Cutaneous Lesions in Dogs With Dirofilaria (Nochtiella) Repens Infestation and Concurrent Tick-borne...

8
© 2002 Blackwell Science Ltd 267 Veterinary Dermatology 2002, 13 , 267– 274 Blackwell Science, Ltd Case report Pruritic dermatitis in dogs with D. repens infestation Cutaneous lesions in dogs with Dirofilaria ( Nochtiella ) repens infestation and concurrent tick-borne transmitted diseases WALTER TARELLO ‘Centro Veterinario Alessandrino’, via Amendola 1, Alessandria, Italy ( Received 29 March 2001; accepted 20 June 2002) Abstract A pruritic dermatitis characterized by the presence of erythema, papules, focal or multifocal alopecia, crusting and nodules was seen in 28 dogs with Dirofilaria repens microfilariae infestation in an endemic area in north-west Italy. Previous unsuccessful nonspecific antipruritic treatments, flea control and restricted diet were recorded in 53.6% of the patients. Both the Knott and the antigen tests were negative for Dirofilaria immitis and Acanthocheilonema reconditum. Concurrent babesiosis and/or canine granulocytic ehrlichiosis was also diag- nosed in many affected dogs. Preliminary treatment of the concurrent diseases was followed by specific filaricide treatment. The cutaneous lesions, although slightly improved with the initial treatment, resolved completely with macro- and microfilaricide treatment. Although D. repens may be an opportunistic pathogen, this parasite should not be considered as harmless as previously thought and its potential pathogenic role in causing cutaneous lesions in dogs should be considered. Furthermore, it has a zoonotic importance as human cases have been reported worldwide. Keywords : dermatitis, Dirofilaria (Nochtiella) repens , dog, microfilaria, skin INTRODUCTION Subcutaneous dirofilariasis due to Dirofilaria repens is a helminthic zoonosis, widely distributed through- out Europe, Asia and Africa, 1 with higher prevalence found in dogs from Sri Lanka (30 – 60%), 2 Iran (60.8%) 3 and Italy (20.5 –25%). 4,5 Among the dirofilariases of zoonotic importance, D. repens is the most frequent and widely distributed, with 782 human cases recorded in 30 countries, 6,7 com- pared with no more than 190 cases associated with D. immitis and approximately 50 cases with D. tenuis. 8 Italy appears to be the country most affected, with the majority of cases centred in the north-west. 7 In humans, an uncommon host, microfilariasis is rare 9 and the adult parasite causes either a benign subcuta- neous cyst or oedema associated with pruritus, urti- caria and painful lesions. 1,6 Microfilariasis has been reported in dogs in those areas of Italy 4,5 in which the climate allows the development of a large population of mosquitoes (intermediate hosts). 1 Dogs, cats, foxes and other wild carnivores (definitive hosts) constitute the sources of infection for humans. 1 The adult worms reside in the subcutaneous connective tissue, 10,11 whereas the micro- filariae are present in the blood without showing a nocturnal periodicity. 12 Subcutaneous dirofilariosis is endemic in some Southern European countries such as Italy, 5 France, 13 Spain 14 and Greece. 15 In north-west Italy, 20.5 and 23.9% of dogs have been found to host D. repens and D. immitis micro- filariae. 5 D. repens infection was also found in cats resid- ing in the same area (20%). 16 It has been suggested that the apparent opportunistic role of D. repens might well explain the presence of asymptomatic carriers, the concurrent observation of nondermatological clinical signs and the development of dermatitis associated with D. repens microfilariasis in a subgroup of parasitized dogs. 17 Since 1954, 18,19 it has been recognized that D. repens (previously believed to be harmless and asymptomatic) is a possible cause of a pruritic dermatitis in dogs. The embolization of micro- filariae, 13 the movement of adults in the subcutaneous tissue, 1 and the immunological response to parasitic stages L3 L5 and/or microfilariae 20 are thought to cause the cutaneous lesions observed in some affected dogs, similar to what happens in dermatitis asso- ciated with aberrant locations of D. immitis . 21 The pathogenicity of the nematode is poorly understood, because: (i) skin lesions appear only in a subset of infected dogs and are not predictable; 11 (ii) the gastrointestinal signs 17,18 and poor performance 17 in symptomatic dogs are not strictly pathognomonic; (iii) classic macro- and microfilaricide treatments seldom produce complete recovery and no specific therapy has been reported to date. 21 There is increasing evidence that the pathogenicity of the parasite may be influenced Correspondence: Walter Tarello, CP1644, 06129 Perugia, Italy. E-mail: [email protected]

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Transcript of Cutaneous Lesions in Dogs With Dirofilaria (Nochtiella) Repens Infestation and Concurrent Tick-borne...

