LAPORAN KASUS

PENYAKIT SIRKULASI
Dirofilaria Immitis in a Dog

Oleh:
DHARMA AUDIA SAMSURI
NIM: 2009611034
KELOMPOK 17G

LABORATORIUM ILMU PENYAKIT DALAM VETERINER

PENDIDIKAN PROFESI DOKTER HEWAN
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA
DENPASAR
2021
 PENDAHULUAN
Dirofilaria immitis adalah golongan parasit nematoda filarial dan merupakan salah satu
parasit yang berbahaya bagi anjing, kucing, dan mamalia lainnya. Banyak hewan peliharaan
seperti anjing dan kucing adalah inang utama parasit ini (Atkins, 2003). D. immitis pada anjing
sangat berkaitan dengan kondisi lingkungan, populasi vector, dan situasi infeksi. Dirofilaria
immiti merupakan penyebab penyakit parasit yang serius pada anjing. Cacing tersebut hidup
pada arteri pulmonalis dan ventrikel kanan, sehingga disebut sebagai cacing jantung.
Dirofilariasis pada anjing dapat menyebabkan gejala klinis seperti sesak nafas, batuk terus
menerus, gagal jantung kongestif, hemoptysis, hemolysis intravascular, tromboemboli paru,
asites, kehilangan nafsu makan dan berat badan (Davood, 2019).

REKAM MEDIS
1. Signalment dan Anamnesa
Kasus 1 : Seekor anjing gembala Belgian campuran jantan berusia 3 tahun seberat 19kg
dibawa ke Rumah sakit Hewan di Bukares, dengan riwayat depresi, kurang
nafsu makan, dan batuk terus menerus serta mengalami pingsan.
Kasus 2 : Seekor anjing betina berusia 7 tahun di bawa ke Rumah Sakit Pendidikan Hewan,
Universitas Federal, Nigeria. Anjing tersebut mengalami keluhan sering batuk
selama sekitar dua tahun. Batuknya menjadi terus menerus dan parah sekitar
dua minggu sebelum di bawa ke rumah sakit hewan.
Kasus 3 : Seekor anjing betina berusia 3 tahun di bawa ke Rumah Sakit Hewan di
Universitas College Dublin dengan riwayat batuk kering non-produktif selama
empat bulan. Anjing tersebut dinyatakan positif mengandung antigen D.
immitis.
2. Pemeriksaan Klinis
Kasus 1 : Setelah dilakukan pemeriksaan klinis, anjing menunjukkan anoreksia akut,
distensi abdomen, mukosa saliva pucat, denyut nadi perifer lemah, terdapat
murmur jantung sisi kanan kelas III/VI pada tingkat area proyeksi trikuspidalis ,
distensi jugularis dan denyut nadi jugularis yang terikat.
Kasus 2 : Hasil pemeriksaan klinis, hewan tersebut memiliki berat 17 kg, suhu rektal
40,2°C, dan detak jantung 81 denyut per menit. Selaput lender mata berwarna
merah muda dan tidak terjadi pembesaran kelenjar getah bening. Waktu
pengisian kapiler adalah satu detik dan vena jugularis tampak normal. Anjing
 tersebut terengah-engah dan batuk beberapa saat di ruang pemeriksaan, dan
auskultasi paru menunjukkan ronki parah di kedua sisi dada.
Kasus 3 : Hasil pemeriksaan klinis anjing tersebut mukosa berwarna merah muda dan
lembab, tidak ditemukan kelainan pada palpasi abdomen dan kelenjar getah
bening perifer dalam batas normal. Auskultasi jantung dan toraks normal,
detak jantung 136 detak per menit dan anjing mengalami takipnea sedang
dengan kecepatan pernapasan 48 napas per menit. Suhu rektal 38,9°C.
3. Pemeriksaan Penunjang
Kasus 1 : Sampel darah dikumpulkan dan menjadi sasaran pemeriksaan hematologis dan
biokimia rutin dan untuk analisis laboratorium parasitology. Pemeriksaan
parasite dengan menggunakan rapid test imunokromatografi untuk mendeteksi
adanya antigen D. immitis dan teknik Knott yang dimodifikasi untuk
mendeteksi mikrofilaria dan sonography Thoracic FAST (TFAST). Setelah
dilakukan teknik Knott yang dimodifikasi menunjukkan mikrofilaria dengan
karakteristik morfologi ekor lurus dan ekstremitas cephalic spindleshaped
(Gambar 1). Serta hasil dari sonography TFAST menunjukkan massa cacing
jantung di seluruh katup tricuspidalis dan ventrikel kanan melebar (Gambar 2).

Gambar 1. Mikrofilaria dari Dirofilaria immitis oleh pemeriksaan mikroskopis

menggunakan tes Knott yang dimodifikasi
 Gambar 2. Tampilan sumbu panjang dua dimensi dari jendela parasternal kiri
menunjukkan cacing jantung hyperechoic di seluruh katup tricuspidalis dan
ventrikel kanan yang melebar
Kasus 2 : Sampel darah di uji dengan menggunakan uji Knott dan spesies Dirofilaria
ditemukan secara mikroskopis (Gambar 3). Serta menggunakan uji radiographic
toraks menggunakan X-ray (Gambar 4).

Gambar 3. Perbesaran 100x terdapat Dirofilaria immitis (panah)

Gambar 4. Gambaran radiografi toraks lateral menunjukkan hipertrofi ventrikel kanan

dengan pembesaran arteri pulmonalis dan peningkatan kekeruhan bronkial
yang konsisten dengan dirofilariasis anjing
Kasus 3 : Pemeriksaan penunjang dilakukan dengan tes darah rutin, dengan hematologi
menunjukkan trombositopenia ringan dan limfositosis ringan. Uji Knott yang di
modifikasi menunjukkan hasil negative. Radiografi toraks menunjukkan
pembesaran arteri pulmonalis, pembesaran ventrikel kanan ringan hingga
sedang (Gambar 5).
 Gambar 5. Radiografi lateral kiri toraks. Ada pembesaran arteri lobar kranial kanan
(panah kuning) dan arteri lobar kaudal kanan (panah merah). Peningkatan
kontak antara siluet jantung dan tulang dada menunjukkan pembesaran
ventrikel kanan (panah hijau). Pola alveolar terletak di dalam lobus paru-paru
caudal kanan (panah putih).

4. Diagnosis
Kasus 1 : Berdasarkan pemeriksaan klinis dan ultrasonography TFAST, menunjukkan
adanya cacing jantung hyperechoic di seluruh katup tricuspidalis dan ventrikel
kanan yang melebar. Pada kasus ini hewan di diagnosa Dirofilariasis.
Kasus 2 : Berdasarkan pemeriksaan klinis dan pemeriksaan mikroskopis menggunakan uji
Knott, menunjukkan adanya cacing jantung yang nampak pada pemeriksaan
mikroskopis, sedangkan pada radiografi torak menunjukkan hipertrofi ventrikel
kanan dengan pembesaran arteri pulmonalis dan peningkatan kekeruhan
bronkus. Pada kasus ini hewan di diagnose Dirofilariasis.
Kasus 3 : Berdasarkan pemeriksaan klinis dan radiografi toraks menunjukkan adanya
tanda tanda dari Dirofilaria immitis. Pada radio toraks menunjukkan
kardiomegali sisi kanan, perburukan dari paru alveolar, konsisten dengan
perdarahan pneumoni dan pelebaran parah arteri pulmonalis lobar kranial
kanan. Pada kasus ini hewan di diagnose Dirofilariasis
5. Prognosis
Berdasarkan diagnosa dan pemeriksaan klinis hewan menunjukkan prognosa fausta,
prognosa dapat menjadi tidak baik apabila tidak segera dilakukan penanganan dapat
menyebabkan kematian pada hewan tersebut.

6. Treatment
Kasus 1 : Treatment dilakukan dengan pembedahan untuk menghilangkan cacing pada
jantung. Untuk awalnya, terapi darurat dimulai untuk menstabilkan pasien. Kateter perifer
 ditempatkan pada vena chepalica dan pemberian obat premedikasi dengan prednisolone (1
mg/kg, secara subkutan) sehari sekali dan Ceftriaxone (25 mg/kg intravena) dua kali sehari.
Kasus 2 : Treatment yang digunakan dengan pemberian ivermectin yang diberi secara
subkutan setiap dua minggu. Sebagai tambahan 2,5 mg ½ tab Enalapril secara oral sekali
sehari
Kasus 3 : Treatment dengan pemberian prednisolone 0,5 mg/kg secara oral, dua kali sehari
selanjutnya pada hari berikutnya dengan pemberian doksisiklin oral 10 mg/kg

PEMBAHASAN

Dirofilarian immitis atau heartworm disease adalah filarial yang bersifat zoonosis
nematode ditularkan oleh nyamuk dari spesies Culex, Aedes, dan Anopeles yang menyebabkan
penyakit heartworm pada banyak spesies termasuk anjing dan kucing. Cacing jantung
menginfeksi anjingnya dengan perantara gigitan vector nyamuk yang mengandung larva cacing
setelah menghisap darah anjing terinfeksi Jadi infeksi cacing jantung ditularkan secara
langsung dari anjing keanjing oleh nyamuk yang menghisap darah. Larva cacing jantung
disebut microfilaria ikut peredaran darah dari anjing yang terinfeksi. Ketika ada nyamuk yang
menghisap darah dari anjing itu, microfilaria ini juga ikut tercernar ditularkan ke anjing lain
yang kemudian diisap darahnya. Setelah masuk dalam aliran darah microfilaria bergerak dalam
sirkulasi kealiran darah jantung , paru-paru dan pembuluh darah besar , disitu larva akhirnya
berkembang menjadi cacing dewasa yang mulai menghasilkan microfilaria generasi
berikutnya. Atkins (2005) menyatakan bahwa kebanyakan kasus infeksi cacing jantung adalah
asimptomatik. Sejarah penyakit anjing penderita sangat bervariasi, di antaranya kehilangan
berat badan, toleransi terhadap latihan menurun, letargi, batuk, dispnea, sinkop, dan distensi
abdominal (ascites). Pengobatan terhadap infeksi cacing jantung sangat sulit. Ada beberapa
strategi yang dapat digunakan, termasuk pilihan untuk tidak melakukan pengobatan sama
sekali
 DAFTAR PUSTAKA
Adebayo, O. O., Akande, F. A., Adenubi, O. T. 2020. Canine Dirofilariasis : A Case Report
and Review of The Literature. FOLIA VETERINARIA, 64, 3: 75-81.
Atkins C. E (2003) Comparison of results of three commercial heartworm antigen test kits in
dogs with low heartworm burdens. J Am Vet Med Assoc 222:1221–1223.
Davood A., Dariush S., Abolghasem S., Shirzad G. 2019. Prevalence of dirofilariasis in
shepherd and stray dogs in Iranshahr, southeast of Iran. J Parasit Dis 43(2):319-323.
Esther L. B., Carlos M. G., Eimear S., Emma J. O. N. 2019. Case Study : Canine Heartworm
Disease Diagnose in Ireland. Veterinary Ireland Journal Volume 10 (5): 251-256.
Gina T.G, Radu C., Camelia I., Mariana I., Ioan L. M., 2018. A Creative concept for
transvenous extraction of Dirofilaria immitis in dogs with heartworm caval
syndrome: a case report. Sci Parasitol 19(1-2): 52-61.
Sci Parasitol 19(1-2):52-61, December 2018
ISSN 1582-1366 ORIGINAL RESEARCH ARTICLE

