and anechoic The formation from theofbladder andurachal ended Patenta tubular urachus was present in only content. one mixed-breed dog began of 6 months age. The umbilicus (Figurestructure 5). at the umbilicus (Figure 5). and anechoic content. The formation began from the bladder and ended presented a tubular structure at the umbilicus (Figure 5).

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(a)

(b)

(c)

Figure5.5.Longitudinal Longitudinal ultrasound ultrasound images inin a dog.

AA tubular structure (â&#x2030;¤5 (â&#x2030;¤5 mmmm Figure imagesofofaapatent patenturachus urachus a dog. tubular structure diameter)with withaasmall smallamount amountof ofanechoic anechoiccontent content extends extends from from the the cranio-ventral cranio-ventral bladder wall to the diameter) the umbilical region. reactivity ofperitoneal the peritoneal fat and a small quantity of peritoneal are umbilical region.

MildMild reactivity of the fat and a small quantity of peritoneal fluidfluid are present in proximity of the (a) urachus. (a) urachus Terminalpart urachus part the reaching the umbilical (b) inpresent proximity of the urachus.

Terminal reaching umbilical region; (b)region; intermediate intermediate urachus part; (c) urachus part in continuity with the bladder apex. urachus part; (c) urachus part in continuity with the bladder apex.

Nourachal urachalsinus sinus was was diagnosed diagnosed during study.

No duringthe theperiod periodofofthe theretrospective retrospective study.

Twenty-three out of 60 (38.3%) cats did not present bladder content anomalies at ultrasound Twenty-three out of 60 (38.3%) cats did not present bladder content anomalies at ultrasound evaluation, and 28/60 (46.6%) cats did not present any bladder wall anomaly; 20/60 (33.3%) hadhad evaluation, and 28/60 (46.6%) cats did not present any bladder wall anomaly; 20/60 (33.3%) sediment and 30/60 (50%) reported diffuse wall thickening (Table 2). sediment and 30/60 (50%) reported diffuse wall thickening (Table 2).

Eighteen out of 38 dogs (47.4%) did not have any other bladder anomalies at ultrasound evaluation.

Twenty out of 38 dogs (52.6%) had alterations: calculi were the most of urinary bladder content andother wall anomalies in all patients included withprevalent different Table 2. Prevalence content anomaly (13/38, 31.6%), and diffuse thickening was the most prevalent wall anomaly (16/38, type of urachal anomalies.

42.1%) (Table 2).

Urachal Anomalies

Species

Intramural vesicourachal Urachal Anomalies diverticulum

Cats

Urinary Bladder

n

Urinary Bladder

Wall Anomalies Table 2. Prevalence of urinary bladder Content content Anomalies and wall anomalies in all patients included with Calculi 8/45 different type of urachal anomalies.

Diffuse or regional Sediment

Species

Cats

Dogs

Intramural vesicourachal diverticulum

Urinary Blood Bladder Content clot Anomaliesbands Hyperechoic NoCalculi anomalies Sediment Calculi Blood clot Sediment Hyperechoic bands No anomalies No anomalies

15/45 10/28 1/45 8/28 3/45 10/28 18/45

thickening

Urinary Bladder Wall Focal thickening Anomalies

No anomalies

Diffuse or regional Diffuse or regional thickening thickening Focal Focal thickening thickening No No anomalies anomalies

25/45 1/45 n 19/45 25/45

14/28 1/45 4/28 19/45 10/28

Diffuseor orregional regional Diffuse 4/12 14/28 thickening thickening 8/12 Dogs 4/28 No anomalies Focal thickening No anomalies 10/28 Diffuse or regional No anomalies Calculi 1/7 1/7 Dogs thickening 5/12 Diffuse or regional NoCalculi anomalies 6/7 6/7 4/12 No anomalies Cats Sediment 3/12 thickening 8/12 Diffuse or regional Extramural vesicourachal No anomalies 4/12 No anomalies 1/2 Cats Sediment 2/2 thickening Urachal cysts 1/2 diverticulum Diffuse or regional Focal thickening Calculi 1/7 1/7 Dogs thickening Diffuse or regional No anomalies 6/7 6/7 Calculi 1/3 1/3 No anomalies Dogs thickening No anomalies 2/3 2/3 Diffuse or regional No anomalies 1/2 Cats Sediment 2/2 thickening Patent urachus Dogs No anomalies 1/1 No anomalies 1/1 1/2 Focal thickening Urachal cysts Diffuse or regional Calculi 1/3 1/3 Dogs did not have any other bladder anomalies thickening Eighteen out of 38 dogs (47.4%) at ultrasound evaluation.

