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Parasitol ResDOI 10.1007/s00436-007-0713-6 Crenosoma vulpis in dog: first case report in Italyand use of the FLOTAC technique for copromicroscopicdiagnosis L. Rinaldi & G. Calabria & S. Carbone & A. Carrella &G. Cringoli Received: 12 June 2007 / Accepted: 1 August 2007 Abstract Crenosoma vulpis is a metastrongylid nematode In conclusion, the discovery of C. vulpis for the first time in that infects the bronchi, bronchioles, and trachea of wild a dog in Italy indicates that the fox lungworm should be and domestic canids and various other carnivores. It is considered in the differential diagnosis of respiratory endemic in the red fox population in the north-eastern parts disease in dogs; in addition, the findings of the comparison of North America and in Europe, including Italy. Dogs are study showed that the FLOTAC technique may improve the susceptible to infection with clinical signs consisting ability to accurately diagnose canine lungworm infections.
primarily in a chronic cough. The present paper reports—to the authors’ knowledge—the first case of spontaneousC. vulpis infection in a dog in Italy. In addition, it also reports, for the first time, the use of the FLOTAC techniquefor C. vulpis diagnosis in canine fecal samples, with results Crenosoma vulpis Dujardin 1945, the fox lungworm, is a compared to the following four standard copromicroscopic metastrongylid nematode that infects the bronchi, bron- techniques: the Baermann technique, the McMaster tech- chioles, and trachea of wild and domestic canids and nique, the simple flotation technique, and the Wisconsin various other carnivores (Bihr and Conboy ). It is technique. The results showed that the FLOTAC technique endemic in red fox (Vulpes vulpes) populations in the north- produced mean larvae per gram of feces greater than that eastern parts of North America and in Europe (Sreter et al.
produced by the other more widely used diagnostic tools.
; Nevarez et al. ; Saaed et al. ), including After the treatment of the C. vulpis infected dog with a Italy (Iori et al. ; Manfredi et al. ). Since the first single oral dose of 0.5mg/kg milbemycin oxime, the report in a domestic dog in the UK (Cobb and Fisher clinical signs resolved and the shedding of larvae ceased.
very few cases in dogs in Europe have been reported inliterature, e.g., in Ireland (Reilly et al. ), Switzerland(Unterer et al. and Germany (Barutzki and Schaper Dipartimento di Patologia e Sanità Animale, Infection in dogs appears to be non-lethal with clinical Università degli Studi di Napoli “Federico II”–CREMOPAR signs consisting mainly of chronic cough; diagnosis is based on detecting first-stage larvae in fecal samples using the Baermann technique or fecal flotation techniques (Bihr Dipartimento di Patologia e Sanità Animale, Via della Veterinaria, 1. 80137 Naples, Italy the first case of spontaneous C. vulpis infection in a dog in Italy. In addition, it also reports, for the first time, the use ofthe FLOTAC technique (Cringoli ) for C. vulpis diagnosis in canine fecal samples, with results compared G. Calabria : A. CarrellaMarigliano, Naples, Italy to other four standard copromicroscopic techniques.
A 2-year-old male English Setter from the Campania regionof southern Italy was presented to the referring clinician witha productive cough, a dribbled saliva, and dyspnea. Onauscultation, the dog had increased lung sounds over theentire lung fields. Bronchoscopic examination revealed ahyperemic trachea and a mucopurulent exudate affecting thelower bronchi. Nematode parasites were visible grossly, andthe examination of fluid collected by bronchoalveolar lavagerevealed the presence of adults of C. vulpis, easily identifiedby microscopic examination, as the presence of theirdistinctive horizontal cuticolar ridges at their anterior ends(Fig. Craig and Anderson Georgi and Georgi ).
Fig. 2 C. vulpis first stage larvae at 400× magnification. The larvae Fecal examination by the FLOTAC technique (Cringoli have a straight, pointed tail and their length ranges from 246 and308 μm (Wetzel ) ; see next section) revealed the presence of C. vulpislarvae (95 larvae per gram of feces, LPG; Fig. and thepresence of eggs of Toxocara canis (4,428 eggs per gram of 2. The FLOTAC technique (Cringoli ), a new feces, EPG), Ancylostoma caninum (26 EPG), and Trichuris multivalent copromicroscopic technique in both human The dog was treated with a single oral dose of 0.5mg/kg 3. The McMaster technique (MAFF ), the most milbemycin oxime (Interceptor®, Novartis Animal Health), universally used technique for estimating the number of helminth eggs/larvae in animal feces (Cringoli et al.