A creative concept for transvenous extraction of Dirofilaria immitis

in dogs with heartworm caval syndrome: a case report

Gina Teodora Girdan, Radu Constantinescu, Camelia Ion, Mariana Ionita, Ioan Liviu Mitrea

University of Agronomic Sciences and Veterinary Medicine of Bucharest, Faculty of Veterinary Medicine, 105 Splaiul
Independentei, 5th district, 050097, Bucharest, Romania.
Correspondence: Tel. +40771151263, E-mail gina_girdan@yahoo.com

Abstract. Heartworm disease (cardio-pulmonary dirofilariosis), caused by the filarioid mosquito-borne

nematode Dirofilaria immitis, is a serious and potentially fatal condition in dogs. Caval syndrome (CS) is a
life-threatening manifestation in the late stage of the disease; surgical removal of worms is the onl y
treatment option for dogs in this condition. Given that risks associated with heartworm surgical removal
have been registered, various minimally invasive techniques and better instruments continue to be
designed.
Here, we describe a case report on heartworm surgical removal in a 3 years old Belgian Shepherd dog with
CS, using a minimally invasive procedure based on a creative device. The device consists of a string type
horse hair brush that lies behind the surgical utensil. The transvenous right jugular approach was employed
under echocardiographic guidance.
A total number of 28 worms were removed by the procedure, but the echocardiogram showed that some
worms still remained. Regardless, the goal was to remove as many intact worms and to re -establish the
blood circulation, relieving in this way some of the heart failure condition symptoms. Next day following the
procedure, the dog had reversed to stage III of the disease, and the echocardiographic evaluation revealed
that the initial remaining worms could no longer be detected in the heart; it was hypothesized that they
have returned back into the pulmonary arteries due to haemodynamic forces of the blood flow. Marked
improvement was achieved in the treatment of right-sided congestive heart failure. The dog had recovered
and was discharged 10 days after worm removal; a protocol treatment including Doxycycline (10 mg/kg)
for 30 days and Ivermectin (6 μg/kg every 2 weeks) for six months was recommended. One year later, the
dog became antigen free.
In conclusion, the surgical technique presented here exceeded the initial goal of being minimally invasive,
but also demonstrated the efficacy of this two-pieces device, which can be easily assembled and be used for
the heartworm extraction in dog with CS.

Keywords: Dirofilariosis; Caval syndrome; Echocardiography; Tayama String horsehair brush; Dog.
Received 05.11.2018. Accepted 03.12.2018.

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Introduction
Heartworm disease (HW) (cardio-pulmonary
dirofilariosis) is caused by the filarioid
nematode Dirofilaria immitis (Nematoda;
Filarioidea). It is transmitted through
mosquitoes’ bites which act as vector and
intermediate host (Mitrea, 2011). Adults live in
the pulmonary arteries and could invade the
right heart chambers. The disease has a fatal
progression if left untreated (Genchi et al.,
2005).
Caval syndrome (CS) or “liver failure
syndrome” appears in the end stage of the
disease (stage IV), as a consequence of cardio-
pulmonary dirofilariosis progression. This was
first mentioned by Adams (1956) which
described an acute form of heartworms
associated with a large number of worms into
the venae cavae and right atrium in a dog.
CS consists in the migration of heartworms
against the blood flow from the pulmonary
arteries to the right ventricle, right atrium and
venae cavae (Strickland, 1998). This occurs
because the heartworms lack the ability to
adhere or to submerge to the endothelium and
also to freely move, causing an increased
vascular resistance within the circulation at the
distal end of pulmonary arteries thus entering
the heart (Jones, 2016). Once the chambers of
the heart and venae cavae are occupied, the
heartworms disrupt the proper functioning of
the tricuspid valve, causing pulmonary
hypertension and reduced pulmonary output
(Strickland, 1998). In summary, stratifying the
likely course of this condition by creating a
framework of the following events are
registered: a retrograde migration of a large
worm burden, a haemodynamic alteration with
acute pulmonary hypertension, reduced
cardiac output and right ventricular
dysfunction with tricuspid regurgitation
(Strickland, 1998; Bové et al., 2010).
In order to re-establish adequate cardiac
function and prevent critical consequences for
affecting the body, CS must be immediately
treated. Surgical removal of worms is the only
treatment option for dogs in this condition
otherwise it will end up fatally. However, many
risks associated with heartworm surgical
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ORIGINAL RESEARCH ARTICLE
removal have been registered. Therefore,
minimally invasive techniques and better
instruments continue to be designed. These
were described since the 1980 as
catheterizations with flow-directed catheters
fluid (Atkins et al., 1988), Ishihara’s flexible
alligator forceps (Ishihara et al., 1986), basket
retrieval devices (Yoon et al., 2011), modified
red rubber feeding tubes (Jones, 2016) or
”snare” guided catheters (Alho et al., 2016).
These devices are very diverse, but all are
designed in order to reduce intravascular
trauma and damage of worm cuticles during
surgical extraction (Strickland, 1998; Garner,
2011; Yoon et al., 2011; Alho et al., 2016).
Here, we describe a case report on heartworm
surgical removal in a dog with CS, using a
minimally invasive procedure based on a
creative device.
Materials and methods
Case presentation
A 3 year-old male Belgian Shepherd dog mixed
breed, weighing 19 kg was presented to the
Clinics of the Faculty of Veterinary Medicine in
Bucharest with a history of a recently
depreciated health condition, lack of appetite,
diarrhea and persistent cough after which he
suddenly collapsed. The dog originated from a
household in which another female dog
showed a similar clinical episode three weeks
prior, after which suddenly died. The dog had
not received heartworm prevention or
vaccination a year ago to this visit, as the
owner stated.
On physical and clinical examinations, the dog
showed acute anorexia, abdominal distension,
and pale mucous membranes with a delayed
capillary refill time, weak peripheral pulse, grade
III/VI right-sided heart murmur at the level of the
tricuspid projection area, jugular distention and
bounding jugular pulse (figure 1).
Laboratory investigations
Blood samples were collected and subjected for
routine hematological and biochemical
investigations and for parasitological
laboratory analyzes.
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Figure 1. Distended right jugular vein of a 3 year-old mixed Belgian Shepherd dog with Caval syndrome
Imagistic investigation using of Focused
Assessment with Sonography for Triage
(FAST) to asses an underlying cause has been
performed applying the Abdominal FAST
(AFAST) and Thoracic FAST (TFAST)
procedures (Boysen et al., 2004).
Parasitological investigations, by using of a
commercial immuno-chromatographic rapid
test (SNAP®4DX® Plus, IDEXX Laboratories,
2017) for detecting circulating female
antigen of D. immitis and a modified Knott
technique for detecting circulating
microfilariae (Georgi and Georgi, 1992;
Mitrea, 2011) were performed.
Results
Paraclinical investigations
The serum biochemistry profile (table 1)
performed prior to the surgical procedure,
pointed out pre-renal azotemia and
increased hepatic enzymes due to the passive
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ORIGINAL RESEARCH ARTICLE
congestion following right cardiac
enlargement.
The SNAP®4DX® Plus test showed positive
results for Ag of D. immitis.
The modified Knott technique showed
microfilariae with a characteristic
morphology of straight tail and a spindle-
shaped cephalic extremity, compatible for D.
immitis (Genchi et al., 2005) (figure 2).
The AFAST technique revealed splenomegaly,
hepatomegaly with hepatic congestion and
free intra-abdominal fluid (figure 3). TFAST
pointed out a mass of heartworms across the
tricuspid valve and a dilated right ventricle,
which correspond to CS (figure 4) (Kittleson
and Kienle, 1998; Venco and Vezzoni, 2001).
Diagnostic
By corroborating all the above results the
diagnostic was assumed as dirofilariosis,
stage IV, which is consistent with CS.
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Table 1. Serum biochemistry values in a 3 year old Belgian Shepherd mixed breed
with caval syndrome (dirofilariosis stage IV)

Serum biochemistry parameters Results Reference value

(Boon and Rebar, 2010)
Albumin (ALB) 2.3 2.2-4.0 (g/dl)
Phosphatase Alkaline (ALKP) ↑ 677 23-212 (u/L)
Alanine Aminotransferaze (ALT) ↑ 340 10-100 (u/L)
Amylase (AMYL) ↓ 412 500-1250 (u/L)
Blood Urea Nitrogen (BUN) ↑ 121 7-27 (mg/dl)
Calcium (Ca) 10.8 7.9-12 (mg/dl)
Creatinine (CREA) ↑ 3.5 0.5-1.8 (mg/dl)
Gamma Glutamyl Transferaze (GGT) ↑ 50 0-7 (u/L)
Glucose (GLU) ↓ 55 70-143 (mg/dl)
Lipase (LIPA) 1672 200-1800 (u/L)
Total Bilurubin (TBIL) ↑3 0.0-0.9 (mg/dl)
Total Proteins (TP) ↓ 4.5 5.2-8.2 (g/dl)
GLOBULINS (GLOB) ↓ 2.2 2.5-4.5 (g/dl)

Table 2. Hematological results in a 3 year old Belgian Shepherd mixed breed with caval syndrome

Hematological parameters Results Reference values

(Hart and James, 2006)
Hematocrit (HCT) ↓ 33.6% 37.0-55.0%
Hemoglobin (HGB) ↓ 10.7 g/dL 12.0-18.0 g/dL
Mean Corpuscular Hemoglobin
Concentration (MCHC) 34.8 g/dL 30.0-36.9 g/dL
White Blood Cells (WBC) ↓ 5.90 K/µL 6.00-16.90 K/µL
Granulocytes (Grans) 4.20 K/µL 3.30-12.00 K/µL
% (GRANS) 71.2 %
Lymphocytes/ Monocytes (L/M) 1.7x10˄9/L 1.1-6.3 x10˄9/L
(%L/M) 29 %
Platelets (PLT) ↓ 160 K/µL 175-500 K/µL

