9
271 frequency of associated alterations of bile ducts and gallbladder (29.1%) or liver, bile ducts, and gallbladder in infected animals (12.5%) was higher than in animals that did not eliminate eggs (20.8% and 2.1% respec- tively), suggesting that associated sono- graphic alterations should be an indicator of Platynosomum spp. infection. INTRODUCTION Although different trematode species of the families Opisthorchiidae and Dicrocoeliidae can be found in the liver of domestic cats, 1 the genus Platynosomum Looss, 1907 is the most commonly reported. 2 The literature cites P. concinnum, P. illiciens, and P. fas- tosum infecting the gallbladder and bile ducts of cats; however, all these species Ultrasonography in Hepatobiliary Evaluation of Domestic Cats (Felis catus, L., 1758) Infected by Platynosomum Looss, 1907 Márcia Salomão, DVM, MSc * Letícia M. Souza-Dantas, DVM Flavya Mendes-de-Almeida, DVM, MSc Aline S. Branco, DVM Otílio P.M. Bastos, MD, PhD § Franklin Sterman, DVM, PhD || Norma Labarthe, DVM, DSc * KEY WORDS: Platynosomum, diagnosis, hepatobiliary, ultrasonography ABSTRACT Platynosomum -infected cats are common in tropical and sub-tropical regions of the world. The helminths elicit unspecific clini- cal signs that are transitory, but, with the evolution of the disease, they generally reappear with chronic mucous diarrhea or jaundice. Due to the absence of specific clinical signs, in vivo diagnosis relies solely in the detection of operculated eggs in feces. A total of 72 cats were examined by abdom- inal ultrasound and fecal samples and 33% were found to be infected. It was noted that although no individual sonic alteration could be associated with the infection, the Intern J Appl Res Vet Med Vol. 3, No. 3, 2005 * Departamento de Patologia e Clínica Veterinária Universidade Federal Fluminense Niterói, Brazil Curso de Pós-Graduação em Medicina Veterinária, Faculdade de Veterinária Universidade Federal Fluminense Niterói, Rio de Janeiro, Brazil Curso de Pós-Graduação em Ciências Veterinárias, Universidade Federal Rural do Rio de Janeiro Seropédica, Brazil § Instituto Biomédico Universidade Federal Fluminense Niterói, Rio de Janeiro, Brazil || Faculdade de Medicina Veterinária e Zootecnia Universidade de São Paulo São Paulo, Brazil

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frequency of associated alterations of bileducts and gallbladder (29.1%) or liver, bileducts, and gallbladder in infected animals(12.5%) was higher than in animals that didnot eliminate eggs (20.8% and 2.1% respec-tively), suggesting that associated sono-graphic alterations should be an indicator ofP l a t y n o s o m u m spp. infection.

INTRODUCTIONAlthough different trematode species of thefamilies Opisthorchiidae and Dicrocoeliidaecan be found in the liver of domestic cats,1

the genus P l a t y n o s o m u m Looss, 1907 is themost commonly reported.2 The literaturecites P. concinnum, P. illiciens, and P. fas-t o s u m infecting the gallbladder and bileducts of cats; however, all these species

Ultrasonography in HepatobiliaryEvaluation of Domestic Cats(Felis catus, L., 1758) Infected byPlatynosomum Looss, 1907Márcia Salomão, DVM, MSc*

Letícia M. Souza-Dantas, DVM†

Flavya Mendes-de-Almeida, DVM, MSc‡

Aline S. Branco, DVM†

Otílio P.M. Bastos, MD, PhD§

Franklin Sterman, DVM, PhD||

Norma Labarthe, DVM, DSc*

KEY WORDS: P l a t y n o s o m u m, diagnosis,hepatobiliary, ultrasonography

ABSTRACTP l a t y n o s o m u m-infected cats are common intropical and sub-tropical regions of theworld. The helminths elicit unspecific clini-cal signs that are transitory, but, with theevolution of the disease, they generallyreappear with chronic mucous diarrhea orjaundice. Due to the absence of specificclinical signs, in vivo diagnosis relies solelyin the detection of operculated eggs in feces.A total of 72 cats were examined by abdom-inal ultrasound and fecal samples and 33%were found to be infected. It was noted thatalthough no individual sonic alterationcould be associated with the infection, the

Intern J Appl Res Vet Med • Vol. 3, No. 3, 2005

*Departamento de Patologia e Clínica VeterináriaUniversidade Federal FluminenseNiterói, Brazil