Comparison of copromicroscopic techniques 4. The simple flotation technique (MAFF utilized as copromicroscopic technique at most veterinary For the study on the copromicroscopic diagnosis of C.
vulpis, the following five techniques were compared: 1. The Baermann technique, considered as choice tech- nique for the lungworm diagnosis in canids (Bihr and A 1-day fecal sample (130g) was collected from the C. vulpis infected dog and accurately homogenized. First,ten replicates of 10g-based Baermann technique (technique1) were performed and analyzed 24h later. Second, theremaining 30g were suspended in tap water (dilution ratio =1:10). The suspension was then poured through a wiremesh screen having an aperture of 350μm and, afterdiscarding debris and homogenizing, was divided into 40aliquots of 6ml to have ten replicates of each of the fourflotation-based methods (techniques 2, 3, 4, and 5). Alltubes were centrifuged for 2min at 1,500rpm, and thesupernatant was poured off and discarded (MAFF leaving only a pellet in the tube, thus containing 1/6 ofgram of feces. Each tube was then randomly assigned to atechnique. A zinc sulfate solution (specific gravity = 1.200)was used for techniques 2, 3, 4, and 5. This solution waschosen from a battery of 14 solutions with specific gravityranging between 1.200 and 1.450 (Cringoli et al. after a pre-testing study performed on the canine fecal Fig. 1 Anterior end of an adult of C. vulpis at 400× magnification.
Note the presence of the distinctive horizontal cuticolar ridges sample containing C. vulpis larvae (data not shown).
When the FLOTAC or the McMaster technique was used FLOTAC technique was significantly higher (P < 0.05) than (techniques 2 and 3), the tube was filled with the solution to that obtained by all the other four techniques. Statistical the previous 6-ml level and slowly agitated. The resulting differences were observed neither between the mean LPG agitated suspension was then taken up by a pipette to load produced by the Baermann technique and the flotation the two chambers of either the McMaster slide (Weber technique (P = 0.793) nor between the mean LPG produced Scientific International, England, volume = 1.0ml) or one by the McMaster technique and the Wisconsin technique chamber of the FLOTAC® apparatus (volume = 5ml).
When the simple flotation or the Wisconsin technique was used (techniques 4 and 5), the tube was filled with thesolution to 15ml, covered with a coverslip, and left for 15min (technique 4) or centrifuged at 1,500rpm for 10min(technique 5).
European literature reports of C. vulpis in dogs are quitescant. Spontaneous infections have been recently reported in dogs from UK (Cobb and Fisher Ireland (Reilly et al.
and Switzerland (Unterer et al. ); in addition, Data were double-entered and cross-checked, and statistical data from 8,438 dogs from Germany revealed a C. vulpis analyses were performed using version 13 of the SPSS prevalence of 0.9% (Barutzki and Schaper The software for Windows (SPSS; Chicago, USA). Mean, present paper reports, according to the author’s knowledge, standard error (SE) and 25th, 50th, and 75th percentiles of the first case report of C. vulpis infection in Italy, a country LPG values were calculated for the five different tech- where this lungworm has been already reported in red foxes niques. The statistical differences between the mean LPG (Iori et al. Manfredi et al. The infected dog had were analysed using analysis of variance (ANOVA; GLM a typical respiratory disease caused by metastrongylidae. The for repeated measures) in conjunction with the Bonferroni treatment with milbemycin oxime showed full efficacy against C. vulpis—as previously reported by Conboy)—as well as against T. canis and T. vulpis. Besidesmylbemicyn oxime, an anthelmintic currently approved for use in dogs, although there is no label claim for C. vulpis,other successful treatment options against the fox lungworm After treatment, the C. vulpis infected dog made a rapid in dogs include febandazole, febantel, levamisole, diethyl- recovery, with resolution of all clinical symptoms within carbamazine, and ivermectin (Bihr and Conboy ).
14days; in addition, shedding of larvae in feces ceased as The findings of the present paper also provide important revealed by the copromicroscopic examination performed new information on the performance of available methods with the FLOTAC technique, performed at follow-up for the in vivo diagnosis of C. vulpis infection in domestic examination 2weeks after treatment. Further, no more eggs dogs, an infection that might be more widespread than the of T. canis and T. vulpis were found in the dog’s feces.
literature reports suggest (Reilly et al. ). In fact, larvae Table summarizes C. vulpis LPG values (mean, SE, and are not generally detected using the standard fecal flotation percentiles) according to the copromicroscopic technique techniques utilized at most veterinary clinics; thus, a huge used and the multiplication factors utilized for each technique number of C. vulpis infected dogs could be misdiagnosed to obtain LPG values. The mean LPG revealed by the as having allergic respiratory disease (Bihr and Conboy Table 1 LPG values (mean, standard error, and percentiles) of Crenosoma vulpis detected by the five copromicroscopic techniques *Significant differences for different letters (P<0.05).