Figure 2. Microfilariae of Dirofilaria immitis by the modified Knott test

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Treatment
A surgical approach for removing of worms has
been chosen as treatment option for the dog,
by using a minimally invasive procedure based
on a creative device (figure 5).
For the beginning, an emergency therapy was
initiated to stabilize the patient. A peripheral
catheter was placed on the cephalic vein and
aggressive shock therapy was initiated with
crystalloid fluids, to compensate for
intravascular volume deficiency expressed by
the following clinical signs: prolonged capillary
Figure 3. Large anechoic fluid collection exposing the well-defined linear margins of the liver
Surgical procedure
The basis of the instrument adapted consists
of a string type horse hair brush, named
Tayama The device, respectively, a
“heartworm extraction brush” was assembled
in the operating theater, from a flexible
guidewire of a 7-French central venous
catheter, to which was attached a non-
absorbable monofilament suture - much as possible.
Polypropylene 2/0 and 0 (Kittleson and
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ORIGINAL RESEARCH ARTICLE
refill time (>2 seconds), tachycardia (heart rate
100 beats/minute), pale mucous membranes
and a low systolic blood pressure of 80 mm Hg.
Supplemental oxygen via face mask has been
delivered.
Taking in consideration the risk associated
with possible thromboembolism following the
heart catheterization, the dog was
premedicated with Prednisolone (1 mg/kg,
subcutaneously [SC]) once daily and
Ceftriaxone (25 mg/kg intravenously) [IV]
twice daily (b.i.d.).
Kienle, 1998; Strickland, 1998; Yoon et al.,
2011). The straight edges of polypropylene
suture were inserted with alternating loops
fixed to the proximal end of the flexible guide-
wire.
The striations of the flexible guide-wire
prevent the suture from sliding and, at the
same time, allow the knots to be tightened as
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Figure 4. Two-dimensional long axis view from the left parasternal window revealing hyperechoic heartworms across the
tricuspid valve and a dilated right ventricle

Figure 5. "Tayama" brush consisting in a combination of a flexible guidewire,

a 7 - French central venous catheter and a non-absorbable monofilament suture

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The surgical procedure was guided by
ultrasonography taking advantage of the fact
that the heartworm’s cuticular wall is
reflective and easily visualized by
ultrasonographic examination (Jones, 2016).
The anesthesia was inducted using initially
Diazepam (0.2 mg/kg), followed by Ketamine,
approximately 3 mg/kg tapered to the desired
effect. Intubation was performed using an
endotracheal tube number 8.5. Anesthesia
was maintained using Isoflurane (1.5%) and a
local infiltration of Lidocaine 2%. The dog was
positioned on left lateral recumbence on a
special table with a cut to allow for the
ultrasound probe to be in contact to the
patient’s chest wall.
Heartworm embolectomy was accomplished
by approaching the right external jugular vein
with an extemporaneous device. By holding
the handle, the surgeon slowly, rotated the
device and gently pulled out repeatedly in a
delicate and gradual manner.
Using echocardiographic guidance we were
able to follow the surgeon’s trajectory and
Figure 6. Surgical extraction of adult helminths from the right jugular approach
in a 3 year-old mixed Belgian Shepherd dog with Caval syndrome
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ORIGINAL RESEARCH ARTICLE
passage through the right heart chambers;
also, the characteristic, hyperechoic cuticular
heartworm was easily identified as two
parallel lines (Jones, 2016) similar in
appearance to the “=” (equal sign) and a
hypoechoic center (Alho et al., 2016)
confirming the presence of heartworms.
A total number of 28 adult heartworms were
removed by the procedure (figure 6), in a
total of four attempts, but the
echocardiogram showed that some worms
still remained. Two hours after surgery the
animal completely regained consciousness.
Follow-up
Next day following the procedure, the dog
had reversed to stage III of the HW disease
and the echocardiographic evaluation
revealed that the initial remaining worms
could no longer be detected in the heart. It
was hypothesized that they have returned
back into the pulmonary arteries,
presumably, due to haemodynamic forces of
the blood flow.
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Marked improvement was achieved in the
treatment of right-sided congestive heart
failure using Pimobendan 0.25 mg/kg (b.i.d.),
Benazepril 0.5 mg/kg (s.i.d.), Furosemid 2
mg/kg (b.i.d.) and Cardio Strength (Vetri
Science®) 2 capsules (s.i.d.). The dog had
recovered and was discharged 10 days after
worm removal.
A protocol treatment including Doxycycline (10
mg/kg) for 30 days and Ivermectin (6 μg/kg
every 2 weeks) for six months was
recommended (Grandi et al., 2010).
The dog was evaluated at each 3 months post
treatment for parasite microfilaremia and
antigenemia. At first evaluation p.t., the dog
was negative for microfilariae, but still
remained Ag positive. One year later, the dog
became antigen negative.
Discussion
Here we describe a case report on heartworm
surgical removal in a dog with CS, using a
minimally invasive procedure based on a
creative device.
The removal of the heartworms had resulted in
the cessation of the tricuspid valve
regurgitation, allowing for an increased cardiac
output and a decrease in the pulmonary
arterial pressure. Despite of the fact that not all
the worms were removed, the goal was to
extract as many intact worms as possible and
to re-establish the blood circulation thus
reduces the symptoms of the heart failure
condition.
Nevertheless, a complete remission of the
symptoms of CS is not possible. One study
performed by Kittleson and Kienle (1998)
examined dogs with a large worm burden, and
showed that the group that had the mean
pulmonary artery pressure of 60 mmHg,
developed CS while another group, with similar
worm burden but a mean pulmonary arterial
pressure of 30 mmHg, did not develop the
syndrome. Therefore, a reliable prediction of
CS occurrence is doubtful.
This combination of treatment based on
doxycycline and ivermectin abolish the
59
ORIGINAL RESEARCH ARTICLE
Wolbachia endosymbiont population which is
vital for worm development and fertility. One
study performed by Bazzocchi et al. (2008)
showed uterine injury of adult Dirofilaria
females after doxycycline and ivermectin
treatment.
Before attempting any surgical procedure, it is
critical that the pacient is in stable condition. In
order to do so, fluid therapy along with
medication is recommended, before and after
the surgery, to prevent the occurrence of
serious complications (Nelson, 2015). Often,
after the death of one or more adult worms, the
onset of clinical signs occurs due to the release
of vasoactive substances that cause
inflammation. The decrease in parenchymal
and arterial wall damage is attributed to the
effects of Prednisolone (Atwell and Tarish,
1995) which reduces pulmonary inflammatory
lesions at a tapering dosage (Atkins and Seaks,
2018).
Several anesthetic procedures for heartworms
removal have been suggested, including
alpha2-receptor agonists premedication
(Chiavaccini et al., 2014) but these are related
with a reducing of cardiac output and
increasing in pulmonary pressure which
aggravates pulmonary hypertension (Flacke et
al., 1993). Anticholinergics used in
premedication such as Atropine suggested by
Yoon et al. (2011) cause a significantly higher
heart rate. This slows coronary blood flow and
myocardial oxygenation which happens during
diastole (Greene, 2001). Ketamine was used
because, as a dissociative agent, stimulates
indirectly the cardiovascular system by
enhancing the sympathetic tone, thus causing
an increase in heart rate, cardiac output and
mean arterial pressure (Waxman et al., 1980).
The benzodiazepines, when used alone, have a
minimal cardiopulmonary depressant effect
(Greene, 2001) and this association between
Diazepam and Ketamine has been reported to
maintain good cardiovascular performance in
high-risk patients (Waxman et al., 1980). This
is preferred to Propofol induction which can
cause myocardial depression, peripherally
vasodilation and hypotension (Macintire et al.,
2012). Isoflurane do not sensitize the heart to
the effect of catecholamines and cause no heart
rhythm disturbances (Brock, 2001).
Sci Parasitol 19(1-2):52-61, December 2018
ISSN 1582-1366
This surgical technique presented here,
exceeds the initial goal of just being less
invasive, but also efficient and easy to
perform compared to the alligator forceps or
basket retrieval devices and can be easily
assembled and be used for the extraction of
D. immitis helminths from the heart
chambers and venae cavae. The feature of the
soft and curved tip, allows a convenient
passage through the jugular vein and its easy
lowering into the right atrium and right
ventricle. As opposed to the alligator forceps
which are rigid instruments that can
perforate the blood vessels and cardiac
chambers while with its jaws could macerate
the worms, the soft and curved tip of Tayama
string allows for an easy passage through the
jugular vein and smooth lowering into the
right atrium and right ventricle (Kittleson
and Kienle, 1998). Furthermore, the
movements of the heartworms can cause
inconvenient challenges in grabbing the
worms using forceps. Standard red rubber
feeding tubes can be modified and used
instead of the flexible guidewire of the
central venous catheter, but there is big
disadvantage in using it because the tubes
can become lost during surgery (Jones,
2016).
Acute pulmonary thromboembolism can be
inevitable, but attempting to decrease the risk
is essential. Worm fragments as well as platelet
aggregation and inflammation can form
thromboemboli that block circulation,
especially in caudal lobes of the lungs (Greene,
2011). It is important to be aware and manage
the risk as much as possible, because fatal
outcomes is possible even the patient starts to
feel better after the surgery; therefore exercise
restriction is mandatory.
In conclusion, this minimally invasive
technique has been proven successful in this
trial and appropriate for handling the
movements of heartworms while providing a
rapid recovery time and better prognosis for
the patient. The significance of this approach
lies also in the fact that is offering a new
insight and a creative approach for using a
common and an easily available instrument.
60
ORIGINAL RESEARCH ARTICLE
References
Adams E.W. 1956. A case of dirofilariasis with
obstruction of hepatic veins. North Am. Vet.
37:299-302.
Alho A.M., Fiarresga A., Landum M., Lima C., Gamboa
O., Meireles J., Sales Luis J., Madeira de Carvalho
L. 2016. A Homemade Snare: An Alternative
Method for Mechanical Removal of Dirofilaria
immitis in Dogs. Vet. Med. Int. 5780408: 1-16.
Atkins C.E., Seaks J.L. 2018. Overview of heartworm
disease. Merck & Co. Inc., Kenilworth, N.J., USA.
As accessed in August 2017 from http://
www.msdvetmanual.com.
Atkins C.E., Keene B.W., McGuirk S.M. 1988.
Investigation of caval syndrome in dogs
experimentally infected with Dirofilaria immitis.
J. Vet. Intern. Med. 2(1):36-40.
Atwell R., Tarish J.H. 1995. The effect of oral, low
dose prednisolone on the extent of pulmonary
pathology associated with dead Dirofilaria
immitis in a canine lung model. Proceedings of
the Heartworm Symposium. Batavia, IL:
American Heartworm Society 28:103-111.
Bazzocchi C., Mortarino M., Grandi G., Kramer L.H.,
Genchi C. Bandi C., Genchi M.,Sacchi L., McCall
J.W. 2008. Combined ivermectin and
doxycycline treatment has microfilaricidal and
adulticidal activity against Dirofilaria immitis in
experimentally infected dogs. Int. J. Parasitol.
38(12):1401-1410.
Boon G.D., Rebar A.H. 2010. IDEXX VetTest
Chemestry Analyzer Operator’s manual, IDEXX
Laboratories, As accessed in April 2017 from
https:// www.idexx.com/en.
Bové C.M., Gordon S.G., Saunders A.B., Miller M.W.,
Roland R.M., Achen S.E., Drourr L.T., Boggess
M.M. 2010. Outcome of minimally invasive
surgical treatment of heartworm caval
syndrome in dogs: 42 cases (1999-2007)
JAVMA 236(2):187-192.
Boysen S. R., Rozanski E. A., Tidwell A. S., Holm J.L.,
Shaw S.P., Rush J.E. 2004. Evaluation of a
focused assessment with sonography for
trauma protocol to detect free abdominal fluid
in dogs involved in motor vehicle accidents. J.
Am. Vet. Med. Assoc. 225(8):1198-1204.
Brock K.A. 2001. Preanesthetic use of atropine in
small animals 79(1): 24-25.
Chiavaccini L., Claude A.K., Meyer R.E. 2014. An
anesthetic protocol for adult heartworms
removal in two cases of canine caval syndrome.
Vet. Anaesth. Analg. 41(1):105-106.
Flacke W.E., Flacke J.W., Bloor B.C. 1993. Effects of
dexmedetomidine on systemic and coronary
haemodynamics in the anesthetized dog. J.
Cardiothorac. Vasc. Anesth. 7:41-49.
Sci Parasitol 19(1-2):52-61, December 2018
ISSN 1582-1366
Genchi C., Venco L., Genchi M. 2005. Guideline for
the laboratory diagnosis of canine and feline
Dirofilaria infections. Mappe Parasitologiche,
Italia, 8:139-144.
Garner S. 2011. Caval Syndrome. As accessed in
August 2017 from http://www.safarivet.com.
Georgi J. R., Georgi M.E. 1992. Heartworms and
other filarids. Canine clinical parasitology, Lea &
Febiger, Philadelphia, PA. 192-198.
Grandi G., Quintavalla C., Mavropoulou A., Genchi
M., Gnudi G., Bertoni G., Kramer L. 2010. A
combination of doxycycline and ivermectin is
adulticidal in dogs with naturally acquired
heartworm disease (Dirofilaria immitis). Vet.
Parasitol. 169:347-351.
Greene C. 2011. Infectious Diseases of the Dog and
Cat. 4th ed., Chapter 83, Saunders:865-867.
Greene S. 2001. Veterinary Anesthesia and Pain
Management Secrets (Chapter 6). Hanley and
Belphus-INC/Philadelphia Medical Publisher
(Chapter 15):91-96.
Hart A., James R. 2006. VetAutoread Hematology
IDEXX Laboratories As accessed in April 2017
from https://www.idexx.com/en.
Ishihara K., Sasaki Y., Kitagawa H. 1986.
Development of a flexible alligator forceps: a
new instrument for removal of heartworms in
the pulmonary arteries of dogs. Nihon Juigaku
Zasshi. 48(5):989-991.
Jones S.L. 2016. Management of Caval Syndrome.
Today’s Veterinary Practice. vol. 6, part 3:55-61.
61
ORIGINAL RESEARCH ARTICLE
Kittleson M.D., Kienle R.D. 1998. Heartworm
infection and disease (dirofilariasis)-caval
syndrome. In: Small Animal Cardiovascular
Medicine. 2nd ed (Chapter 23), Mosby 370-401.
As accessed in May 2017 from
http://www.vetmed.ucdavis.edu.
Macintire K.D., Drobatz K.J., Haskins S.C., Saxon W.D.
2012. Manual of Small Animal Emergency and
Critical Care Medicine, 2nd edition, Chapter 5,
John Wiley & sons, Inc, 41-62.
Mitrea I.L. 2011. Parasitology and Parasitic Diseases
(in Romanian) (Chapter 3), Ceres, pp. 474-481.
Nelson T.C. 2015. Canine heartworm disease
principles of treatment. Vol. 5, part 2: Animal
Medical Center, Anniston, Alabama Companion
Animal Practices of North America, 53-59.
Strickland K.N. 1998. Canine and feline caval
syndrome. Clin. Tech. Small Anim. Pract.
13(2):88-95.
Venco L.,Vezzoni A. 2001. Heartworm (Dirofilaria
immitis) disease in dogs and cats. Heartworms
infection in humans and animals Fernando
Simón and Claudio Genchi (Editors), Chapter
IX:161-174.
Waxman K., Shoemaker W.C., Lippmann M. 1980.
Cardiovascular effects of anesthetic induction
with ketamine. Anesth. Analog. 59(5):355-358.
Yoon W.K., Han D., Hyun C. 2011. Catheter-guided
percutaneous heartworm removal using a
nitinol basket in dogs with caval syndrome. J.
Vet. Sci. 12(2):199-201.
DOI: 10.2478/fv-2020-0029