Page 1: Cutaneous Lesions in Dogs With Dirofilaria (Nochtiella) Repens Infestation and Concurrent Tick-borne Transmitted Diseases

© 2002 Blackwell Science Ltd 267

Veterinary Dermatology

2002,

13

, 267–274

Blackwell Science, Ltd

Case report

Pruritic dermatitis in dogs with D. repens infestation

Cutaneous lesions in dogs with

Dirofilaria

(

Nochtiella

)

repens

infestation and concurrent tick-borne transmitted diseases

WALTER TARELLO

‘Centro Veterinario Alessandrino’, via Amendola 1, Alessandria, Italy

(

Received

29

March

2001;

accepted

20

June

2002)

Abstract

A pruritic dermatitis characterized by the presence of erythema, papules, focal or multifocal alopecia,crusting and nodules was seen in 28 dogs with

Dirofilaria repens

microfilariae infestation in an endemic area innorth-west Italy. Previous unsuccessful nonspecific antipruritic treatments, flea control and restricted diet wererecorded in 53.6% of the patients. Both the Knott and the antigen tests were negative for

Dirofilaria immitis

and

Acanthocheilonema reconditum.

Concurrent babesiosis and/or canine granulocytic ehrlichiosis was also diag-nosed in many affected dogs. Preliminary treatment of the concurrent diseases was followed by specific filaricidetreatment. The cutaneous lesions, although slightly improved with the initial treatment, resolved completely withmacro- and microfilaricide treatment. Although

D. repens

may be an opportunistic pathogen, this parasite shouldnot be considered as harmless as previously thought and its potential pathogenic role in causing cutaneous lesionsin dogs should be considered. Furthermore, it has a zoonotic importance as human cases have been reportedworldwide.

Keywords

:

dermatitis,

Dirofilaria (Nochtiella) repens

, dog, microfilaria, skin

INTRODUCTION

Subcutaneous dirofilariasis due to

Dirofilaria repens

is a helminthic zoonosis, widely distributed through-out Europe, Asia and Africa,

1

with higher prevalencefound in dogs from Sri Lanka (30–60%),

2

Iran (60.8%)

3

and Italy (20.5–25%).

4,5

Among the dirofilariases of zoonotic importance,

D. repens

is the most frequent and widely distributed,with 782 human cases recorded in 30 countries,

6,7

com-pared with no more than 190 cases associated with

D. immitis

and approximately 50 cases with

D. tenuis.

8

Italy appears to be the country most affected, withthe majority of cases centred in the north-west.

7

Inhumans, an uncommon host, microfilariasis is rare

9

and the adult parasite causes either a benign subcuta-neous cyst or oedema associated with pruritus, urti-caria and painful lesions.

1,6

Microfilariasis has been reported in dogs in thoseareas of Italy

4,5

in which the climate allows thedevelopment of a large population of mosquitoes(intermediate hosts).

1

Dogs, cats, foxes and other wildcarnivores (definitive hosts) constitute the sources ofinfection for humans.

1

The adult worms reside in thesubcutaneous connective tissue,

10,11

whereas the micro-filariae are present in the blood without showing anocturnal periodicity.

12

Subcutaneous dirofilariosis is endemic in someSouthern European countries such as Italy,

5

France,

13

Spain

14

and Greece.

15

In north-west Italy, 20.5 and 23.9% of dogs havebeen found to host

D. repens

and

D. immitis

micro-filariae.

5

D. repens

infection was also found in cats resid-ing in the same area (20%).

16

It has been suggestedthat the apparent opportunistic role of

D. repens

mightwell explain the presence of asymptomatic carriers,the concurrent observation of nondermatologicalclinical signs and the development of dermatitisassociated with

D. repens

microfilariasis in a subgroupof parasitized dogs.

17

Since 1954,

18,19

it has beenrecognized that

D. repens

(previously believed to beharmless and asymptomatic) is a possible cause of apruritic dermatitis in dogs. The embolization of micro-filariae,

13

the movement of adults in the subcutaneoustissue,

1

and the immunological response to parasiticstages L3

L5 and/or microfilariae

20

are thought tocause the cutaneous lesions observed in some affecteddogs, similar to what happens in dermatitis asso-ciated with aberrant locations of

D. immitis

.

21

Thepathogenicity of the nematode is poorly understood,because: (i) skin lesions appear only in a subset ofinfected dogs and are not predictable;

11

(ii) thegastrointestinal signs

17,18

and poor performance

17

insymptomatic dogs are not strictly pathognomonic; (iii)classic macro- and microfilaricide treatments seldomproduce complete recovery and no specific therapy hasbeen reported to date.