No anomalies 2/3 2/3 No anomalies Twenty out of 38 dogs (52.6%) had other alterations: calculi were the most prevalent content anomaly Patent urachus Dogs No anomalies 1/1 No anomalies 1/1 Extramural vesicourachal diverticulum

Cats

Calculi Calculi Sediment Sediment No anomalies

15/45 1/45 n 3/45 18/45 8/45

n

5/12

10/28 3/12 8/28 4/12 10/28

(13/38, 31.6%), and diffuse thickening was the most prevalent wall anomaly (16/38, 42.1%) (Table 2).

On cats (38.3%) (38.3%)and and22/38 22/38 dogs (57.9%) no urinary clinical signs (Table Onhistory, history, 23/60 23/60 cats dogs (57.9%) hadhad no urinary clinical signs (Table 3). In 3).

Inparticular, particular, in cats, no statistically significant difference in the percentage patients with or in cats, no statistically significant difference in the percentage of patientsofwith or without clinical signs wassigns foundwas (p =found 0.56) for intramural andintramural extramuraland vesicourachal diverticulum, without clinical (p both = 0.56) for both extramural vesicourachal although a non-significant trend of highertrend percentage of patients withof clinical signs wasclinical noticed. diverticulum, although a non-significant of higher percentage patients with signs was noticed. While in dogs the percentage of animals with no clinical signs was significantly higher

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(p = 0.01) than the percentage of animals with clinical signs, for both intramural and extramural vesicourachal diverticulum.

Table 3. Prevalence of clinical urinary findings in all patients included with different type of urachal anomalies.

Urachal Anomalies

Intramural vesicourachal diverticulum

Extramural vesicourachal diverticulum

Urachal cysts

Patent urachus

Urinary Symptoms

Cats

Dogs

Hematuria Pollakiuria Stranguria Urinary incontinence Asymptomatic Hematuria Pollakiuria Stranguria Urinary incontinence Asymptomatic Hematuria Pollakiuria Stranguria Urinary incontinence Asymptomatic Hematuria Pollakiuria Stranguria Urinary incontinence Asymptomatic

5/45 8/45 13/45 0 17/45 4/12 2/12 4/12 0 5/12 0 1/2 0 0 1/2 0 1/1 0 0 0

3/28 5/28 6/28 3/28 15/28 1/7 1/7 0 0 5/7 0 1/3 0 0 2/3 0 0 0 0 0

For intramural vesicourachal diverticulum, stranguria was the most frequent alteration (28.8% and 21.4% for cats and dogs, respectively), followed by pollakiuria (17.7% for cats and 17.8% for dogs), while 37.7% of cats and 53.6% of dogs were without clinical signs.

Thirteen out of 37 cats (35.0%) and 6/16 dogs (37.5%) with urinary clinical signs were presented in emergency for urethral obstruction.

Fifty-two out of 98 (36 cats and 16 dogs) had urinalysis available for review. Leukocyturia and hematuria were the most prevalent urinalysis anomalies in both cats (24/36, 66.6% and 30/36, 83.3%, respectively) and dogs (12/16, 75.0% and 10/16, 62.5%, respectively). Crystalluria was present in 31.2% of dogs and in 52.7% of cats, while bacteriuria was present, respectively, in 25.0% and 27.8% of dogs and cats. In particular for intramural vesicourachal diverticulum, leukocyturia and hematuria were present, respectively, in 83.3% and 58.3% of dogs, and in 63.3% and 86.6% of cats.

In cats, crystalluria was present in 53.3% of cats with intramural vesicourachal diverticula, 25.0% of cats with extramural vesicourachal diverticula and in one cat with urachal cyst and patent urachus.

Crystalluria was present in 41.6% of dogs with intramural vesicourachal diverticulum, while it was absent in the remaining UA. In cats, crystalluria was due to struvite in 13/16 cats (81.3%) and to calcium oxalate in 3/16 cats (18.7%). In dogs, crystalluria was due to struvite in 3/5 dogs (60.0%), to calcium oxalate in 1/5 dogs (20.0%), and to cystine in 1/5 dogs (20.0%).