†Curso de Pós-Graduação em MedicinaVeterinária, Faculdade de VeterináriaUniversidade Federal FluminenseNiterói, Rio de Janeiro, Brazil

‡Curso de Pós-Graduação em CiênciasVeterinárias, Universidade Federal Rural do Riode JaneiroSeropédica, Brazil

§Instituto BiomédicoUniversidade Federal FluminenseNiterói, Rio de Janeiro, Brazil

||Faculdade de Medicina Veterinária e ZootecniaUniversidade de São PauloSão Paulo, Brazil

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may be synonymous.3 According toTravassos, Freitas, and Kohn4 in Brazil wefind the species P. illiciens (Braun, 1901)Kossack, 1910, P. deflectens ( R u d o l p h i ,1819) Nicoll, 1915, and P. reficiens ( B r a u n ,1901) Travassos, 1916, but only the P. illi-c i e n s parasitizes the bile ducts and gallblad-der of domestic cats. In this study, due tothe controversy regarding nomenclature andthe lack of recent taxonomic studies, weopted for calling the parasitesP l a t y n o s o m u m s p p .

Cats infected with this helminth can befound in tropical and sub-tropical regions allover the world. It has been described in theA n t i l l e s ,5 A u s t r a l i a ,6 the Bahamas,7

M a l a y s i a ,8 New Guinea,2 N i g e r i a ,9

P o l y n e s i a ,2 Puerto Rico,1 0 and in the US inthe states of Ohio,1 1 F l o r i d a ,1 2 and Hawaii.1 3 , 1 4

In Brazil, there is a recognized prevalenceof 37.2%1 5 , 1 6 to 45% in the state of Rio deJaneiro and capable of reaching 56.25%.1 7

Occurrences of P l a t y n o s o m u m spp werealso reported in the state of São Paulo1 8 w i t han incidence of 1.07% to 5.6%.1 9 , 2 0

The life cycle of this parasite is not wellunderstood, but it is common knowledgethat cats acquire them through ingestion ofsmall lizards. The cycle starts with the elim-ination of eggs in the feces of infected cats.In the environment, the eggs are ingested byslugs or snails and within approximately 15minutes miracidia emerge and migrate tothe connective tissue of the mollusks.During the next 28 days, the miracidiadevelop to sporocysts I, generating a greatnumber of sporocysts II, which then migrateto the soil through the breathing pores of themollusks. In the environment, the stage IIsporocysts mature and in 30 days they willcontain cercariae. At this point of the cycle,they can be ingested by paratenic hosts suchas beetles. Lizards or frogs can ingest stageII sporocysts either directly from the envi-ronment or by ingesting the infectedparatenic hosts. In both events, the metacer-cariae will be released and remain encystedin the gallbladder of the intermediate hostuntil being ingested by the final host. A few

hours after the cat ingests the parasitizedintermediary host, the metacercariae migratethrough the minor duodenal papillae to thecommon bile duct. Although rare, somemetacercariae can migrate through theminor duodenal papilla and reach the pan-creas through the side branches of the pan-creatic duct.2 1 The predator instinct of thecats ensures that the cycle completesbecause, even receiving food from theirowners, cats keep their habit of hunting.1 0 , 2 2

Under experimental conditions, the pro-duction of eggs starts 4 to 5 weeks after thecercariae reach the liver. The prepatent peri-od is 8 to 12 weeks. The life expectancy ofthe adult forms, although unknown, is longas is the period of egg production.3 , 2 3 T h epathogenesis of this infection also involvesthe size and number of parasites. Adult par-asites have a flat body of ellipsoid or egg-like shape covered by a thin cuticle, andtheir size varies between 2.9 to 6.7 mm inlength and 0.9 to 1.7 mm in width.4

The clinical signs displayed by the catsvary, and their seriousness depends on thenumber of adult parasites, the time of infec-t i o n ,2 2 and on the individual reaction to para-site aggression.1 0 Under experimentalconditions, it was shown that cats with dis-crete infections (up to 125 parasites) remainclinically asymptomatic while animals with ahigh number of parasites (more than 1000)show lack of appetite and lethargy.1 0 W h e npresent, the clinical signs can be observedbetween the seventh and sixteenth week afterinfection and include lethargy, weight loss,and abdominal tenderness. Jaundice, anorex-ia, and enlargement of the liver may beobserved although most cats show no recog-nizable clinical alterations.1 0 , 2 2−2 4 B e s i d e sbeing unspecific, the signs are transitory, but,with the evolution of the disease, the unspe-cific symptoms generally reappear togetherwith chronic mucous diarrhea or jaundice. Inthis stage of the disease, the animals die inmost cases. Jaundice observed in infectedcats with high parasite load is related to bilestasis due to presence of high number of par-asites in the bile ducts. Hyperplasia or con-