21

There is increasing evidencethat the pathogenicity of the parasite may be influenced

Correspondence: Walter Tarello, CP1644, 06129 Perugia, Italy.E-mail: [email protected]

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268 W. Tarello

© 2002 Blackwell Science Ltd,

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,

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, 267–274

by concurrent infections, such as babesiosis, granulocyticehrlichiosis,

17

leishmaniosis

21

and haemobartonellosis.

16

Our clinical report aims to increase knowledge of thepathogenic role of

D. repens

in canine dermatology.

MATERIALS AND METHODS

Animals

Twenty-eight dogs, living in the province of Alessan-dria in north-west Italy, were presented at the author’spractice, over an eight-month period (spring toautumn 1998) for a pruritic dermatitis. The history,duration of the disease, previous treatments anddermatological and general clinical signs were recorded.Laboratory tests for

Dirofilaria

(Nochtiella)

repens

,

Dirofilaria immitis

and

Acanthocheilonema

(Dipe-talonema)

reconditum

were carried out.All dogs included in this study had: (i) pruritus for

more than one week, (ii) presence of cutaneous lesionsand (iii) microfilariasis caused only by

D. (Nochtiella)repens

. Thirty healthy dogs were also tested for infesta-tion with

Dilofilaria

spp. as a control group.

Laboratory investigations

A blood sample was collected from each dog for Knottconcentration and canine heartworm antigen tests

(Wittness Dirofilaria, Merial). Microfilariae wereidentified by fixation in 2% formalin and examinationusing light microscopy. Six microscopy preparationswere made from each sample. A fresh blood smear,Wright-stained, was also carried out for each dog tocheck for other canine haemoparasites. A test forleishmaniosis (Leishcan 16, ELISA) was carried out insuspected cases.

Follow-up

Follow-up included a clinical re-examination and aKnott test one month after the end of treatment; aphone call to the owners was then made in January2000.

RESULTS

Animals

The history, duration of the disease, previous treat-ments, dermatological and general clinical signs, and theresults of blood tests are reported in Table 1. The ageof the animals ranged between 4 months and 12 years.Their gender was evenly distributed between male andfemale (14/14).

No dog had received preventive medication forheartworm during the last year.

Seven of 30 healthy dogs were found to be carriersof

D. repens

microfilariae in absence of any sign of dis-ease, at the time of their first examination (data notshown). The owners of the infested dogs declined treat-ment at this time. However, three of the seven dogs(identified in the study group as numbers 2, 13 and 22)developed pruritic skin lesions, respectively, 5, 1 and4 months later.

Clinical findings

The clinical signs and the skin lesions are listed inTable 1 and shown in Figs 1–3. All dogs had pruritus,manifested by localized scratching, licking and biting.Two dogs (numbers 5 and 9) showed lesions involvingthe whole surface of the body. Gross lesions includedprimarily erythema (86% of dogs), papules (50%),alopecia (43%) crusts (29%), and nodules (25%).

Figure 1. Nodule on the chest of dog 28 with a serpiginous lesionrepresenting a subcutaneous migration channel (Reproduced withpermission from Rev Méd Vét 1999; 150: 691–702).

Figure 2. Swelling, alopecia and crusting of the hind leg of dog 6. Figure 3. Erythema and alopecia on the hind legs of dog 14.

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Pruritic derm

atitis in dogs with

D. repens

infestation269

Table 1.

Signs, history, clinical findings and results of the laboratory tests in 28 dogs with

Dirofilaria

(Nochtiella) repens

infestation

DogSex, agebreed

Duration ofdisease

Previous tests and/ortreatment outcome Dermatological findings Clinical signs

Knott results* andconcurrent diseases

1 F, 12 years 2 years Corticosteroids, restricted diet, Erythema (FL, LS region) 2

DFR

µ

f.Miniature Poodle desonide lotion (

no benefit

) Babesiosis, CGE2 F, 8 years 2 weeks 3

DFR

µ

f at Knott

test Erythema (LS region, HL) Lethargy 10

DFR

µ

f.English Setter 5 months before Babesiosis, CGE

3 F, 2 years 2 weeks None Erythema, papules, nodules, 9

DFR

µ

f.German Shepherd Dog alopecia (abdomen and HL) Babesiosis

4

, 4 years 3 years Corticosteroids, flea control, Erythema, crusts, alopecia, papules, Conjunctivitis 6