FOLIA VETERINARIA, 64, 3: 75—81, 2020

CANINE DIROFILARIASIS: A CASE REPORT

AND REVIEW OF THE LITERATURE

Adebayo, O. O.1, Akande, F. A.2, Adenubi, O. T.3

Veterinary Teaching Hospital, Federal University of Agriculture

1

PMB 2240, Alabata, Abeokuta, Ogun State

2
Department of Veterinary Parasitology and Entomology
3
Department of Veterinary Pharmacology and Toxicology, College of Veterinary Medicine
Federal University of Agriculture, PMB 2240, Alabata, Abeokuta, Ogun State
Nigeria

bukiadenubi@gmail.com

ABSTRACT climate change and international pet travel regulations,

Dirofilariasis is a disease of clinical importance
in dogs. It is to this end that a case of a seven-year-old
mongrel with dirofilariasis was presented to examine the
unique features and presentation in the canine patient
in question. The dog had clinical signs consistent with
the disease. Further diagnostic tests were performed to
establish the presence and severity of the disease and
make an appropriate treatment plan. The Knott’s test
revealed Dirofilaria species in the circulating blood and
radiography showed right ventricular hypertrophy with
pulmonary arterial enlargement and increased bronchi-
al opacification. The treatment instituted was ivermec-
tin therapy by subcutaneous injection every two weeks
for six months, cardiac glycoside and antibiotics for
14 days. The clinical signs resolved after completion of
the treatment. A general overview of heartworm infec-
tion in dogs was also done to update current knowledge
of the disease. Though the risk of significant propaga-
tion of Dirofilaria immitis is considered low, with the
this emerging zoonosis remains a threat.
Key words: case report; Dirofilaria immitis; dog; Ni-
geria; zoonosis
INTRODUCTION
Etiology and Epidemiology
Canine dirofilariasis, also called heartworm disease, is a
non-contagious, parasitic disease caused by a filarial/small
thread-like worm, Dirofilaria immitis of the family Oncho-
cercidae [20]. The parasite is one of the most pathogenic
nematodes distributed worldwide, primarily affecting dogs
and cats [34]. Mosquitoes (Aedes, Culex, Anopheles spe-
cies) are the vectors which transmit this parasite from host
to host [18]. Alongside D. immitis is another filarial worm,
D. repens, and both are considered to have great clinical
importance. They are relatively widespread in many parts
of the world and have significant zoonotic potential [35].

