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Kajian Pustaka: Dilatasi Kardiomiopati Pada Anjing

(DILATED CARDIOMYOPATHY IN DOG: A LITERATURE REVIEW)

Putu Intan Kusuma Wardani1,


I Gusti Made Krisna Erawan2
1
Mahasiswa Profesi Dokter Hewan,
2
Laboratorium Ilmu Penyakit Dalam Veteriner,
Fakultas Kedoteran Hewan Universitas
Udayana,
Jl. Sudirman, Sanglah, Denpasar, Bali, Indonesia, 80234
Telp/Fax: (0361) 223791
Email: intanksmwardani@gmail.com

ABSTRAK
Dilated Cardiomyopathy (DCM) adalah penyakit miokard utama, ditandai dengan pembesaran
ruang jantung dan disfungsi sistolik yang parah. Beberapa laporan menunjukkan bahwa DCM terutama
menyerang anjing ras besar. Usia umum saat diagnosis adalah 6 sampai 8 tahun. Tanda-tanda klinis
DCM meliputi kelemahan, kelesuan, takipnea atau dispnea, intoleransi olahraga, batuk, anoreksia,
distensi perut, asites, dan sinkop. DCM sekunder mungkin terkait dengan perubahan toksik, agen
infeksius, endokrinopati, dan gangguan nutrisi. Beberapa metode untuk diagnosis DCM, seperti
elektrikardiografi, radiografi toraks dan ekokardiografi. Penanganan pada kasus DCM dilakukan dengan
cara pemberian obat seperti pimobendane, furosemid, torasemid, taurin, ramipril, dan remocapril. Dua
dari tiga kasus mengalami kematian mendadak setelah mendapat pengobatan. Satu kasus lainnya tetap
stabil dengan melanjutkan pengobatan.

Kata-kata kunci: dilated cardiomyopathy; jantung

ABSTRACT
Dilated Cardiomyopathy (DCM) is a major myocardial disease, characterized by enlargement of
the cardiac chambers and severe systolic dysfunction. Some reports indicate that DCM mainly affects
large breed dogs. The common age at diagnosis is 6 to 8 years. Clinical signs of DCM include weakness,
lethargy, tachypnea or dyspnea, exercise intolerance, cough, anorexia, abdominal distention, ascites, and
syncope. Secondary DCM may be associated with toxic changes, infectious agents, endocrinopathies, and
nutritional disorders. Several methods for the diagnosis of DCM, such as electrocardiography, chest
radiography and echocardiography. Treatment of DCM cases is carried out by administering drugs such
as pimobendane, furosemide, torasemid, taurine, ramipril, and remocapril. Two out of three cases
experienced sudden death after receiving treatment. One other case remained stable by continuing
treatment.

Keywords: dilated cardiomyopathy; heart


PENDAHULUAN

Dilatasi kardiomiopati atau dilated cardiomyopathy (DCM) adalah penyakit miokard


utama, ditandai dengan pembesaran ruang jantung dan disfungsi sistolik yang parah. Beberapa
laporan menunjukkan bahwa DCM terutama menyerang anjing ras besar, seperti Doberman
pinscher, Great Dane, Irish wolfhound, dan Scottish deerhound. Usia umum saat diagnosis
adalah 6 sampai 8 tahun. Namun, beberapa anjing mengembangkan DCM saat remaja dan mati
dalam beberapa bulan. Sejauh ini, bentuk remaja dari dilatasi kardiomiopati telah dilaporkan
hanya pada 3 ras yaitu Doberman pinscher, Portuguese water dog, dan toy Manchester terrier
(Shimizu et al., 2022).
Tanda-tanda klinis DCM meliputi kelemahan, kelesuan, takipnea atau dispnea, intoleransi
olahraga, batuk, anoreksia, distensi perut, asites, dan sinkop. Namun, tanda-tanda klinis mungkin
tidak diperhatikan sampai DCM berkembang. DCM sekunder mungkin terkait dengan perubahan
toksik, agen infeksius, endokrinopati, dan gangguan nutrisi. Laporan sebelumnya telah
menunjukkan bahwa tingkat taurin dan karnitin yang lebih rendah dapat mempengaruhi ras
seperti Standard schnauzer dan Portuguese water dogs, khususnya Cocker Spaniels. Selain itu,
DCM dapat terjadi jika anjing normal diberi lebih sedikit taurin dan karnitin. Pemberian
suplementasi taurin dapat meningkatkan waktu kelangsungan hidup mereka (An et al., 2021).

Penelitian sebelumnya telah melaporkan beberapa metode untuk diagnosis DCM, seperti
radiografi toraks dengan temuan termasuk kardiomegali, seringkali dengan pembesaran atrium
kiri, berbagai tingkat edema paru, kongesti vena, dan terkadang asites dan efusi pleura.
Ekokardiografi adalah penilaian yang paling berguna untuk mendiagnosis DCM. Mendiagnosis
adanya pembesaran ruang spesifik dan kegagalan miokard memerlukan M-mode dan
ekokardiografi dua dimensi (2D). Temuan ekokardiografi meliputi peningkatan dimensi akhir
diastolik ventrikel kiri, dimensi akhir sistolik, peningkatan pemisahan septum titik E (EPSS), dan
penurunan pemendekan fraksional (FS) (An et al., 2021).