4. Discussion Urachal anomalies are uncommon disorders of the urinary bladder, and often incidental findings in veterinary medicine [3â&#x20AC;&#x201C;5,8]. The real incidence is yet unknown because there are only a few case reports [11â&#x20AC;&#x201C;13,21] or reviews [3â&#x20AC;&#x201C;5,10] concerning this topic. Similar to veterinary medicine, the incidence of urachal anomalies in human medicine is relatively low [7,22], with the majority of cases showing no clinical signs, and being diagnosed incidentally [7]. In particular, urachal anomalies are more frequently diagnosed in children, where an incidence of 1 case on 7.610 for patent urachus and 1 case on 5.000 of urachal cyst was reported [22].

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In our study, the prevalence of UA was 0.93% in cats and 0.18% in dogs, similar to what is reported Vet. Sci. 2020, 7, x 8 of 12 in humans. Interestingly, only 5% of cats and 18% of dogs diagnosed with UA were < 1 year old.

In our a median age ofage 5 years (4 months–15 years)years) was reported for cats, a median age of old.

Instudy, our study, a median of 5 years (4 months–15 was reported forand cats, and a median 8.5 years (2 months–15 years) for dogs.

Median age at diagnosis seems higher in veterinary patients age of 8.5 years (2 months–15 years) for dogs. Median age at diagnosis seems higher in veterinary compared to humans.

This finding in agreement with previous in studies veterinary medicine, patients compared to humans.

Thisisfinding is in agreement with studies previous in veterinary in which mean age mean at diagnosis was far above 1 year old1 [4,8].

In a[4,8]. study 24 clinically normal medicine, in which age at diagnosis was far above year old In of a study of 24 clinically cats with radiographic evidence of an intramural vesicourachal diverticulum, a mean age of 2.5 normal cats with radiographic evidence of an intramural vesicourachal diverticulum, a mean age of years waswas reported, while in another study of 149 symptomatic catscats with diverticula, a mean ageage of 2.5 years reported, while in another study of 149 symptomatic with diverticula, a mean 3.7 ± 2.7 years was reported of 3.7 ± 2.7 years was reported[4].

[4].Mean Meanage ageatatdiagnosis diagnosiswas waseven evenhigher higherin in dogs, dogs, where where Groesslinger Groesslinger and colleagues reported a mean age of 10.4 ± 4.4 years, with only 8% of dogs 1 years oldThe [8]. and colleagues reported a mean age of 10.4 ± 4.4 years, with only 8% of dogs < 1 < years old [8].

The authors hypothesize thatincreased the increased median at diagnosis our cohort is related authors hypothesize that the median age atage diagnosis of UAofinUA ourincohort is related to the to the high prevalence of asymptomatic patients.

UA was often an incidental finding in patients high prevalence of asymptomatic patients. UA was often an incidental finding in patients requiring requiring ultrasonography forother reasons other than urinary tract disease. our study the majority of ultrasonography for reasons than urinary tract disease.

In our In study the majority of dogs dogs (57.9%) asymptomatic.

This finding was in agreement a previous study in which (57.9%) were were asymptomatic.

This finding was in agreement withwith a previous study [8], [8], in which the the diagnosis of UA was not associated with clinical signs of UTI in 34% of dogs [8].

In the cats of diagnosis of UA was not associated with clinical signs of UTI in 34% of dogs [8]. In the cats of our our cohort prevalence of asymptomatic subjects was lowerthan thanthat thatfound found in in dogs dogs (38.3%). cohort the the prevalence of asymptomatic subjects was lower (38.3%). In In particular, while the number of dogs with no clinical signs was significantly higher than the number particular, while the number of dogs with no clinical signs was significantly higher than the number of of dogs dogs with with clinical clinical signs, signs, for for both both intramural intramural and and extramural extramural diverticulum, diverticulum, this this difference difference was was not not statistically statistically evident evident in in cats cats (Figure (Figure 6).

6). Unpublished Unpublished clinical clinical experience experience showed showed that that clinical clinical signs signs of of LUTD are a more frequent reason for ultrasonography in feline, rather than in canine patients.