75
 Fig. 1. Biological life cycle for Dirofilaria immitis and Dirofilaria repens [35]
Dirofilaria immitis establishes itself in the cardiovascular
system of the primary host, while D. repens invades the
subcutaneous tissues of the primary host (Fig. 1) [35].
Pathophysiology
Dogs are considered the definitive host for D. immitis,
though, more than 30 animal species (e. g. coyotes, foxes,
wolves, domestic and wild felids, ferrets) and humans (ac-
cidental hosts) may be infected [2, 17]. Adult worms most-
ly dwell in the right ventricle and pulmonary artery, but
occasionally can be found in the epidural space, brain, an-
terior chamber of the eye, lungs or the arterial system [5].
Microfilariae, larvae in the first larval stage (L1), are
produced by the female adult worm and released into the
bloodstream of the primary host [31]. Further develop-
ment of the microfilariae must take place in the vector after
taking a blood meal from the host [35]. The development
from L1 to L3 can occur in different mosquito species, re-
quiring an average temperature of about 14—18 °C over a
period of 30—60 days [8, 16]. The infective larval stage L3,
is transmitted through inoculation into the skin of anoth-
er primary host by the vector and undergoes development
from L3 to L4 in the host’s subcutaneous tissue in about
76
10—12 days [35]. Development from L4 to L5 takes place
in the muscles of the host 50 to 70 days after injection [16].
Juvenile worms (L5) penetrate the systemic veins and are
transported to the pulmonary arteries where they continue
to develop into adult worms. In severe cases, worms may
also enter the right heart chamber and caudal vena cava,
but in most cases, they are retained in the pulmonary ar-
tery and its branches [14].
The maturation of the female worms in the pulmonary
arteries of the primary host cause inflammatory reactions
in the pulmonary microvasculature and larger arteries of
the hosts [16]. The pulmonary artery expands in diameter,
the endothelium and tunica media thicken, and the blood
vessels may become obstructed by formation of thrombi
causing pulmonary hypertension [35]. The presenting le-
sions of right ventricular enlargement, pulmonary vascu-
lature dilation  and parenchymal lung infiltrates are con-
sistent with heartworm disease [3] (Fig. 2). As the disease
progresses, the clinical signs seen will depend on the dura-
tion of the infection, the worm burden in the host and the
host-parasite interactions [1]. This eventually culminates
into a multisystemic disorder affecting the heart, lungs, liv-
er and kidneys [30].
 Fig. 2. Ventro-dorsal thoracic radiograph showing blunted, enlarged and tortuous pulmonary arteries (large black arrows)
and an enlarged pulmonary trunk (small black arrows) [3]
Prevalence and risk factors
The prevalence depends on many factors, such as the
methods performed and preselection of the samples; there-
fore, different prevalence reports exist within and between
countries. The prevalence of D. immitis is reported to be
1.0 % in South Australia [10], 5.5 % in Brazil [25], 19.0 %
in Spain [19], 20.9 % in South Korea [29] and 30.8 % in
South Africa [26]. In Nigeria, reports of the prevalence of
dirofilariasis vary from 4.8 % as reported in Northeast Ni-
geria [11], 3.36 % in Eastern Nigeria [34] and 2.15 % in the
Middle belt of Nigeria [22]. This has been proposed to be
due to an increase in dog ownership, effects of stray dogs,
international pet travel etc.
Factors determining the prevalence of D. immitis in
an area include: climate, mosquito species/subspecies and
the density of the primary host population [16]. Risk fac-
tors for infection of the primary host include: animal spe-
cies (dogs are the natural primary host), sex (male dogs
are more vulnerable), habitat (dogs who live outdoors are
more exposed to infection), the size of the primary host
(large dogs are more likely to become infected than small
dogs), and age due to the longer period of exposure to
mosquito bites [12].
Clinical signs
The clinical signs of heartworm disease are due to the
damage caused to the organs in which they are established
e.g. the pulmonary arteries, the right heart chamber, eyes,
kidneys, central nervous system and subcutaneous tissue
[17]. The signs can be mild, moderate or severe. The mild
signs include: cough, chest pain, hemoptysis, low-grade
fever, chills and malaise. The moderate signs are: dysp-
noea, coughing, weight loss, syncope, and other signs of
right-sided heart failure [17]. Caval syndrome can be seen
in severely affected dogs, where worms invade the right
ventricle and caudal vena cava. This interferes with the
closure of the tricuspid valve impeding normal blood flow,
leading to cardiovascular collapse. Dogs may also present
with intravascular haemolysis, hemoglobinuria and acute
general malaise [15].
In some cases, there could be occult infections in which
the microfilariae in the circulating blood of infected dogs
are not seen. This may be due to: single sex worm infection
(male or female), the presence of immature females during
the prepatent period of development, geriatric infection or
ectopic infection [6].
Diagnosis
Direct diagnosis of heartworm infection can be done
by microscopic identification of microfilariae in the blood,
while indirect infection can be diagnosed using sever-
al blood tests to determine the presence of antigens and/
or microfilariae in the host. The presence of worms in
the heart or subcutaneous tissues during surgery or post-
77
mortem is definitive [27]. Laboratory examinations using
parasitological (Buffy coat, wet mount, modified Knott’s
test) and serological (ELISA) techniques may aid the di-
agnosis.  Molecular testing, such as the polymerase chain
reaction (PCR) and tissue histochemistry, can help differ-
entiate microfilaria species [16]. Other diagnostic proce-
dures such as general blood tests, radiography, echocardi-
ography and electrocardiography should be performed to
determine the degree of severity and serve as a guide in the
treatment regimen.
Prophylaxis, treatment and control
Wolbachia pipientis, an intracellular bacterium, lives
in symbiosis with D. immitis. Studies have shown that the
inflammatory reaction occurring during heartworm infec-
tion is partly due to W. pipientis [32]. Therefore, the use of
an anthelminthic agent in combination with an antibacte-
rial agent is strongly recommended [24, 33]. Melarsomine
dihydrochloride, an organic arsenical, is the most used an-
thelminthic agent. It is administered at a dosage of 2.5 mg.
kg–1, deep intramuscular injection in the lumbar muscles,
twice within a 24-hour interval. Ivermectin, a macrocyclic
lactone, at 200 µg.kg–1 can be given as a single dose sub-
cutaneously, four to six weeks after treatment with melar-
somine dihydrochloride [8]. Doxycycline, an antibacterial
agent, will reduce the burden of W. pipientis in all stages of
D. immitis infections.
Prophylactic treatment of all dogs living in areas ex-
posed to infections is recommended to reduce the number
of microfilariae in the bloodstream, and thereby curtail
transmission. The treatment consists of a monthly dose of
orally administered milbemycin or topically applied iver-
mectin.
CASE PRESENTATION
On the 17th of September, 2018, a seven-year-old, fe-
male mongrel was presented to the Veterinary Teaching
Hospital, Federal University of Agriculture, Abeokuta,
Nigeria, with complaints of frequent episodes of coughing
for about two years. The coughing became persistent and
severe about two weeks before presentation. The pet had
been placed on multivitamins and a teaspoon of cod-liver
oil given four times daily in food orally before presenta-
tion. Different antibiotics such as oxytetracycline, penicil-
78
lin-streptomycin and tylosin had been prescribed for the
pet at different times by different veterinarians.
On clinical examination, the pet weighed 17 kg, rectal
temperature was 40.2 °C, and the heart rate was 81 beats
per min. The ocular mucous membranes were pinkish and
there was no enlargement of the superficial lymph nodes.
Heart auscultation revealed arrhythmia, although the fem-
oral pulse was strong and regular. Capillary refill time was
one second and the jugular vein appeared normal without
visible pulsations. The dog was panting and coughing to
some extent in the examination room and auscultation
of the lungs revealed severe crackles on both sides of the
chest.
A tentative diagnosis of bronchopneumonia and diro-
filariasis was made. The differential diagnoses included:
congestive heart failure, endocarditis and pericarditis. The
blood was obtained for haematology and parasitological
analysis. The pet was also scheduled for chest x-ray (lateral
and ventro-dorsal views).
The haematology was within normal limits (Packed
Cell Volume, PCV—50 %; total white blood cell count,
WBC—10.8 × 109.l–1), no parasite was found in the blood
film using the wet mount and thin smear techniques. On
day two of the presentation, Knott’s test was carried out on
the blood sample and Dirofilaria species was found micro-
scopically (Fig. 3).
The radiography results showed right ventricular hy-
pertrophy with pulmonary arterial enlargement, and in-
creased bronchial opacification (Fig. 4). Based on the med-
ical history, clinical signs and the presence of the worms, a
confirmatory diagnosis of canine dirofilariasis was made.
The dog was classified as moderately affected.
Management and outcome
Treatment included 300 µg.kg–1 ivermectin (Ivomec®,
Merial) administered subcutaneously every two weeks.
In addition, 2.5 mg (1/2 tab.) enalapril (Lotrial®, ATOZ
Pharmaceuticals, India) orally once daily and 0.125 mg
(1/2 tab.) digoxin orally once daily was administered for
14 days. After treatment daily, the dog was admitted to the
veterinary clinic for observation for six hours. The dog was
released from the clinic in the evenings, for observation by
the owners. Exercise was limited the first few weeks after
each treatment. No side effects were observed following
the treatments.
Fig. 3. Dirofilaria immitis (Arrow). Magnification ×100 of the micro-
scope with a phone (Infinix) camera from top. The anterior end of
Dirofilaria immitis tapers anteriorly as seen with the Knott’s method
which is the standard for diagnosis of canine dirofilariasis [7]
By day  14, the dog’s clinical signs had improved and
there was no microfilaria detection in the blood after the
first shot of ivermectin. The dog continued to have a mild
cough at this stage, and was treated with doxycycline (Ron-
axan vet®, Merial) 10 mg.kg–1 once daily for 14 days which
was initiated to take care of the potential concurrent in-
fection with W. pipientis. Ivermectin therapy at 300 µg.kg–1
was continued every two weeks for six months.
Three months later, a serological antigen test was car-
ried out (immunoassay, Laboklin Laboratories, Germany)
and the test was negative. Six months later, the dog was
presented to the clinic in very good physical condition and
had stopped coughing. The breathing pattern and respira-
tory rate were normal.
DISCUSSION
This case of canine dirofilariasis in a seven-year-old
patient was diagnosed based on the history, clinical signs
observed, the laboratory investigations (PCV, CBC, Knott’s
test) and radiographic findings. This agrees with  V a t n e  by  B a r r  et al. [3].
[35] who reported canine dirofilariasis in a three-year-old
dog. With a prepatent period of about six months, where
female D. immitis worms grow between 13.5 to 30.5 cm
long and can start producing microfilariae, it is unlikely to
see clinical signs in dogs younger than one-year-old [8].
The long duration of coughing episodes in the bitch
coupled with the previous administration of tylosin with-
out remission aided in the diagnosis of this case. An adult
Fig. 4. The lateral thoracic radiographic view of the animal showing
right ventricular hypertrophy with pulmonary arterial enlargement
and increased bronchial opacification consistent with canine dirofila­
riasis
worm can survive for up to seven years in the primary host,
while microfilariae have a lifespan of up to two years, hence
the long duration [27]. Clinical signs seen are consistent
with other cases of moderate canine dirofilariasis reported
[4, 13, 23]. Eosinophilia is most often seen in dirofilariasis
which is caused by the body’s cellular response to the cir-
culating microfilaria in the blood vessels.
The modified Knott’s method [28] was used for the di-
agnosis of the blood parasite in this case, a method that is
more sensitive than a thin smear in diagnosing microfilari-
ae and it helps in concentrating microfilariae for easy iden-
tification. The parasitological technique is a type of con-
centration test used in screening parasites in blood of low
parasitaemia and this technique is used to distinguish be-
tween Dirofilaria and Dipetalonema species. A stationary
rather than a migratory pattern of movement is indicative
of Dirofilaria species when viewed under the microscope.
Another diagnostic technique used to aid in diagnosing
this case was radiography. The lateral view of the thoracic
region of the pet showed enlargement of the right chamber
of the heart and pulmonary artery, as previously reported
Ivermectin, a macrocyclic lactone, was administered
as an endectocide, subcutaneously once every two weeks.
It  works by the activation of glutamate-gated chloride
channels, preventing the secretion of immunomodulatory
proteins by the parasite, resulting in increased vulnerabili-
ty of the worm to attack by the host’s immune system [36].
According to  N e l s o n  et al. [21], the use of ivermectin
can be used to treat the adult stages of the worm. Enalapril
79
and digoxin were dispensed as a supportive treatment in
this case to reduce and alleviate the cardiopulmonary signs
in the pet. Enalapril, an angiotensin converting enzyme in-
hibitor, is indicated for the treatment of congestive heart
failure and hypertension. This drug, whose use in dogs in
well tolerated, acts by preventing the formation of angio-
tensin-11 (a potent vasoconstrictor) by competing with
angiotensin-1 for the enzyme angiotensin-converting en-
zyme. [9]. Digoxin, a cardio-tonic glycoside, also indicated
for use in the treatment of congestive heart failure in dogs
was administered to the dog. The drug acts by increasing
myocardial contractility with increased cardiac output.
CONCLUSIONS
A case of canine dirofilariasis based on the history,
clinical findings, laboratory investigations and radiogra-
phy were presented. Veterinarians, physicians, pathologists
and parasitologists should have an increased awareness of
this entity. Various epidemiological and diagnostic means
for the identification and molecular characterization of the
species, and natural hosts can help to establish low prev-
alence rates of this emerging zoonosis and devise control
measures.
REFERENCES
1. Alho, A. M., Marcelino, I., Colella, V., Flanagan, C., Silva,
N., Correia, J. J., et al., 2017: Dirofilaria immitis in pinnipeds
and a new host record. Parasit. Vectors, 10, 142. DOI: 10.1186/
s13071-017-2073-0.
2. Anyanwu, I. N., Agbede, R. I., Ajanusi, O. J., Umoh, J. U.,
Ibrahim, N. D., 2000: The incrimination of Aedes (stego-
myia) aegypti as the vector of Dirofilaria repens in Nigeria.
Vet. Parasitol., 92, 319—327. DOI: 10.1016/S0304-4017(00)
00311-3.
3. Barr, C. M.,  Boynton, E. P.,  Schmidt, P. L.,  Bossong,
F.,  Johnston, G. R., 2011: Diagnosis of canine heartworm
infection. Today’s Vet. Practice, 30—37.
4. Bhoomika, M. P., Murugavelu, M., 2019: Dirofilariasis: An
emerging zoonoses. J. Pharmacogn. Phytochem., 8, 3, 3014—
3018.
5. Boreham, P. F., Atwell, R. B., 2017: Dirofilariasis. CRC Press,
Boca Raton, 29—46.
80
6. Borthakur, S. K., Deka, D. K., Islam, S., Sarmah, P C.,
2016: Occult dirofilariosis in dogs of North Eastern region in
India. J. Arthropod-Borne Dis., 10, 1, 92—97.
7. Bowman, D., Little, S. E., Lorentzen, L., Shields, J., Sulli-
van, M. P., Carlin, E. P., 2009: Prevalence and geograph-
ic distribution of Dirofilaria immitis, Borrelia burgdorferi,
Ehrlichia canis, and Anaplasma phagocytophilum in dogs in
the United States: results of a national clinic-based serologic
survey. Vet. Parasitol., 160, 1—2, 138—148. DOI: 10.1016/j.
vetpar.2008.10.093.
8. Calvert, C. A., Rawlings, C. A., McCall, J. W., 1999: Canine
heartworm disease. In Fox, P. R., Sisson, D., Moïse, N. S.:
Textbook of Canine and Feline Cardiology Principles and Clin-
ical Practice. 2nd edn., Saunders, Philadelphia, 702—726.
9. Campbell, D. J., 1995: Angiotensin converting enzyme
(ACE) inhibitors and kinin metabolism: evidence that ACE
inhibitors may inhibit a kininase other than ACE. Clin. Exp.
Pharmacol. P.,  22, 12, 903—911. DOI: 10.1111/j.1440-1681.
1995.tb02325.x.
10. Copland, M. D., O’Callaghan, M. G., Hajduk, P., O’Dono-
ghue, P. J., 1992: The occurrence of Dirofilaria immitis in dogs
in South Australia. Aust. Vet. J., 69, 31—32. DOI:  10.1111/
j.1751-0813.1992.tb07429.x.
11. Ezema, K. U., Bukar, Y. M., Konto, M., Malgwi, S. A., 2019:
Serological and parasitological survey of canine Dirofilaria
immitis infection in Maiduguri, Borno state, Northeastern
Nigeria.  Alex. J. Vet. Sci.,  62, 2, 11—15. DOI: 10.5455/ajvs.
31614.
12. Fan, C.  K., Su, K.  E., Lin, Y.  H., Liao, C.  W., Du, W.  Y., Chiou,
H. Y., 2001: Seroepidemiologic survey of Dirofilaria immitis
infection among domestic dogs in Taipei city and mountain
aboriginal districts in Taiwan (1998—1999). Vet. Parasitol.,
102, 113—120. DOI: 10.1016/S0304-4017(01)00511-8.
13. Genchi, C., Kramer, L. H., Prieto, G., 2001: Epidemiology
of canine and feline dirofilariasis, a global view. In Simón,
F., Genchi, C.: Heartworm Infection in Humans and Animals.
Ediciones Universidad de Salamanca, Salamanca, 121—134.
14. Henry, L. G., Bruson, K. J., Walden, H. S., Wenzlow, N.,
Beachboard, S. E., Barr, K., Long, M., 2018: Comparison
of six commercial antigen kits for detection of Dirofilaria
immitis infection in canine with necropsy-confirmed heart-
worm status. Vet. Parasitol., 30, 254, 178—182. DOI: 10.1016/
j.vetpar. 2018.02.037.
15. Hoch, H., Strickland, K., 2008: Canine and feline dirofila-
riasis: life cycle, pathophysiology, and diagnosis. Compendi-
um, 30, 3, 133—141.
16. Kittleson, M. D., 1998: Heartworm infestation and disease
(Dirofilariasis). In Kittleson, M. D., Kienle, R. D.: Small Ani-
mal Cardiovascular Medicine. Mosby, St. Louis, 370—401.
17. McCall, J. W., Genchi, C., Kramer, L. H., Guerrero, J., Venco,
L., 2008: Heartworm disease in animals and humans. Adv. Par-
asitol., 66, 193—285. DOI: 10.1016/S0065-308X(08) 00204-2.
18. Mirahmadi, H., Maleki, A., Hasanzadeh, R., Ahoo, M. B.,
Mobedi, I., Rostami, A., 2017: Ocular dirofilariasis by Di-
rofilaria immitis in a child in Iran: a case report and review
of the literature. Parasitol. Int., 66, 978—981. DOI: 10.1016/j.
parint.2016.10.022.
19. Montoya-Alonso, J. A., Carretón, E., Juste, M. C., Mellado,
I., Morchón, R., Simón, F., 2010: Epidemiological survey of
canine heartworm disease on the island of Gran Canaria (Ca-
nary Islands-Spain) between 2000 and 2008. Vet. Parasitol.,
173, 165—168. DOI: 10.1016/j.vetpar.2010.06.008.
20. Nelson, C. T., McCall, J. W., Carithers, D., 2014: Current
canine guidelines for the prevention, diagnosis, and man-
agement of heartworm (Dirofilaria immitis) infection in
dogs. Am. Heartworm Soc., 1—30.
21. Nelson, C. T., McCall, J. W., Rubin, S. B., Buzhardt, L. F.,
Dorion, D. W., Graham, W. et al., 2005:  Guidelines for the
diagnosis, prevention and management of heartworm (Diro-
filaria immitis) infection in dogs.  Vet. Parasitol.,  133, 2—3,
255—266.
22. Ogbaje, C. I., Danjuma, A., 2016: Prevalence and risk fac-
tors associated with Dirofilaria immitis infection in dogs in
Makurdi, Benue State, Nigeria. J. Adv. Vet. Anim. Res., 3, 4,
338—344. DOI: 10.5455/javar.2016.c170.
23. Otranto, D., Brianti, E., Dantas-Torres, F., Weigl, S., Lat-
rofa, M. S., Gaglio, G., et al., 2011: Morphological and mo-
lecular data on the dermal microfilariae of a species of Cer-
copithifilaria from a dog in Sicily. Vet. Parasitol., 182, 2—4,
221—229. DOI: 10.1016/j.vetpar.2011.05.043.
24. Prichard, R. K., Geary, T. G., 2019: Perspectives on the util-
ity of moxidectin for the control of parasitic nematodes in
the face of developing anthelmintic resistance. Inter. J. Par-
asitol.-Drug, 10, 69—83. DOI: 10.1016/j.ijpddr.2019.06.002.
25. Reifur, L., Thomaz-Soccol, V., Montiani-Ferreira, F., 2004:
Epidemiological aspects of filariosis in dogs on the coast of
Paraná state, Brazil: with emphasis on Dirofilaria immitis. Vet.
Parasitol., 122, 273—286. DOI: 10.1016/j.vetpar.2004.05.017.
26. Schwand, E. V., Durand, D. T., 2002: Canine filariosis caused
by Dirofilaria immitis in Mozambique: a small survey based
on the identification of microfilariae. J. S. Afr. Vet. Assoc., 73, 3,
124—126. DOI: hdl.handle.net/10520/EJC99482.
27. Simón, F., Siles-Lucas, M., Morchón, R., González-Miguel,
J., Mellado, I., Carretón, E., et al., 2012: Human and ani-
mal dirofilariasis: The emergence of a zoonotic mosaic. Clin.
Microbiol. Rev., 25, 507—544. DOI: 10.1128/CMR.00012-12.
28. Simonsen, P. E., Fischer, P. U., Hoerauf, A., Weil, G. J.,
2014: The filariases. In Manson’s Tropical Infectious Diseas-
es, 23rd edn., 737—765. DOI: 10.1016\B978-0-7020-5101-2.
00055.8.
29. Song, K. H., Park, J. E., Lee, D. H., Lee, S. H., Shin, H. J.,
2010: Serological update and molecular characterization of
Dirofilaria immitis in dogs. South Korea Res. Vet. Sci., 88,
467—469. DOI: 10.1016/j.rvsc.2009.10.007.
30. Su, W. L., Shyu, J. Z., Chiang, G. H., Wang, M. H., Pan,
M. J., 2004: Clinical pathologic, electrocardiographic and
echocardiographic findings in the Taiwanese dogs with
Class 1 or 2 dirofilariasis. Adv. Anim. Cardiol., 37, 2, 47—56.
DOI: 10.11276/jsvc.37.47.
31. Svobodova, V., Svobodova, Z., Beladicova, V., Valentova,
D., 2005: First case of canine dirofilariosis in Slovakia: a case
report. Vet. Med., 50, 11, 510—512.
32. Tabar, M. D., Altet, L., Martinez, V., Roura, X., 2013: Wol-
bachia, filariae and Leishmania coinfection in dogs from a
Mediterranean area. J. Small Anim. Pract., 54, 4, 174—178.  
DOI: 10.1111/jsap.12041.
33. Turner, J. D., Marriott, A. E., Hong, D., O’Neill, P., Ward,
S. A., Taylor, M. J., 2020: Novel anti-Wolbachia drugs, a new
approach in the treatment and prevention of veterinary fil-
ariasis ?  Vet. Parasitol.,  279, 109057. DOI: 10.1016/j.vetpar.
2020.109057.
34. Ugochukwu, C. I. I., Omekam, N., Ugochukwu, E. I., 2016:
Incidence of Dirofilaria immitis in dogs presented at Univer-
sity of Nigeria, Nsukka Veterinary Teaching Hospital, using
wet smear and buffy coat techniques. Asian Pac. J. Trop. Dis.,
8, 627—630. DOI: 10.1016/S2222-1808(16)61098-8.
35. Vatne, L. I., 2015: Heartworm infection caused by Dirofilar-
ia immitis in a dog imported to Norway. Eur. J. Companion
Anim. Pract., 25, 4, 60—67. DOI: http://www.ejcap.org.
36. Wolsttenholme, A. J., Vatta, A., Sloan, M., Camus, M., Rog-
ers, A., Evans, C., et al., 2013: What do the macrocyclic lac-
tones do to heartworms, and how do they do it ? Heartworms
today: the search for solutions symposium. Am. Heartworm
Soc., 22—23.
Received April 20, 2020
Accepted August 17, 2020
81
 FOCUS < COMPANION ANIMAL