METODE PENULISAN
Metode penulisan yang digunakan adalah penelusuran literatur. Penelusuran dilakukan
dengan melakukan pencarian data dari jurnal, buku, dan artikel yang terkait dari beberapa
sumber seperti ResearchGate, PubMed, dan Google scholar dengan menggunakan kata kunci
“Dilated Cardiomyopathy in Dog”. Kriteria artikel yang dipilih ialah artikel yang ditulis
dalam rentang
waktu 10 tahun terakhir, objek kasus merupakan jenis hewan anjing. Namun, penulis tidak
menutup kemungkinan dapat menggunakan literatur seperti buku yang ditulis di luar rentang
waktu 10 tahun terakhir, dengan tujuan untuk memperkaya informasi pada kajian pustaka ini.
Data dari literatur tersebut kemudian dikumpulkan seperti anamnesis, sinyalemen, pemeriksaan
klinis, dan pemeriksaan penunjang untuk digunakan sebagai pembanding antar kasus.

HASIL DAN PEMBAHASAN


Sinyalmen dan anamnesis
Anjing kasus dengan ras Shiba Inu betina berusia 6 bulan, dengan berat badan 6,2 kg; ras
Malta betina berusia 6 tahun, dengan berat badan 4,95 kg; dan ras Papillon betina berusia 11
tahun, dengan berat badan 2,1 kg. Ketiga anjing kasus rata-rata memiliki keluhan utama yang
sama yaitu mengalami batuk serta keluhan nafas cepat dan dangkal.
Pemeriksaan klinis
Pada salah satu kasus didapatkan auskultasi aritmia, dengan tingkat pernapasannya 132
per menit, dua dari tiga kasus pada auskultasi terdengar suara murmur sistolik (Levine 2/6).
Pemeriksaan penunjang
Pemeriksaan penunjang dari kasus ini yaitu pemeriksaan CBC (Complete Blood Count),
biokimia darah, elektrokardiografi (EKG), radiografi toraks, dan ekokardiografi. Dua dari tiga
kasus menyebutkan hasil pemeriksaan CBC yang menunjukkan hasil normal dan peningkatan
ringan neutrofil, dengan hasil biokimia darah menunjukkan hiperglikemia (162 mg/dL) dan
hipokalemia (3,1 mmol/L), dan konsentrasi tiroksin (3.21mg/dL) berada dalam rentang normal.
Temuan EKG untuk DCM meliputi pelebaran kompleks QRS, pelebaran dan bentukan
gelombang P, kompleks prematur ventrikel seragam atau multiform (VPC), dan takikardia
ventrikel paroksismal. Dalam kasus ini, EKG mengungkapkan gelombang P dan VPC yang
tinggi dan lebar.

Gambar 1. Elektrokardiogram anjing kasus menunjukkan gelombang P tinggi dan lebar dengan
kompleks prematur ventrikel (panah) (Sumber: An et al., 2021)
Radiografi toraks pada posisi dorsoventral dan lateral kanan menunjukkan atrium dan
ventrikel kiri yang membesar, meskipun pembesaran vena paru kranial ditunjukkan, edema paru
tidak diamati.

Gambar 2. Radiografi Dorsoventral (A) dan lateral kanan (B) diambil pada Hari 1. Meskipun
edema paru yang jelas tidak terlihat, pembesaran atrium kiri dan ventrikel kiri serta
pembesaran vena pulmonal kranial terlihat (Sumber: Shimizu et al., 2022).

Gambar 3. Radiografi toraks dorsoventral (A), lateral kanan (B), dan lateral kiri (C)
menunjukkan pembesaran moderat ventrikel kiri (kepala panah) dengan penonjolan
ringan pada atrium kanan (kepala panah putih) dan kiri (panah hitam). Pola alveolar
sedang (tanda bintang) di lobus paru kanan dan bagian kranial lobus paru kiri juga
terdeteksi (Sumber: An et al., 2021).

Gambar 4. Radiografi toraks gambar kiri mewakili pandangan dorsoventral, dan gambar kanan
mewakili pandangan lateral kanan. Opacity sedikit meningkat di bidang paru-paru.
Ukuran jantung vertebral (VHS) adalah 13,2 vertebra, menunjukkan pembesaran
jantung (Sumber; Saito et al., 2022).
Ekokardiografi dua dimensi menunjukkan regurgitasi mitral (MR), jantung sisi kiri yang
sangat melebar dan jantung sisi kanan yang sedikit membesar. Rasio LA:Ao adalah 2,45 (kisaran
referensi: <1,3). Dimensi akhir diastolik ventrikel kiri (LVDd) adalah 42,3 mm (normal: 22,0-
31,0 mm), dimensi akhir sistolik ventrikel kiri (LVD) adalah 37,3 mm (normal: 12,0-22,0 mm),
ketebalan septum interventrikular akhir diastolik 4,8 mm (normal: 4,0-9,0 mm), dan ketebalan
dinding posterior ventrikel kiri akhir diastolic adalah 4,1 mm (normal: 4,0-9,0 mm), dan
pemendekan fraksional (FS) adalah 11,8% (normal: 25,3%- 49,9%). Rekaman Doppler spektral
mengungkapkan kecepatan regurgitasi mitral yang tinggi (5,96 m/s).