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strictive fibrosis of the bile duct may occur,causing obstruction of bile flow to the duode-n u m .2 The presence of the parasites in thebile tract can favor secondary bacterial con-tamination and contribute to the developmentof cholangitis and liver abscesses andincrease the risk of cholangiocarcinoma andpyogenic cholangitis.2 5−2 8

Due to the absence of specific clinicalsigns, the diagnosis techniques are of spe-cial importance.1 0 Conclusive diagnosis invivo is made through detection of operculat-ed eggs in the feces,2 2 although this dependson the technique employed2 9 and on thenumber of samples examined.1 7 U l t r a s o u n dexamination is the method of choice fordiagnosing jaundice in humans, and its usein veterinary medicine is increasing.3 0 It is,however, a subjective technique because thesame sonographic aspect can appear in dif-ferent diseases and their interpretation isthus dependant on the skills of the operatorand on objective evaluation parameters.3 1 , 3 2

The objective of this project was tostudy the hepatobiliary characteristicsdetectable with ultrasound for obtaining abetter knowledge of evaluation parametersof ultrasound findings in cats infected withP l a t y n o s o m u m s p p .

MATERIAL AND METHODSThe study included domestic cats of morethan 6 months of age3 3 collected from differ-ent parts of urban Rio de Janeiro. These ani-mals were submitted to ultrasonographicand coproparasitological examinations with-in a maximum interval of 60 days.

All the cats were examined with the freeand informed consent of the owners. Thelifestyle of the animals was classified as fol-lows: 1) free, living without direct supervi-sion; 2) semi-confined, living under directsupervision and receiving food regularly butwith access to the streets; or 3) confined,cats held in a household without havingaccess to the streets. The study was con-ducted in a double-blind fashion.

For the ultrasound procedures, the catswere sedated intramuscularly with a combina-

tion of ketamine chlorhydrate (Vetaset®, FortDodge Saúde Animal Ltda., Campinas, Brazil)at the dose of 10 mg/kg and xylazine chlorhy-drate (Rompum®, Bayer do Brasil S.A., SãoPaulo, Brazil) at the dose of 2 mg/kg.3 4

The samples of feces were obtainedfrom the sedated animals after spontaneousdefecation or directly collected from therectum. The samples were transferred toappropriate vials without conserving agentand maintained at 4˚ C for up to 24 hours,then processed using the Faust’s technique.3 5

The ultrasound exams were carried outwith portable bidimensional equipment(General Electrics [GE]® Logiq 100Pro)with multifrequency transducers (1 con-vex of 5.0−7.5 MHz, 1 linear of 7.5−1 0 . 0MHz). Tricotomy was performed with ashaving machine (Shave Machine GoldenA5 Oster® with blade 40). After cleaning thearea with a dry paper towel, ultrasound gelwas applied (Carbogel®). The best imageswere selected and recorded in a videographic printer (Video Graphic PrinterS o n y® UPP 895 MD) with appropriate ultra-sound printing paper (Ultrasound PrintingPaper Sony® UPP-110 HG).

The animals were examined in dorsal aswell as left and right lateral decubitus posi-tion. Images from liver, gallbladder, andbile ducts were taken in longitudinal, trans-versal and oblique plane.

Ultrasonographic CriteriaThe size of the liver was evaluated subjec-tively based on its position in the abdomenin relation to the transducer. The parametersand criteria for evaluation are presented inTable 1.

Statistical AnalysisFor analysis of discrete data frequency wasused. For comparison of 2 proportions, the ztest was used.4 0 Differences were consideredsignificant when P < 0.05.

RESULTSSeventy two animals (33 males and 39females) were included in the study.Thirty-three percent of them (24/72) were

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infected with P l a t y n o s o m u m spp. Thenumber of infected females was higher(38.5%; 15/39) than that of infected males(27.3%; 9/33), although the difference wasnot significant. The lifestyle of the studiedanimals influenced the prevalence of theinfection. There was significant differenceamong the free-living (42%; 21/50) andconfined cats (7.1%; 1/14). The frequencyof infection of the semi-confined cats(28.6%; 2/7) showed no significant differ-ence in comparison to free-living and con-fined cats (Table 2).