DFR

µ

f.Cocker Spaniel restricted diet (

no benefit

) acantosis (LS region & perineum) Babesiosis, CGE5 F, 10 years 8 years Corticosteroids, cephalosporin, Erythema, crusts, pustulae, alopecia, Conjunctivitis, diarrhoea 14

DFR

µ

f.Crossbreed flea control, restricted diet lichenification (whole body) vomiting Babesiosis, CGE

(

transient relief

;

recurrence

)6 F, 8 years 2 years Corticosteroids, antibiotics, Lumbar erythema, crusts, alopecia, Fever (39.4

°

C) 10

DFR

µ

f.Crossbreed restricted diet, benzodiazepine nodules (HL) Babesiosis

(

transient relief

;

recurrence

)7 F, 9 years 6 years Antibiotics, flea control, Erythema, crusts, alopecia, Lethargy, conjunctivitis, 6

DFR

µ

f.German Shepherd Dog restricted diet (

no benefit

) ulceration on LS region otitis Babesiosis, CGE8

, 10 months 1 month Flea control, restricted diet Erythema, papules, alopecia, Conjunctivitis, otitis 12

DFR

µ

f.Dog de Bordeaux (

no benefit

) nodules (LS region) Babesiosis9 F, 9 years 10 months Enrofloxacin, flea control Erythema, crusts, nodules, Anorexia, conjunctivitis 15

DFR

µ

f.Crossbreed (

no benefit

) papules, lichenification haematuria Babesiosis, CGE(whole body)

10 F, 7 months 3 months Antibiotics, ivermectin Erythema, nodules, papules Lethargy 6

DFR

µ

f.Boxer (

no benefit

) (neck, chest, abdomen, HL and FL) Babesiosis11 F, 2 and a half years 3 months None Erythema, alopecia (chest and Conjunctivitis and 9

DFR

µ

f.Crossbreed ventral side of the neck) coughing Babesiosis

12

, 9 years 4 months Antibiotics (

no benefit

) Erythema, alopecia, papules, Fever (39.5

°

C) and 6

DFR

µ

f.German Shepherd Dog pyoderma (HL) lymphadenopathy Babesiosis, CGE,

and TW13

, 6 months 2 weeks 7

DFR

µ

f. at Knott’s test Papules on abdomen Anorexia, coughing 11

DFR

µ

f.Crossbreed 1 month before diarrhoea, vomiting Babesiosis

14 F, 12 years 2 weeks None Erythema, alopecia (HL) 6

DFR

µ

f.German Shepherd Dog Babesiosis

15

, 8 months 1 month None Erythema, pustulae (abdomen) Anorexia, conjunctivitis 10

DFR

µ

f.Shih-tzu Babesiosis

16

, 1 and a half year 1 month None Erythema, crusts (LS region) Anorexia 6

DFR

µ

f.Siberian Husky Babesiosis

17 F, 4 years 1 years Antibiotics, restricted diet Erythema on abdomen Lethargy, seizures, 9

DFR

µ

f.Boxer (

no benefit

) asthma, fever (39.3

°

C), Babesiosisconjunctivitis and otitis

18 F, 2 years 2 weeks None Erythema, papules Conjunctivitis, lymph 7

DFR

µ

f.German Shepherd Dog (elbows, abdomen) adenopathy, fever (41

°

C) CGE19

, 10 years, 1 month None Papules (abdomen, LS region) Polydipsia, asthma, 10

DFR

µ

f.Boxer conjunctivitis Babesiosis, CGE

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274

20 , 2 and a half year 6 months Antibiotics, restricted diet Erythema, crusts, alopecia, Anorexia, vomiting, 9 DFR µf.Yorkshire Terrier (no benefit) papules (LS region, hocks) fresh blood on stool, Conjunctivitis Babesiosis, CGE

21 F, 6 years, 1 month Antibiotics, omeprazole Erythema (FL, perineal) Conjunctivitis and 8 DFR µf.Crossbreed (no benefit) lameness Babesiosis

22 , 4 years, 2 weeks 6 DFR µf. at Knott test Erythema, papules 9 DFR µf.Dachsund 4 months before (abdomen and LS region) CGE

23 , 1 years 3 months Enrofloxacin, flea control Erythema (neck and chest), Conjunctivitis and otitis 19 DFR µf.Pittbull Terrier restricted diet, amitraz pyoderma intertrigo, acne CGE and

(no benefit) of the chin Leishmaniosis24 F, 4 years 4 years Corticosteroids, flea control, Erythema, alopecia, papules, Epilepsy, chronic otitis, 9 DFR µf.

Fox Terrier restricted diet, phenobarbital (elbows, chest, perineum) conjunctivitis Babesiosis, TW25 , 5 years 3 months Costicosteroids, antihelmintics, Erythema, alopecia (head, Epilepsy, vomiting, 6 DFR µf.