Case study: Canine heartworm disease

diagnosed in Ireland

A case of heartworm was

detected in a dog at the
UCD Veterinary Hospital
in the latter end of 2019.

Esther López Bailén DVM, internal medicine intern, University College Dublin
Veterinary Hospital, presents an intriguing case study detailing the detection,
diagnosis and treatment of heartworm in a Staffordshire bull terrier-cross

INTRODUCTION non-productive cough and recent episodes of haemoptysis.

Dirofilaria immitis (D. immitis) is a zoonotic filarial
nematode transmitted by mosquitoes of the species Culex,
Aedes, and Anopheles, that causes heartworm disease
in many species including dogs and cats. In recent years,
there has been an increase in the spread of this pathogen
from southern to more northern European countries. This is
thought to reflect both environmental and climatic factors,
as well as the more frequent movement of pets within the
European Union (EU). To the author's knowledge, there
have been no previous publications reporting heartworm
infection in dogs in Ireland.
HISTORY AND PHYSICAL EXAMINATION
A three-year-old female neutered, Staffordshire bull terrier-
cross was presented to University College Dublin Veterinary
Hospital in September 2019 with a four-month history of a dry,
The dog had tested positive for D. immitis antigen (SNAP
4DX Plus test, IDEXX); the most recent test was performed
one week prior to presentation. The dog had been imported
from the Canary Islands (Spain) in September 2019 following
rehoming from an animal shelter in May 2019. Treatment in
Spain and Ireland prior to presentation had included injectable
moxidectin and topical fluralaner.
At presentation, the dog was bright, alert, and responsive
with a body condition score of four out of nine. The mucous
membranes were pink and moist with a capillary refill time of
fewer than two seconds. Cardiac and thoracic auscultation
were unremarkable; the heart rate was 136 beats per minute
and the dog was moderately tachypneic with a respiratory rate
of 48 breaths per minute. The rectal temperature was 38.9oC.
No abnormalities were found on abdominal palpation and
peripheral lymph nodes were within normal limits.