The ultrasound findings of the liver,gallbladder (Figure 1), and bile ducts(Figure 2) occurred with similar frequencyin animals that eliminated and those that didnot eliminate eggs of P l a t y n o s o m u m s p p .(Figure 3, Table 3).

The frequency of associated alterationsof bile ducts and gallbladder (29.1%) orliver, bile ducts, and gallbladder in infectedanimals (12.5%) was higher than in animalsthat did not eliminate eggs (20.8% and 2.1%respectively), although the differences werenot significant (Table 4).

Figure 1. Sonographic images of gallbladders (GB) of Platynosomum spp. infected cats. A)Moderate distension, hyperechoic walls (p), and anechoic content; B) Accentuated distension,hyperechoic walls, and echogenic content (c).

Table 1. Parameters and Criteria for Evaluating the Ultrasound Exam of the Liver, Gallbladder,and Bile Ducts of Domestic Cats (Felis catus, L., 1758).Structure Parameters Normal Changed

Dimensions Liver contained Enlargedin the costal arch Reduced

Shape Regular Irregular

Liver Echogenicity Intermediate HyperechoicHipoechoic

Texture Homogeneous HeterogeneousHepatic vessels Gradual reduction Homogeneous and

of diameter more apparent dilation of vesselsDistension Related to ingesta Accentuated

Gallbladder Form Pyriform, oval or round —Walls Not visualized >2 mmContent Anechoic EchogenicDiameter Not visualized >4 mm at the maximum

<4 mm point of distensionBile ducts Course Regular Tortuous

Periductal NWM HyperechoicEchogenicity

NWM = not worth mentioning.

A BGB

cGB p

GBp

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DISCUSSIONThe free-living cats were more frequentlyinfected than the confined cats, suggestingthat a constant and abundant source of foodtogether with restricted access to preyreduced the risk of P l a t y n o s o m u m s p p .infection. The fact that no difference ininfection frequency was observed betweenconfined and semi-confined cats may beattributed to the sample size of semi-con-fined cats.

The number of females eliminating eggswas not higher than that of males although itis to be expected that females get infectedmore often while teaching their offspring toh u n t .4 1 However, it is known that urbanfemales form colonies where the provisionof food is constant and abundant, whilemales either join the female colonies or tran-sit among them.4 2 , 4 3 Thus, the free-roamingfemales living in urban centers only eat preyas a complement and mostly hunt to teach

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Figure 2. Images of bile ducts (BiD) of Platynosomum spp. infected cats. A) Distended, measur-ing 0.6 cm; B) Distended and tortuous with bullet-like shape (in detail, right inferior corner).

Table 2. Distribution of Domestic Cats Infected by Platynosomum spp. (+)* According to Sexand Lifestyle (urban region of Rio de Janeiro).

LifestyleFree Semi-confined Confined Total

Sex +/total % +/total % +/total % +/total %

Male 8/21 38 1/4 25 0/8 0 9/33 27.3Female 13/29 44.8 1/3 33.3 1/6 16.6 15/39† 38.5Total 21/50 42a 2/7 28.5 1/14 7.1b 24/72† 33.3Different letters in columns significant at a level of % (z = 2112; P = 0.035).*Coproparasitological exam.35

†The lifestyle of one of the animals was not reported by the responsible caretaker (female that did not shed eggs ofPlatynosomum spp.).

Figure 3. Photomicrographs of eggs of the genus Platynosomum found in the feces of cats usingFaust’s technique. (A) Egg with poorly visible operculum; (B) Egg with well–defined operculum;(C) Egg with disrupted operculum.

A B

GB

BiD

BiD

BiD

A B C

20µm

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their young, rarely eating the prey but gener-ally offering it to the kittens.4 1 C o n s e q u e n t l y ,it is possible that the first infection withP l a t y n o s o m u m spp. is acquired by the younganimals while learning to hunt.

When analyzing the ultrasonographicparameters in a hepatobiliary system in iso-lation (liver, gallbladder, or bile ducts) andrelating them to the elimination of eggs ofthe parasite, it can be noted that none of thealterations was more frequent in infectedcats than in cats not eliminating eggs (Table3). The changes on the liver such asenlargement and echogenicity of the hepaticparenchyma detected in the ultrasound examwere only observed in animals that did noteliminate eggs.