). In addition, also the Baermann technique, consid- Conboy G (2004) Natural infections of Crenosoma vulpis and Angiostrongylus vasorum in dogs in Atlantic Canada and their ered as choice technique for this lungworm infection, had treatment with milbemycin oxime. Vet Rec 155:16–18 proven negative in a dog with spontaneous infection (Reilly Cox DD, Todd AC (1962) Survey of gastrointestinal parasitism in Wisconsin dairy cattle. J Am Vet Med Ass 141:706–709 In the present study, the FLOTAC technique produced Craig RE, Anderson RC (1972) The genus Crenosoma (Nematoda: Metastrongyloidea) in New World mammals. Can J Zool mean LPG greater than that produced by the other more widely used diagnostic tools, i.e., the Baermann, the Cringoli G (2006) FLOTAC, a novel apparatus for a multivalent faecal McMaster, the simple flotation, and the Wisconsin tech- egg count technique. Parassitologia 48:381–384 nique. For the flotation of the C. vulpis larvae, the zinc Cringoli G, Rinaldi L, Veneziano V, Capelli G, Scala A (2004) The influence of flotation solution, sample dilution and the choice of sulfate solution is recommended as reported by Bihr and McMaster slide area (volume) on the reliability of the McMaster Conboy (and as shown in our pre-testing study on 14 technique in estimating the faecal egg counts of gastrointestinal flotation solutions. It is important to note that flotation strongyles and Dicrocoelium dendriticum in sheep. Vet Parasitol solutions utilized at most veterinary clinics, e.g., sodium Egwand TG, Slocombe JO (1982) Evaluation of the Cornell– chloride (s.g. = 1.200) and sodium nitrate (s.g. = 1.200), Wisconsin centrifugal flotation technique for recovering tricho- produced false negative results or produced very few strongylid eggs from bovine feces. Can J Comp Med 46:133–137 C. vulpis larvae (data not shown). This demonstrates once Georgi JR, Georgi ME (1992) Nematodes. Canine clinical parasitol- again that the type of solution used in the flotation-based ogy. Lea and FebigerPhiladelphiapp 151–209 Iori A, Costantini R, Cancrini G (1990) Parassiti di volpi (Vulpes vulpes) copromicroscopic techniques significantly influences LPG/ provenienti da alcune regioni italiane. Parassitologia 32:153–154 EPG values; solutions having the same density may give MAFF (1986) Manual of veterinary parasitological laboratory tech- different mean LPG/EPG in the helminth egg/larva counts niques. Ministry of Agriculture, Fisheries and Food, Reference Manfredi MT, Giacometti A, Fraquelli C, Piccolo G (2003) Studio The findings of the present paper showed that the della popolazione elmintica in volpi (Vulpes Vulpes) del Trentino FLOTAC technique can be utilized for quantifying lung- worm larva burdens in canine fecal samples because of its Nevarez A, Lopez A, Conboy G, Ireland W, Sims D (2005) higher sensitivity compared to the other more widely used Distribution of Crenosoma vulpis and Eucoleus aerophilus inthe lung of free-ranging red foxes (Vulpes vulpes). J Vet Diagn diagnostic tools; these results thus underscore previous observations made for various parasites of veterinary and Reilly GA, McGarry JW, Martin M, Belford C (2000) Crenosoma vulpis.
human importance (Cringoli ; Rinaldi et al. , the fox lungworm, in a dog in Ireland. Vet Rec 146:764–765 Rinaldi L, Russo T, Schioppi M, Pennacchio S, Cringoli G (2007) (557–561) Passalurus ambiguus. : new insights into copromicro- In conclusion, the discovery of C. vulpis for the first time scopic diagnosis and circadian rhythm of egg excretion. Parasitol in a dog in Italy indicates that the fox lungworm should be considered in the differential diagnosis of respiratory Saeed I, Maddox-Hyttel C, Monrad J, Kapel CM (2006) Helminths of disease in dogs; in addition, the findings of the comparison red foxes (Vulpes vulpes) in Denmark. Vet Parasitol 139:168–179 Sreter T, Szell Z, Marucci G, Pozio E, Varga I (2003) Extraintestinal study showed that the FLOTAC technique may improve the nematode infections of red foxes (Vulpes vulpes) in Hungary. Vet ability to accurately diagnose canine lungworm infections.
Unterer S, Deplazes P, Arnold P, Fluckiger M, Reusch CE, Glaus TM (2002) Spontaneous Crenosoma vulpis infection in 10 dogs:laboratory, radiographic and endoscopic findings. Schweiz Arch Utzinger J, Rinaldi L, Lohourignon LK, Rohner F, Zimmermann MB, Barutzki D, Schaper R (2003) Endoparasites in dogs and cats in Tschannen AB, N’Goran EK, Cringoli G (2007) FLOTAC: a new Germany 1999–2002. Parasitol Res 90:148–150 sensitive technique for the diagnosis of hookworm infections in Bihr T, Conboy GA (1999) Lungworm (Crenosoma vulpis) infection humans. Trans R Soc Trop Med Hyg (in press) in dogs on Prince Edward Island. Can Vet J 40:555–559 Wetzel R (1940) Zur biologie des fuchslungenwurmes Crenosoma Cobb MA, Fisher MA (1992) Crenosoma vulpis. infection in a dog.
vulpis, I. Mitteilung. Archiv. Fur Wissenschaftliche und Praktische

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