Pomeranian (no benefit) chest, LS region, HL) conjunctivitis Babesiosis,CGE and TW

26 F, 4 months 2 weeks None Papules, nodules, crusts (HL) 16 DFR µf.Bloodhound Babesiosis

27 , 5 years 2 weeks None Erythema (abdomen, HL) Polydipsia 7 DFR µf.Bichon Frisé Hepatozoonosis and CGE

28 , 4 years 2 weeks None Papules, nodules, serpiginous Lethargy, anorexia, 12 DFR µf.Bloodhound lesion on neck and chest conjunctivitis Babesiosis

(subcutaneous migration channel) Adult nematodeand 2 larvae in a nodule

CGE, Canine granulocytic ehrlichiosis; DFR, Dirofilaria repens; FL, forelimbs; HL, hindlimbs; LS, lumbosacral; µf, microfilariae; TW, tapeworm.

*All dogs were Dirofilaria immitis negative using both the Knott and the antigen test.

DogSex, agebreed

Duration ofdisease

Previous tests and/ortreatment outcome Dermatological findings Clinical signs

Knott results* andconcurrent diseases

Table 1. continued

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Pruritic dermatitis in dogs with D. repens infestation 271

Affected regions included the lumbosacral area(43%), abdomen (40%), hind limbs (40%), chest (25%),neck (21%), forelimbs (18%), perineum (18%), elbows(14%), head (14%) and hocks (10%).

The principal additional clinical signs includedconjunctivitis (57%), anorexia (21%), lethargy (18%),vomiting (14%) and pyrexia (14%).

Laboratory investigationsMicroscopy examination of six slides from every Knottconcentration test was carried out and D. (Nochtiella)repens microfilariae were found in the blood of alldogs (Fig. 4), their count ranging from 2 to 19 per sample.An adult female and two L4 larvae were recoveredfrom a nodule on the neck of dog 28 (Fig. 5). D. immitisand A. reconditum were not found and the test forheartworm antigen was negative in all dogs.

Concurrent infection with babesiosis was diagnosedin 25 dogs (89%), canine granulocytic ehrlichiosis(CGE) in 14 (50%), tapeworm in 3 (11.4%), hepatozo-onosis in 1 (3.5%) and leishmaniosis in 1 (3.5%).

TherapyTherapy for the concurrent conditions (Babesia spp.,Ehrlichia spp. and Hepatozoon canis infections) wascarried out before treating the dogs with the filaricide

therapy, using a combination of imidocarb dipropionate(Carbesia, Schering-Plough Animal Health, 7.13 mg kg−1,subcutaneously, once a week, for four treatments) anddoxycycline (Ronaxan, Merial, 10 mg kg−1, orally, for21 days). A dog with a concurrent infection withLeishmania spp. was initially treated with amminosidine(Amminofarma, Centralvet-Vetem, 10 mg kg−1, sub-cutaneously, twice a day for 10 days). Three dogs alsoinfested with Taenia spp. were initially treated withpraziquantel (Droncit, Bayer, 5 mg kg−1, subcutaneously).

Treatment with imidocarb dipropionate and doxy-cycline resolved the systemic clinical signs, such aslethargy, conjunctivitis, anorexia, vomiting and fever. Asignificant, concurrent improvement of the cutaneouslesions and pruritus was also observed in all dogsincluding that one treated for leishmaniosis.

The macrofilaricide treatment using melarsomine(Immiticide, Rhone-Mérieux, 2.5 mg kg−1, intramus-cularly, twice every 24 h) was initiated 2–3 days aftercompleting the therapy for babesiosis and ehrlichiosisand this led to further improvement of the cutaneouslesions including pruritus (Fig. 6). The speed of therecovery depended on the duration of the disease andthe severity of the lesions. Ten days later, treatmentwas completed with the microfilaricide, ivermectin(Ivomec, Merial, 50 µg kg−1 given subcutaneously as asingle injection).

Follow-upClinical re-examination and a Knott test, carried outone month after the completion of treatment, showedthe resolution of the cutaneous lesions and the absenceof D. repens microfilariae in the blood.

Recurrences of cutaneous lesions and pruritus werereported, during the following year (1999) in only threedogs (numbers 11, 19 and 26) whose owners neglected tocarry out the preventive treatment with oral ivermectin.

DISCUSSION

This study describe 28 cases of canine pruritic derma-titis associated with Dirofilaria repens microfilariae in

Figure 4. Dirofilaria repens microfilaria (Knott test, ×10).