These alterations normally reflect histo-logical alterations like fibrosis and vacuolardegeneration that can be observed in theultrasound exam in an advanced stage ofliver disease, including disease caused byparasites of the genus P l a t y n o s o m u m.4 4

Thus, in the course of platynosomiasis,lesions probably appear in the ultrasoundexam in an advanced stage of the diseaseand may be dependent on the parasite load.

P l a t y n o s o m u m spp. infection may haveinfluenced the sonographic aspect of thegallbladder walls of the cats, given thathyperechogenicity was more frequent amonginfected cats. This aspect, however, was alsoobserved among animals that did not elimi-nate eggs of the parasite, suggesting thathyperechogenicity: 1) can indicate an unspe-cific inflammatory process; 2) can be an arti-fact of the technique; or 3) can indicateindividual alterations.3 8 , 3 9 Thus, hypere-chogenicity may be due to a series of fac-tors, among them inflammation caused byparasites of the genus P l a t y n o s o m u m.Another alteration of the bile ducts wasechogenic content that, when observed, wasmore frequent in infected cats (71.4%). Thisalteration possibly is a consequence of along fasting period,3 9 , 4 5 and perhaps appearedmore frequently among infected cats due tothe inflammatory process or to partial bileduct obstruction caused by the parasites.

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Furthermore, 3 animals presented withaccentuated distension of the gallbladdertogether with extrahepatic biliary obstruc-tion, not noted in any of the animals of theother group. This emphasizes the possibilityof platynosomiasis being involved in theobstruction of the bile ducts, especially inanimals developing ductal fibrosis as a con-sequence of the presence of adult forms ofthe parasite.2 2

The ultrasound evaluation of the bileducts showed that this structure presentedalterations more frequently (55.5%; 40/72),independently of parasitosis. Consideringonly the infected animals, alterations in thebile ducts were observed in 67% (16/24),emphasizing the importance of examiningthis structure when platynosomiasis is sus-pected, because the bile ducts can enlarge orpresent tortuosity as a consequence ofchronic inflammation or obstruction.3 3 , 4 5

The joint assessment of alterations ofthe gallbladder and bile ducts or liver, gall-bladder, and bile ducts (Table 4) made clearthat, as already suggested, frequencies werehigher in infected animals than in animalsthat did not eliminate eggs.4 4 It has to bepointed out that when comparisons weremade by means of necropsies for diagnosingthe infection, none of the uninfected catspresented lesions in all 3 hepatobiliarystructures and that 89%, if presenting alter-ations, only presented them in 1 structure.4 4

Thus, although the difference was not sig-nificant, associated sonographic alterationsof bile ducts and gallbladder or liver, bileducts, and gallbladder should be an indica-

tor for serial coproparasitological exams asthe elimination of eggs of P l a t y n o s o m u mspp. is weak and intermittent.2 9

Moreover, the low sensitivity of thecoproparasitological exams using only ones a m p l e1 7 may at least in part explain the 12cats that did not eliminate eggs ofP l a t y n o s o m u m spp., but presented with 2 or3 structures with sonographic alterations.Besides, the lesions associated with low par-asite loads (<10 adult forms) may not appearin the ultrasound exams4 4 and some of the 5parasitized animals that did not presentlesions possibly hosted few parasite forms.

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Table 4. Distribution of Domestic Cats Infected by Platynosomum spp. (PL) and PresentingUltrasonographic Alterations of the Liver (L), Gallbladder (GB), and Bile Ducts (BiD) (urbanregion of Rio de Janeiro, May 2003-September 2004).

L GB BiD L/GB L/BiD GB/BiD L/GB/BiD NWM Total+ n 0 3 5 0 1 7 3 5 24

% 0 12.5 20.8 0 4.2 29.1 12.5 20.8 100- n 3 7 12 0 1 10 1 14 48

% 6.2 14.5 25 0 2.1 20.8 2.1 29.1 100Total n 3 10 17 0 2 17 4 19 72

% 4.1 13.8 23.6 0 2.7 23.6 5.5 26.3 100(+) Cats that eliminated Platynosomum spp.; (-) cats that did not eliminate eggs of Platynosomum spp.; NWM = notworth mentioning.

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