Veterinary Ireland Journal I Volume 10 Number 5 251

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 FOCUS > COMPANION ANIMAL
DIAGNOSIS
Routine blood tests were performed, with haematology showing
mild thrombocytopenia (103 x 109/L; reference interval (RI) 150-
500 x109/L) and a mild lymphocytosis 3.97 x 109/L; RI (1-3.6).
Biochemistry and urinalysis were unremarkable. Antigen test for
vector-borne diseases (SNAP 4DX Plus test, IDEXX: D. immitis,
Ehrlichia canis, Ehrlichia ewingii, Borrelia burgdorferi, Anaplasma
phagocytophilum, Anaplasma platys) was positive for D. immitis.
A modified Knott’s test (filtration method for the detection of
microfilaria) was negative.
Thoracic radiographs revealed enlargement of the pulmonary
arteries, mild to moderate right ventricular enlargement and a
moderate diffuse, unstructured interstitial pattern with patchy
alveolar areas within the right cranial and middle lung lobes
(see Figures 1 and 2). Echocardiography revealed right atrial
enlargement with bulging of the interatrial septum to the left, mild
subjective enlargement of the right ventricle and mild to moderate
central pulmonic regurgitation with a mildly elevated velocity
(2.8m/s; reference value <2.2m/s). The pulmonary artery was
mildly enlarged and contained multiple mobile, tortuous linear
hyperechoic structures, likely to reflect the presence of adult
worms (see Figure 3). The laboratory test results in combination
with the imaging findings were consistent with a diagnosis of
canine dirofilariasis.
Figure 1: Left lateral radiograph of the thorax. There is
enlargement of the right cranial lobar artery (yellow arrows)
and of the right caudal lobar artery (red arrows). Increased
contact between the cardiac silhouette and the sternum is
present, indicating right ventricular enlargement (green arrows).
A patchy alveolar pattern is located within the right caudal lung
lobe (white arrows).
Figure 2: Oblique dorso-
ventral projection of the
thorax. The red arrows
indicate enlargement of
the right caudal lobar
pulmonary artery, as
seen in Figure 1.
252 Veterinary Ireland Journal I Volume 10 Number 5
Vet May 20.indd 252
TREATMENT
Initial treatment consisted of prednisolone (day 0) – 0.5mg/kg
orally, twice daily (BID), for seven days followed by a gradual
dosage reduction over a four-week period. On day one, oral
doxycycline – 10mg/kg orally BID was commenced for 28 days
– and a monthly macrocyclic lactone, in this case ivermectin
– 6mcg/kg, subcutaneously, given at the referring practice –
were also started. The dog was discharged the same day with
strict instructions for complete exercise restriction with the
aim of minimising the risk of thromboembolic complications.
A repeat appointment was planned for day 60, to allow for re-
evaluation and administration of the first dose of melarsomine
dihydrochloride (2.5mg/kg intramuscularly into the epaxial
muscles). The plan would then have been to follow this
with a second and third dose of this drug on days 90 and 91
respectively.
The owner contacted us one month after discharge reporting
that the dog had deteriorated during the preceding days,
showing frequent episodes of coughing, some of them
productive with a transparent mildly blood-tinged mucoid
material expectorated. At this point, access to melarsomine
was not yet possible due to the requirement for a special
license. Melarsomine is not currently an authorised veterinary
medicinal product within Ireland, and a delay would have
ensued whilst seeking to obtain the necessary importation
license. Re-starting the original treatment protocol with
prednisolone and doxycycline with continued strict rest was
advised whilst the melarsomine and license were accessed.
Despite this management, the dog’s respiratory condition
deteriorated again one month later, and she re-presented to
us a few days later for reassessment. The prednisolone had
been stopped one week prior to this presentation, resulting in
a recurrence of the episodes of cough and hemoptysis within
a few days, which had then progressed in severity.
When re-presented, the dog was hypoxemic and required
oxygen therapy. Haematology, biochemistry and standard
coagulation times were unremarkable, and the antigen
test for D. immitis was now negative. Thoracic radiographs
revealed right-sided cardiomegaly, a worsening of the
alveolar lung pattern, consistent with haemorrhage or
pneumonia, and a severe widening of the right cranial lobar
pulmonary artery. Echocardiography confirmed enlargement
of the right side of the heart and showed severe tricuspid
insufficiency with increased regurgitation velocity (3.95m/s;
reference value <2.8m/s), suggesting severe pulmonary
hypertension, likely to be the result of the heavy worm
burden identified in the right branch of the pulmonary artery.
The dog remained hospitalised for two days, initially with
oxygen supplementation. Glucocorticoid treatment was
re-commenced, initially with dexamethasone, at 0.1mg/kg
intravenously, once daily (SID); then, oral prednisolone at 0.5
mg/kg SID, as well as doxycycline at 10mg/kg, orally SID.
Given the presence of pulmonary hypertension, as evidenced
by the abnormal increase in tricuspid regurgitation velocity in
the absence of pulmonic stenosis, the dog was also started on
28/04/2020 16:51
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Vet May 20.indd 253 28/04/2020 16:51

 FOCUS > COMPANION ANIMAL
sildenafil citrate at 1.25mg/kg orally, three times daily (TID).
It would have been preferential to include an adulticidal
treatment at this stage, however it was not possible to source
the melarsomine in compliance with Irish licensing. However,
based on recent literature1, a nine-month treatment protocol
against adult worms was started with monthly application of
topical imidacloprid 10%/moxidectin 2.5%, and the ongoing
doxycycline at 10mg/kg orally SID, for a total of 28 days.
Figure 3: Right parasternal cranial short axis view of the heart.
Multiple thin hyperechoic linear structures (red arrows),
consistent with adult heartworms, are located within the main
pulmonary artery (MPA). The main pulmonary artery is mildly
enlarged compared to the diameter of the aorta (Ao). PV =
pulmonary valve.
FOLLOW UP
Two months later, the dog was re-presented for assessment.
She was reported to have been doing very well with only mild
episodes of cough observed. Ongoing treatment at this stage
included prednisolone, sildenafil and monthly imidacloprid
10%/moxidectin 2.5%, having had three adulticidal topical
treatments, to date. At presentation, echocardiography
showed the presence of some adult worms in the right branch
of the pulmonary artery, however, these appeared to be less
numerous. Pulmonic and tricuspid valve insufficiency were
similar to the previous visit.
Topical treatment with imidacloprid 10%/moxidectin 2.5% was
to be continued for at least nine months while we continued
to source the melarsomine. The plan is to continue with
treatment at home and reassess the dog in six months. At the
time of writing, the dog was continuing to do well on treatment
at home with sildenafil citrate, prednisolone, and monthly
topical imidacloprid 10%/moxidectin 2.5%.
DISCUSSION
Dirofilariasis is a serious disease caused by infection with
the filarial nematode, D. immitis, the canine heartworm.
This parasite is transmitted by at least 70 different species
of mosquitoes2 and results in a zoonotic disease affecting
mainly dogs and other wild canids, but also cats and, on
rare occasions, humans. Adult worms reside predominantly
in the pulmonary arteries and occasionally the right atrium
254 Veterinary Ireland Journal I Volume 10 Number 5
Vet May 20.indd 254
and ventricle of the heart of infected dogs causing severe
cardiopulmonary disease and even death.
The long lifecycle of D. immitis can last up to nine months
and starts when the mosquito vector ingests microfilariae
or L1 larvae with a blood meal from an infected host. L1
larvae mature in the mosquito to infective L3 larvae, which
are then injected back into another susceptible host. These
L3 microfilariae travel through the new host’s tissues to the
right pulmonary artery as they undergo multiple moults
and become adult worms. Once inside the animal’s heart,
adult worms begin to reproduce rapidly, and the viviparous
females release microfilariae directly into the host’s systemic
circulation. These female adult heartworms can grow up
to 30cm in length and live for up to five to six years. The
microfilariae are also able to survive for up to two years in
the systemic circulation, waiting for the arrival of a mosquito
intermediate host.
The clinical signs displayed by infected animals can range
from asymptomatic carriage or a mild cough through to
severe disease with cough, exercise intolerance, dyspnoea,
haemoptysis and syncope. In addition, dogs with a heavy
worm burden may present with what is known as caval
syndrome (also known as dirofilarial haemoglobinuria),
characterised by a sudden onset of severe lethargy,
weakness and pale mucous membranes accompanied by
haemoglobinaemia and haemoglobinuria. Intravascular lysis
of the red blood cells results from shear forces as the cells
effectively pass through a ‘sieve’ of heartworms present
in the right atrium and venae cavae, causing anaemia and
the characteristic haemoglobinuria resulting from this
intravascular haemolysis. Retrograde migration of adult
heartworms from the pulmonary arteries to the right ventricle,
right atrium, and vena cava can also cause disruption
of the tricuspid apparatus.3 Visualisation of heartworms
within the tricuspid valve and posterior vena cava with
echocardiography, together with the clinical signs, can aid the
diagnosis of this condition. Caval syndrome is typically rapidly
fatal without immediate treatment, consistent in surgical
extraction of the adult worms.
Wolbachia pipiens is a gram-negative endosymbiotic bacteria
known to play an important role in the dirofilarial life cycle
and pathogenesis of filarial disease, although the full details
of this complex interaction are not completely understood.
This bacterium is involved in the promotion of larvae moulting
and additionally provides the female worm with iron, an
essential component for the biosynthesis of both steroidal
and non-steroidal hormones necessary for embryogenesis of
filariae.4,5 In return, the bacterium gains amino acids from the
Dirofilaria filariae that promote bacterial growth.6 Dirofilarial
disease results in a reduction in the host’s renal perfusion
as a result of the inflammatory process and the presence of
vascular thrombosis. In addition to this, direct damage to renal
capillaries and the interstitium of blood vessels results from
the presence of microfilariae and it further contributes to the
development of renal disease. Compounding this situation,
28/04/2020 16:51