Figure 5. A living adult female and two L4 larvae of Dirofilariarepens from a nodule on the neck of dog 28 (Reproduced withpermission from Rev Méd Vét 1999; 150: 691–702).

Figure 6. Complete dermatological remission 6 months after theend of therapy for Dirofilaria repens infection in dog 14.

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the blood. The animals were examined in north-westItaly where dirofilariasis is endemic. The province ofAlessandria has the highest number of human sub-cutaneous dirofilariasis cases of all Italian provinces1,6

and is apparently the most affected area in the world.7

Clinical signs of D. repens infestation are claimed tobe present in only a small percentage of parasitizeddogs.11 However, three of the seven control dogs devel-oped pruritic skin lesions within 5 months, indicatingthat parasitized dogs can eventually develop diseaseand that the occurrence of cutaneous lesions in infesteddogs in frequent in endemic areas.

Dogs show seasonal variations in the number ofmicrofilariae in the blood, with the highest concentra-tions in August and September.22,23

The large number of microfilariae may be associatedwith clinical signs19 probably caused by mechanical,toxic and immunomediated mechanisms.23,24 The deve-lopment of allergic and auto-immune reactions, includ-ing cutaneous lesions, is possible in helminthoses,depending on the number of parasites, the recurrenceof infestation, and the age and nutrition status of theanimal.24

In northern Italy, the potential vectors for dogsappear to be Aedes caspius, Aedes vexans, Aniphelesmaculipennis, Culex modestus and Culex pipiens.1

Mosquitoes suck the blood of definitive hosts (dogs,cats and wild carnivores) ingesting microfilariae (L1),which develop into L2 and infesting L3 larvae within15–20 days. The larvae migrate into the head, reach thelabium and penetrate successively, during a blood meal,into the subcutaneous tissues of a dog, where theyremain for ≈ 6 months before developing into adults.17

The pathogenesis of cutaneous lesions caused byD. repens in humans is attributed to the migration ofthe adult nematodes in the subcutaneous tissue, thuscausing itching and pain.1,6 The same mechanism hasbeen suspected, but not proven, in dogs.25 In thiscase series, disappearance of pruritus (scratching, lickingand/or biting) was the most striking feature of thebenefical macrofilaricide treatment in all animals.

In 24 (85%) of the 28 cases, the part of the body mostaffected by the dermatitis were the lumbo-sacral andthe perineal areas and the hind legs. The flanks, backand the rear limbs are commonly considered the pre-ferential sites of dwelling for both the larvae and adultswhich may concentrate in large numbers in a singlearea.25

Concurrent infection with other pathogens in dogswith D. repens infestation has been reported.3,13,21

Babesiosis and CGE were the most common in thisstudy and all animals were found to be infected with atleast one of these agents. It is questionable whether thecutaneous lesions are due only to the dirofilariasis asthe other protozoal and bacterial diseases have beenreported either anecdotically or in scientific studiesto be associated with cutaneous lesions.26 Concurrentinfections with different pathogens may contributeto the severity of the clinical signs, thus making theclinical presentation unusual.

It is not possible to prove that the skin lesions seenin the dogs in this study were directly caused by themicrofilariae or by the adult stages of D. repens, but itshould be noted that: (i) 15 dogs had previously beenunsuccessfully treated with several antipruritic thera-pies; (ii) none had been treated for the concurrentdiseases; (iii) all patients recovered after specific treat-ment initially against the concurrent diseases but withfurther improvement following treatment of the diro-filariosis. The dermatological signs found in the caninecases described here were similar to the few other casesof subcutaneous dirofilariasis reported sporadicallyover the past 50 years.10,11,13,17–19,21,25

Mixed infections with Dirofilaria immitis, which isseen in 11.7% of the cases in the geographical area inwhich this study was carried out, were not includedin this study. It is possible that an aberrant migration ofD. immitis larvae could not be completely ruled out, asD. immitis-associated dermatitis have been reportedin dogs.20 An occult disease, due to the absence ofcirculating microfilariae and/or false negative D. immitisantigen test, may occur when the number of adults islow. The combination of the Knott test and the antigentest improves accuracy, as demonstrated by Hooveret al.27 Thus, the possibility of misdiagnosis in thisstudy is unlikely.

The endemic distribution of D. repens in the studyarea is well known to clinicians,7 but its pathogenic roleis still poorly understood, as most textbooks describeit as a harmless worm residing in the subcutaneousconnective tissue.28,29

In endemic areas concentration tests (Knott andfiltration) to look for D. immitis and D. repens micro-filariae should be carried out routinely, possibly coupledwith serological tests.