As LUTD are a more frequent reason for ultrasonography in feline, rather than in canine patients. As aa consequence, the number of cats consequence, the number of cats requiring requiring ultrasonography, ultrasonography, with with signs signs of of LUTD LUTD may may be be relatively relatively higher Although it it is is possible higher than than in in dogs. dogs. Although possible that that the the diagnosis diagnosis of of UA UA is is more more frequently frequently associated associated with inin dogs, this finding is difficult to interpret due due to the with clinical clinicalsigns signsofofLUTD LUTDinincats catsthan than dogs, this finding is difficult to interpret tofact the that fact previous data data in cats to few [5,11].[5,11]. that previous in are catslimited are limited tocase few reports case reports

6. Chi squared test of the percentage of cats cats and and dogs dogs with with clinical clinical signs signs and and without without clinical clinical Figure 6. signs, for both intramural and and extramural extramural vesicourachal vesicourachal diverticulum. diverticulum.

In symptomatic symptomaticanimals, animals,hematuria, hematuria, dysuria, pollakiuria, urethral obstruction the dysuria, pollakiuria, andand urethral obstruction werewere the most most commonly reported clinical signs associated with the current literature [4,5,12].

In our commonly reported clinical signs associated with UA in UA the in current literature [4,5,12].

In our cohort cohort of patients, the most prevalent clinical symptoms associated withUA UAwere were stranguria stranguria and of patients, the most prevalent clinical symptoms associated with and pollakiuria, particularly in dogs and cats cats with with intramural intramural vesicourachal vesicourachal diverticula. diverticula. Interestingly, urethral obstruction was present in 35% of of cats cats and and in in 37.5% 37.5% of of dogs dogs with with urinary urinary symptoms. symptoms. It is plausible that in patients with urethral obstruction the diagnosis of UA may be facilitated by a condition plausible that in patients with urethral obstruction the diagnosis of UA may be facilitated by a of bladderof overfill. finding seems in agreement with the results of results a previous of Osborne condition bladderThis overfill.

This finding seems in agreement with the of a study previous study of and colleagues, in which urethral obstruction was reported in the 54.5% in of cats with vesicourachal Osborne and colleagues, in which urethral obstruction was reported the 54.5% of cats with diverticula [4]. diverticula The largest [4]. diverticula were found in catswere withfound complete urethral obstruction, vesicourachal The largest diverticula in cats withoutflow complete urethral supposedly due to the increased intraluminal pressureintraluminal in the bladder lumenin [4]. outflow obstruction, supposedly due to the increased pressure the bladder lumen [4].

Unfortunately, urinalysis was only available in a limited number of dogs and cats. Interestingly, the majority of dogs and cats for which urinalysis was available had signs of inflammation, such as hematuria, leukocyturia and crystals. However, it is to be noted that dogs and cats with urinalysis

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Unfortunately, urinalysis was only available in a limited number of dogs and cats. Interestingly, the majority of dogs and cats for which urinalysis was available had signs of inflammation, such as Vet. Sci. 2020, 7, x 9 of 12 hematuria, leukocyturia and crystals. However, it is to be noted that dogs and cats with urinalysis were thosethose patients for which abdominal ultrasonography was performed to investigate urologic clinical were patients for which abdominal ultrasonography was performed to investigate urologic signs.

Therefore, the prevalence of urinary signs of inflammation may be overestimated. clinical signs. Therefore, the prevalence of urinary signs of inflammation may be overestimated.

Historically,the thediagnosis diagnosisof ofUA UAin inveterinary veterinarymedicine medicinewas wasperformed performedby bythe theuse useof ofdifferent different Historically, imaging techniques, such as ultrasonography, contrast cystography, and cystoscopy [3,14,23]. imaging techniques, such as ultrasonography, contrast cystography, and cystoscopy [3,14,23].

In In previous studies, contrast cystography was used diagnoseUA UA[8,12].

[8,12].According AccordingtotoOsborne Osborneand and previous studies, contrast cystography was used toto diagnose colleagues, positive antegrade cystourethrography and retrograde contrastpositive urethrocystography colleagues, positive antegrade cystourethrography and positive retrograde contrast were considered the procedures of choice for the diagnosis of vesicourachal diverticula [4].vesicourachal In the present urethrocystography were considered the procedures of choice for the diagnosis of study the diagnosis UA wasstudy basedthe on diagnosis abdominalofultrasonography only.

Abdominal ultrasound has diverticula [4]. In theofpresent UA was based on abdominal ultrasonography the advantages to be a routinely available and non-invasive imaging technique.