when Wolbachia sp. are released into host tissues allowing
the death of microfilariae or adult worms, bacteria-derived
molecules, including Wolbachia-surface protein (WSP),
can induce an innate pro-inflammatory response7 and, as
a consequence, the accumulation of polymorphonuclear
leukocytes in both kidneys and pulmonary arterial walls.
This exposure to both bacterial antigens and metabolites is
recognised to exacerbate D. immitis-induced nephropathy
and pulmonary disease.8,9 Antimicrobial therapy directed
against this bacterium has been shown to result in decreased
microfilarial loads, inhibition of the development of larval
stages, female worm infertility, and reduced numbers of
Wolbachia sp. organisms within all stages of D. immitis10,
resulting in a reduction in the overall disease severity in
affected patients.
Diagnosis of dirofilariasis in dogs is based on the detection of
microfilariae and/or the detection of circulating heartworm
antigens in combination with compatible clinical examination,
and diagnostic imaging findings.11 Haematology and
serum biochemistry findings in affected animals are often
unremarkable but in some cases, there may be secondary
non-specific abnormalities such as anaemia, eosinophilia,
basophilia or a stress leukogram.12,13
Treatment of dirofilariasis is aimed to eliminate all life stages
of the parasite (microfilariae, larval stages, juveniles, and
adults) along with minimising post-treatment complications.14
The main post-adulticidal treatment complications include
thromboembolism and intense pro-inflammatory reactions
within the lung parenchyma.15 In view of this, stabilisation
of affected animals prior to adulticidal treatment is
recommended with the use of glucocorticoids, such as
prednisolone, at anti-inflammatory doses to decrease the
systemic inflammation triggered by the parasite.
Adjunct therapy with a 28-day course of doxycycline and
prednisolone prior to the administration of melarsomine
is recommended to try minimising the post-adulticidal
treatment complications. Ideally, adulticidal treatment
involves administration of three intramuscular injections
of melarsomine dihydrochoride, an arsenic-containing
compound. This drug should be administered by deep
intramuscular injection in the epaxial muscles in the
third through fifth lumbar region. Drugs belonging to the
macrocyclic lactone class (eg. avermectins and milbemycins)
are recommended for routine heart worm prophylaxis.
These drugs are also effective against susceptible larval
stages and, in some instances, against juveniles and adult
heartworms.16,17 These drugs, together with the application
of an EPA-registered mosquito repellent/ectoparasiticide to
reduce exposure to mosquitoes, is recommended all year
round in endemic countries, as well as for dogs travelling to
these affected areas.14 Exercise restriction is critical for the
entire duration of the treatment, which is thought to reduce
the vascular inflammation and incidence and severity of
thromboembolic events. Recent research has suggested that
shorter protocols, with a faster elimination of heartworms are
Vet May 20.indd 255
FOCUS < COMPANION ANIMAL
effective and have better owner compliance.18
In addition, recent research1 has shown some efficacy of
topical imidacloprid 10%/moxidectin 2.5% spot on together
with doxycycline as an adulticidal therapy. The study showed
that monthly application for nine months resulted in antigen-
negative test in 14/15 dogs in the study. However, this
treatment is considered to be a ‘slow kill’ treatment, requiring
up to a year of treatment, and sometimes much longer. When
the infection is not addressed quickly with an adulticidal
therapy, there is a greater risk of permanent damage to the
pulmonary arterial system, such as fibrosis or pulmonary
arterial hypertension, leading to a necessity for life-long
treatment with sildenafil citrate and/or glucocorticoids.
Sildenafil citrate is a highly selective phosphodiesterase
type V inhibitor that results in increased concentrations of
cyclic guanosine monophosphate and subsequently nitric
oxide-mediated vasodilation.19 It is thought that, when used in
dogs with intracardiac heartworm, it may help mobilising the
heartworms by decreasing pulmonary arterial pressure, and
can thus contribute to improved cardiac output. 20 In view of
these disadvantages, this ‘slow kill’ treatment is currently not
recommended over adulticidal treatment with melarsomine,
with further research into alternative treatments required.
The prognosis for heartworm infection is generally good when
not associated with many clinical signs. The prognosis for
severely affected animals that present with caval syndrome,
massive embolisation, severe pulmonary arterial disease
or heart failure, is guarded, although most cases can be
successfully managed. In this case, the prognosis remains
guarded, in view of the severity of the disease and inability
to source the recommended adulticidal drug. In addition, the
current pulmonary arterial hypertension could progress, and
the dog develop right sided congestive heart failure (CHF).
In view of this, ongoing monitoring for the development of
clinical signs such as pleural effusion, hepatosplenomegaly
or ascites is strongly recommended. Should the dog do well
with the topical adulticidal treatment and prednisolone alone,
the melarsomine may not be essential. However, should it
be sourced, its use would be recommended to increase the
response to treatment and reduce the exposure time to adult
worms.
Historically, heartworm was present only in the southern
European countries, however this distribution has been
continuously changing in recent years due to environmental
and climate change factors, along with changes in the
movement of pets within the European Union. This increased
transit has resulted in the exposure of pets to a variety of
microbial and parasitic pathogens they would have previously
never been exposed to and also have no natural immunity
against. Currently, D. immitis has been found in mosquitoes in
Germany and the infection has been reported in non-endemic
northern European countries such as Czech Republic,
Hungary, Serbia, Switzerland, Romania, Poland and most
recently in Lithuania and Cyprus.21,22 A survey published in
2004 evaluated veterinary awareness and perceptions of
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 FOCUS > COMPANION ANIMAL
canine heartworm in western Europe. It stated that, overall,
10% of the veterinarians in non-endemic areas reported an
increasing number of cases and that heartworm infection
could become endemic in previously non-endemic areas
within the next five to 10 years. 23 This observation emphasises
the importance of vigilance and awareness against this
disease for veterinarians practicing in Ireland and other non-
endemic areas.
RESEARCHERS
• Esther López Bailén DVM, Internal Medicine intern,
University College Dublin Veterinary Hospital
• Carlos Martinez Gil LV Dip ECVIM-CA, Aúna Especialidades
Veterinarias
• Eimear Shorten DVM, resident in Diagnostic Imaging,
University College Dublin Veterinary Hospital
• Emma J O’Neill BSc BVSc PhD DSAM ECVIM-CA,
University College Dublin Veterinary Hospital
REFERENCES
1. Genchi M, Vismarra A, Lucchetti C, Viglietti A, Crosara S,
Gnudi G, et al. Efficacy of imidacloprid 10%/moxidectin
2.5% spot on (Advocate®, Advantage Multi®) and
doxycycline for the treatment of natural Dirofilaria immitis
infections in dogs. Veterinary parasitology. 2019;273:11-6.
2. Cancrini G, Magi M, Gabrielli S, Arispici M, Tolari F,
Dell'Omodarme M, et al. Natural vectors of dirofilariasis in
rural and urban areas of the Tuscan region, central Italy. J
Med Entomol. 2006;43(3):574-9.
3. Strickland KN. Canine and feline caval syndrome. Clinical
techniques in small animal practice. 1998;13(2):88-95.
4. Bandi C, Dunn AM, Hurst GD, Rigaud T. Inherited
microorganisms, sex-specific virulence and reproductive
parasitism. Trends Parasitol. 2001;17(2):88-94.
5. Negri I, Pellecchia M, Grève P, Daffonchio D, Bandi
C, Alma A. Sex and stripping: The key to the intimate
relationship between Wolbachia and host? Commun
Integr Biol. 2010;3(2):110-5.
6. Foster J, Ganatra M, Kamal I, Ware J, Makarova K,
Ivanova N, et al. The Wolbachia genome of Brugia malayi:
endosymbiont evolution within a human pathogenic
nematode. PLoS Biol. 2005;3(4):e121.
7. Saint André Av, Blackwell NM, Hall LR, Hoerauf A,
Brattig NW, Volkmann L, et al. The role of endosymbiotic
Wolbachia bacteria in the pathogenesis of river blindness.
Science. 2002;295(5561):1892-5.
8. Kramer LH, Tamarozzi F, Morchón R, López-Belmonte
J, Marcos-Atxutegi C, Martín-Pacho R, et al. Immune
response to and tissue localization of the Wolbachia
surface protein (WSP) in dogs with natural heartworm
(Dirofilaria immitis) infection. Vet Immunol Immunopathol.
2005;106(3-4):303-8.
256 Veterinary Ireland Journal I Volume 10 Number 5
Vet May 20.indd 256
9. Nelson CT, Myrick ES, Nelson TA. Clinical benefits of
incorporating doxycycline into a canine heartworm
treatment protocol. Parasit Vectors. 2017;10(Suppl 2):515.
10. Frank K, Heald RD. The emerging role of Wolbachia
species in heartworm disease. Compend Contin Educ Vet.
2010;32(4):E4.
11. (ESDA) ESoDaA. Guidelines for clinical management of
canine heartworm disease. ESDA; 2017.
12. Tilley LaS, FWK. The 5-minute Veterinary Consult (Fourth
Edition): Blackwell; 2004.
13. Co M. The Merck Veterinary Manual (Eight Edition):
Merial; 2008.
14. Society AH. Current canine guidelines for the prevention,
diagnosis, and management of heartworm (Dirofilaria
immitis) infection in dogs. American Heartworm Society
Wilmington, DE; 2018.
15. Kramer L, Grandi G, Passeri B, Gianelli P, Genchi M,
Dzimianski MT, et al. Evaluation of lung pathology in
Dirofilaria immitis-experimentally infected dogs treated
with doxycycline or a combination of doxycycline
and ivermectin before administration of melarsomine
dihydrochloride. Vet Parasitol. 2011;176(4):357-60.
16. McCall J, Guerrero J, Roberts R, Supakorndej N, Mansour
A, Dzimianski M. Further evidence of clinical prophylactic,
retro-active (reach-back) and adulticidal activity of
monthly administrations of ivermectin (Heartgard Plus™)
in dogs experimentally infected with heartworms. 2001.
17. McCall JW, Genchi C, Kramer LH, Guerrero J, Venco L.
Heartworm disease in animals and humans. Advances in
parasitology. 2008;66:193-285.
18. Carretón E, Falcón-Cordón Y, Falcón-Cordón S, Morchón
R, Matos JI, Montoya-Alonso JA. Variation of the adulticide
protocol for the treatment of canine heartworm infection:
Can it be shorter? Vet Parasitol. 2019;271:54-6.
19. Humbert M. Sitbon O, Simonneau G. Treatment
of pulmonary arterial hypertension N Engl J Med.
2004;351:1425-36.
20. Tjostheim S, Kellihan H, Grint K, Stepien R. Effect of
sildenafil and pimobendan on intracardiac heartworm
infections in four dogs. Journal of Veterinary Cardiology.
2019;23:96-103.
21. Sabūnas V, Radzijevskaja J, Sakalauskas P, Paulauskas A.
First Report of Heartworm (Helminthologia. 2019;56(1):57-
61.
22. Kokkinos P, Dimzas D, Pantchev N, Tamvakis A, Balzer
J, Diakou A. Filarial infections in dogs in Cyprus, an
apparently heartworm free island. Vet Parasitol Reg Stud
Reports. 2019;18:100330.
23. Genchi C, Bowman D, Drake J. Canine heartworm
disease (Dirofilaria immitis) in Western Europe: survey of
veterinary awareness and perceptions. Parasit Vectors.
2014;7:206.
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