Differentiation among D. immitis, D. repens andAcanthocheilonema reconditum is based mainly onthe morphology of the microfilariae. The microfilariaeobserved in this study had the typical wide aspectof D. repens larvae. On the Knott test, the tails ofA. reconditum are hook-shaped and normally thin likethose of D. immitis.30 The caudal end of D. repensmicrofilariae is much wider. The concentration testis thus very useful to clinicians in order to assess thepresence of D. repens in dogs with pruritic dermatitis.In such cases, dirofilariosis should always be includedin the differential diagnosis of dogs with pruriticdermatitis in endemic areas. The potential role ofD. repens infestation in the development of pruriticdermatitis requires reappraisal and further study.

REFERENCES

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2. Dissanaike, A.S., Abeyewickreme, W., Wijesundera, M.S.et al. Human dirofilariasis caused by Dirofilaria

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(Nochtiella) repens in Sri Lanka. Parassitologia 1997; 39:375–82.

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7. Pampiglione, S., Rivasi, F., Angeli, G. Dirofilariasisdue to Dirofilaria repens in Italy, an emergent zoonosis.Report of 60 new cases. Histopathology 2001; 38: 344–54.

8. Canestri Trotti, G., Pampiglione, S., Rivasi, F. Thespecies of the genus Dirofilaria Railliet & Henry, 1911.Parassitologia 1997; 39: 369–74.

9. Nozais, J.P., Bain, O., Gentilini, M. Un cas de dirofilari-ose à Dirofilaria (Nochtiella) repens avec microfilarémieen provenance de Corse. Bulletin de la Société de Patho-logie Exotique 1994; 87: 183–5.

10. Hubert, B. Cas cliniques: helminthoses canines à mani-festations cutanées. Point Vétérinaire 1985; 17: 43–8.

11. Bredal, W.P., Gjerde, B., Eberhard, M.L. et al. AdultDirofilaria repens in a subcutaneous granuloma on thechest of a dog. Journal of Small Animal Practice 1998; 39:595–7.

12. Webber, W.A.F., Hawking, F. Experimental maintenanceof Dirofilaria repens and Dirofilaria immitis in dogs.Experimental Parasitology 1955; 4: 143–64.

13. Chauve, C. Importance in France of the infestation byDirofilaria (Nochtiella) repens in dogs. Parassitologia1997; 39: 257–83.

14. Cancrini, G., Allende, E., Favia, G. et al. Canine diro-filariosis in two cities of southeastern Spain. VeterinaryParasitology 2000; 92: 81–6.

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17. Tarello, W. La dirofilariose sous-cutanée à Dirofilaria(Nochtiella) repens chez le chien. Revue bibliographique

et cas clinique. Revue de Médecine Vétérinaire 1999; 150:691–702.

18. Ajmerito, G. Contributo allo studio della filariosicutanea del cane. Annali Della Facoltà Di MedicinaVeterinaria Di Torino 1954; 4: 443–9.

19. Scarzi, M. La dirofilariosi cutanea del cane. Obbiettiviand Documenti Veterinari 1995; 6: 11–15.

20. Mozos, E., Ginel, P.J., Lopez, R. et al. Cutaneous lesionsassociated with canine heartworm infection. VeterinaryDermatology 1992; 3: 191–6.

21. Beaufils, J.P., Martin-Granel, J. Polyparasitisme chez unchien, avec passage de leishmanies dans le sang circulant.Pratique Médicale et Chirurgicale Des Animaux deCompagnie 1987; 22: 381–5.

22. Worms, M.J. Circadian and seasonal rhythms in bloodparasites. In: Canning, E., Wright, C.A., eds. Behav-ioural Aspects of Parasite Transmission. New York:Academic Press, 1972: 53–67.

23. Cancrini, G., Coluzzi, M., Balbo, T. et al. Seasonalvariations in microfilaremia and effects of ambientaltemperature in dogs parasitized by Dirofilaria repens.Parassitologia 1975; 17: 75–82.

24. Ershov, V.S., Naumycheva, V., Naumycheva, M.Y.Allergy and autoallergy in the pathology of helminthiasisin animals. In: Gaafar, S.M., Urquhart, G.M., Euzéby, J.et al., eds. Pathology of Parasitic Diseases. Lafayette, IN:Purdue University Studies, 1971: 173–6.

25. Mandelli, G., Mantovani, A. Su di un caso di infestazi-one massiva da Dirofilaria repens nel cane. Parassitologia1966; 8: 21–8.

26. Tarello, W. Babesiosis as an underlying factor influ-encing the severity and duration of perianal fistulas inthree dogs. Revue de Médecine Vétérinaire 2001; 152:83–8.