Similarly, human only. Abdominal ultrasound has the advantages to be a routinely available and non-invasivein imaging medicine, abdominal ultrasound is considered a fast and readily available technique to diagnose UA technique. Similarly, in human medicine, abdominal ultrasound is considered a fast and readily in absence of the risks connectedUA to radiation exposure [7]. However, consider that[7]. the available technique to diagnose in absence of the risks connectedwe to should radiation exposure diagnostic power of abdominal ultrasonography in identifying UA may be reduced by a condition of However, we should consider that the diagnostic power of abdominal ultrasonography in identifying inadequate bladder filling.

In one ofof theinadequate patients ofbladder our study, the diagnosis intramural vesicourachal UA may be reduced by a condition filling.

In one ofofthe patients of our study, diverticulum was made at the second ultrasonography, when the bladder appeared less filled (Figure 7). the diagnosis of intramural vesicourachal diverticulum was made at the second ultrasonography, Therefore, we cannot exclude that small diverticula may be undiagnosed by the use of ultrasonography, when the bladder appeared less filled (Figure 7). Therefore, we cannot exclude that small diverticula in case of inadequateby bladder filling. may be undiagnosed the use of ultrasonography, in case of inadequate bladder filling.

(a)

(b)

Figure Figure7.7. Two Twolongitudinal longitudinalultrasound ultrasoundimages imagesofofthe theurinary urinarybladder bladderofofaadog dogwith withan an intramural intramural vesicourachaldiverticulum. diverticulum.The Theimages imagesshow showtwo twodifferent differentvolumes volumesofofurine urineinto intothe thebladder bladderlumen. lumen. vesicourachal (a)Overly Overly distended: asas a not very visible focalfocal depression in thein cranial-ventral (a) distended: the thediverticulum diverticulumappears appears a not very visible depression the cranialaspect of the bladder, thinning the correspondent bladder wall;bladder (b) ddequately distended: the ventral aspect of the with bladder, withofthinning of the correspondent wall; (b) ddequately diverticulum as an evident, in the cranio-ventral of the bladder. distended: theappears diverticulum appears focal, as an evagination evident, focal, evagination in theaspect cranio-ventral aspect of the bladder.

In our cohort, the vesicourachal diverticulum was the most frequently diagnosed UA, with a prevalence 96.7%the in cats and 89.5% in dogs. In particular, prevalence of intramural In our of cohort, vesicourachal diverticulum was thethe most frequently diagnosedvesicourachal UA, with a diverticulum was 76.7% in cats and 71.1% in dogs.

This was followed by extramural vesicourachal prevalence of 96.7% in cats and 89.5% dogs. In particular, the prevalence of intramural diverticulum diverticulum (18.4% and 20% in76.7% dogs and cats, respectively).

In veterinary medicine,by vesicourachal vesicourachal was in cats and 71.1% in dogs.

This was followed extramural diverticulum diverticulum (both microscopic seemed be the most UA in dogs vesicourachal (18.4%and andmacroscopic) 20% in dogs and cats, to respectively).

In frequent veterinary medicine, and cats [4,8].

For feline patients, one study [24] reported a prevalence of 40% of microscopic vesicourachal diverticulum (both microscopic and macroscopic) seemed to be the most frequent UA diverticula, while another study [4] reported a prevalence of vesicourachal of 22% in in dogs and cats [4,8].

For feline patients, one study [24] reported a prevalencediverticulum of 40% of microscopic cats with urinary symptoms.

For canine patients, one study reported a prevalence of vesicourachal diverticula, while another study [4] reported a prevalence of vesicourachal diverticulum of 22% in diverticulum of 34% [8]. In veterinary medicine, there only one study reporting a different prevalence cats with urinary symptoms.

For canine patients, oneisstudy reported a prevalence of vesicourachal between intramural and extramural (14/33, 33 cats with bladder diverticulum of 34%(19/33, [8]. In57.6%) veterinary medicine, diverticula there is only one42.4%) study in reporting a different

prevalence between intramural (19/33, 57.6%) and extramural diverticula (14/33, 42.4%) in 33 cats with bladder diverticula [4]. In another study of 50 dogs, only 1/17 vesicourachal diverticula was classified as extramural, confirming also in the dog, the lower prevalence of extramural diverticula compared to intramural [8]. Veterinary patients seem to differ from human patients, for whom patent urachus was the most prevalent UA (47%), followed by urachal cyst (30%), and vesicourachal

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diverticula [4]. In another study of 50 dogs, only 1/17 vesicourachal diverticula was classified as extramural, confirming also in the dog, the lower prevalence of extramural diverticula compared to intramural [8]. Veterinary patients seem to differ from human patients, for whom patent urachus was the most prevalent UA (47%), followed by urachal cyst (30%), and vesicourachal diverticulum (3%) [7].

In our study the prevalence of urachal cysts and patent urachus was very low in both cats and dogs.

This finding was in agreement with what was previously described in both case reports [11,21] and reviews [4,5]. The urachal cysts may be under-diagnosed because they are located along the course of the urachus, but they are not necessarily associated and/or adjacent to the bladder, and for example they could be misinterpreted as mesenteric cysts.

No urachal sinus was diagnoses during the period of the retrospective study. One possible explanation could be that the urachal sinus is often associated with non-specific symptoms and is largely asymptomatic unless it develops a complication (most commonly infection). [4,25,26] Another possible explanation could be its anatomical location; indeed, it is not located near the urinary bladder and if asymptomatic it may not be observed during an abdominal ultrasound examination.

In our cohort of patients, UA was frequently associated with other ultrasound alterations of the bladder in terms of content and/or wall anomalies. In both dogs and cats, diffuse or regional thickening was the most prevalent bladder wall alteration. The most common alterations of the urinary bladder content were urolithiasis in dogs and sediment in cats. Similar findings were reported by the study of Osborne and Colleagues [4], in which the most prevalent abnormalities in patients with UA were thickened bladder wall (75%), irregular mucosa (44%), calculi and sediment (33%). These findings, together with unpublished clinical experiences may suggest a potential role of UA in promoting urolithiasis, and/or inflammatory changes of the bladder mucosa. UA may host bacteria, or protein and mineral debris, which may be difficult to clear by the physiologic urine flow. Some studies also reported that macroscopic diverticula may develop from microscopic diverticula, with the concomitant presence of disorders of the lower urinary tract, such as bacterial infections, urolithiasis, urethral plugs, sediment, or idiopathic cystitis. However, the exact relationship between vesicourachal diverticula and other disorders of the lower urinary tract is still unknown [4,27â&#x20AC;&#x201C;30].

This study has some limitations. Due to the retrospective nature of the study, cases with incomplete or uncertain ultrasound diagnosis were excluded from the study. Therefore, it is possible that the exact prevalence of UA may be slightly affected. Data regarding urinalysis were available only for a limited number of subjects. In some cases, urinalysis was not performed as the patients were referred to the hospital only for the ultrasonographic examination, in other cases urinalysis was not included in the initial diagnostic plan. In both cases, the lack of urinalysis might affect our results, in terms of prevalence of signs of urinary inflammation. Moreover, as in the majority of our cases UA were incidental findings, no urine culture was available. The lack of urine culture did not allow us to make any speculation on the prevalence of UTI in these patients. Finally, as abdominal ultrasonography was the only imaging technique used to identify UA, it is possible that some patients with UA were undiagnosed, especially if urinary bladder was inadequately replete, and/or in the case of small diverticula.

5. Conclusions In conclusion, our study confirmed urachal anomalies as uncommon and often incidental findings, with a high number/proportion of patients without urinary clinical signs. When present, clinical signs were mostly characterized by hematuria, stranguria, and/or urethral obstruction. Different from human medicine, UA were diagnosed in dogs and cats of any age, with a lower prevalence in patients < 1 year old. Among different UA, intramural and extramural vesicourachal diverticula were the most prevalent in both canine and feline populations, often associated with other ultrasound signs of bladder inflammation. Abdominal ultrasound is a routinely available and non-invasive imaging technique to investigate UA. However, additional imaging techniques (such as contrast cystography) or repeated abdominal ultrasounds should be considered in the case of inadequate bladder filling and/or in cases of patients with clinical signs where a specific management could be important.

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Author Contributions: Conception, S.C, T.M., D.D.S., M.B.; writing—original draft preparation, F.P.; writing—review and editing, F.P., S.C., I.L., C.P., D.D.S.; statistical analysis, F.P., I.L.; supervision, S.C.; project administration, S.C. All authors have read and agreed to the published version of the manuscript.

Funding: This research received no external funding.

Acknowledgments: The authors thank Alessandro Antonelli for his contribution to realize Figure 1.

Conflicts of Interest: The authors declare no conflict of interest.

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Vet. Med. Small Anim. Clin. 1981, 76, 1745–1747. [PubMed] © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).