27. Hoover, J.P., Campbell, G.A., Fox, J.C. et al. Comparisonof eight diagnostic blood tests for heartworm infection indogs. Canine Practice 1996; 21: 11–24.

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29. Scott, D.W., Miller, W.H., Griffin, C.E. Parasitic skin dis-eases. In: Muller and Kirk’s Small Animal Dermatology,5th edn. Philadelphia: W.B. Saunders, 1995: 402.

30. Schrey, C.F. Epidemiologische Fallanalyse der kardio-vaskularen Dirofilariose (Herzwurmerkrankung) beiHunden in Deutschland. Dissertation for the degree ofDoctor of Veterinary Medicine, der Freien UniversitatBerlin, 1996.

Résumé Une dermatite prurigineuse, caractérisée par la présence d’érythème, de papules, d’alopécie focale oumultifocale, de croûtes et de nodules est rapportée chez 28 chiens du Nord Ouest de l’Italie présentant uneinfestation par Dirofilaria repens. Des traitements antiprurigineux, un contrôle antipuces et un régime d’évictionavaient été mis en place antérieurement sans succès chez 53.6% des patients. Le test de Knott et l’antigénémieétaient négatifs pour Dirofilaria immitis et Acanthocheilonema reconditum. Une babésiose et/ou une ehrlichioseconcommitante ont été diagnostiquées chez de nombreux animaux. Le traitement des maladies concommitantesa été suivi par un traitement filaricide spécifique. Les lésions cutanées ont été modérément améliorées avec letraitement initial, et ont totalement disparu avec le traitement macro et microfilaricide. Bien que D. repens puissen’être qu’un pathogène opportuniste, ce parasite ne devrait pas être considéré comme inoffensif, et son rôlepathogène dans les dermatoses canines mériterait d’être envisagé. De plus, il s’agit d’une zoonose, car des cas chezl’homme ont été rapportés dans le monde entier.

Resumen Una dermatitis prurítica caracterizada por la presencia de eritema, pápulas, alopecia focal o multi-focal, costras y nódulos fue observada en 28 perros con infestación por microfilarias Dirofilaria repens, en una

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zona endémica del Nor-Oeste de Italia. En el 53,6% de los pacientes existían registros de tratamientos previossin éxito con productos antipruríticos inespecíficos, control de pulgas y dieta de restricción. Tanto el test de Knottcomo el de antigeno fueron negativos a Dirofilaria immitis y Acanthocheilonema reconditum. Se diagnosticótambién en muchos perros afectados una babesiosis y/o erliquiosis canina granulocítica concurrentes. Tras eltratamiento de las enfermedades concurrentes se estableció un tratamiento filaricida específico. Las lesionescutáneas, aunque mejoraron levemente con el tratamiento inicial, desaparecieron completamente con el tratamientomacro y microfilaricida. Aunque D. repens puede ser un patógeno oportunista, este parásito no debería serconsiderado completamente inocuo, como se creía hasta el momento, y debería considerarse su posible papelcomo patógeno potencial como causa de lesiones cutáneas en el perro. Además tiene una importancia zoonóticaya que se han descritos caso en todo el mundo.

Zusammenfassung Eine durch Hautrötung, Papeln, fokale oder multifokale Alopezie, Krusten und Knotencharakterisierte juckende Dermatitis wurde bei 28 Hunden mit Mikrofilarieninfestation von Dirofilaria repensin einer endemischen Gegend in Nordwestitalien festgestellt. Bei 53.6% der Patienten waren unspezifischeBehandlungen des Juckreizes, Flohkontrolle und Eliminationsdiäten erfolglos. Sowohl Knott als auch Antigentestwaren für Dirofilaria immitis und Acanthocheilonema reconditum negativ. Gleichzeitige Babesiose und odergranulozytäre Ehrlichiose wurde bei vielen der betroffenen Hunde diagnostiziert. Spezifische filarizide Behandlungfolgte einer vorläufigen Behandlung der gleichzeitig bestehenden Erkrankungen. Die Hautläsionen, die mit derInitialbehandlung leichte Besserung zeigten, verschwanden mit der Behandlung der Makro- und Mikrofilarienvollständig. Obwohl D. repens ein opportunistischer Erreger sein kann, sollte dieser Parasit als nicht so harmlosangesehen werden wie früher angenommen wurde; eine mögliche pathogene Rolle bei der Verursachung vonHautläsionen des Hundes sollte in Betracht gezogen werden. Weiterhin hat der Erreger zoonotisches Potential,da weltweit Veröffentlichungen von humanmedizinischen Fällen vorliegen.

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