Gambar 5. Sumbu panjang parasternal kanan (A, B) dan tampilan sumbu pendek (C)
menunjukkan atrium kiri (LA) dan ventrikel kiri (LV) yang melebar parah.
Ekokardiogram Doppler aliran warna (B) menunjukkan regurgitasi mitral eksentrik
selama sistol (panah). Rasio atrium kiri-aorta (LA/Ao) adalah 2,45 (C) (Sumber: An
et al., 2021).
Diagnosa
Diagnosa dari penyakit CDM didasarkan atas temuan klinis, pemeriksaan radiografi dan
ekokardiografi. Pada ketiga kasus tersebut telah dikonfirmasi bahwa anjing kasus didiagnosis
menderita penyakit dilatasi kardiomiopati.
Prognosis
Prognosis untuk anjing dengan DCM bervariasi mulai dari hari ke tahun, tergantung pada
banyak variabel (Tidholm, 2006), sedangkan waktu kelangsungan hidup ras Great Danes
dilaporkan lebih pendek dibandingkan anjing ras lainnya (Martin et al., 2010). Waktu bertahan
hidup diketahui terkait dengan tanda-tanda klinis terkait jantung, ekokardiografi atau kelainan
listrik jantung (Tidholm, 2006). Jika gejala menunjukkan gagal jantung kongesti, prognosisnya
seringkali buruk (An et al., 2021).

Penanganan
Pengobatan pada ketiga kasus dilakukan dengan pemberian obat ionotropik positif dan
vasodilatator yaitu pimobendan (0,2 – 0,3 mg/kg BB), obat golongan diuretik yaitu furosemid (2
mg/kg BB), torasemid (0,15 mg/kg BB), pemberian taurin (250 – 500 mg/ekor), dan obat ACE-
inhibitor ramipril (0,125 mg/kg BB), remocapril (0,1 mg/kg BB).
Dari tiga kasus DCM yang telah mendapat pengobatan, dua diantaranya mengalami
kematian mendadak. Dosis pimobendane sempat ditingkatkan dari 0,2 menjadi 0,36 mg/kg BB
setelah intoleransi olahraga kambuh. Anjing kasus kemudian dirujuk dengan tanda klinis gagal
jantung diberi resep diltiazem hydrochloride, pimobendan, dan torasemide. Namun, pada hari
1087, anjing tersebut mati mendadak, sedangkan anjing kasus lainnya setelah 10 hari masa
tindak lanjut pengobatan, anjing mengalami kematian mendadak (Shimizu et al., 2022; An et al.,
2021).

Gambar 6. Gambar histologis miokardium ventrikel kiri (pewarnaan HE) menunjukkan serat
miokard melemah dan bergelombang dengan atrofi dan penipisan. Selain itu, edema
stroma terlihat. Bar = 100mm (Sumber: Shimizu et al., 2022).

Pada anjing kasus yang bertahan hidup, pola makan anjing kasus diubah dari pola makan
bebas biji-bijian menjadi pola makan yang mengandung biji-bijian. Untuk pengobatan tidak ada
perubahan pada pengobatan oral (pimobendane [0,3 mg/kg BB], temocapril [0,1 mg/kg BB],
taurin [250 mg/ekor] dan furosemid [2,0 mg/kg BB]) sejak hari ke-10 hingga hari ke-1191.
Karena
peningkatan fungsi jantung diamati setelah perubahan diet, diagnosis klinis DCM terkait diet
dibuat, dan pasien melanjutkan diet yang mengandung biji-bijian. Mengenai pengobatan oral,
furosemide dan taurine dihentikan, sedangkan temocapril dan pimobendan dilanjutkan dalam
dosis yang sama. Pasien tetap stabil selama 1262 hari, tanpa kekambuhan gagal jantung (Saito et
al., 2022).
SIMPULAN
Dilatasi kardiomiopati adalah penyakit miokard utama, ditandai dengan pembesaran
ruang jantung dan disfungsi sistolik yang parah. Tanda-tanda klinis DCM meliputi kelemahan,
kelesuan, takipnea atau dispnea, intoleransi olahraga, batuk, anoreksia, distensi perut, asites, dan
sinkop. Beberapa metode untuk diagnosis DCM, seperti elektrikardiografi, radiografi toraks dan
ekokardiografi.
SARAN
Anjing dengan kasus dilatasi kardiomiopati perlu dilakukan pemantauan yang intensif
karena terdapat resiko kematian mendadak, serta harus rutin memeriksakan anjing ke dokter
hewan.
UCAPAN TERIMA KASIH
Pada kesempatan ini penulis mengucapkan terimakasih kepada pihak Pengampu
Koasistensi Ilmu Penyakit Dalam Veteriner, Fakultas Kedokteran Hewan, Universitas Udayana
yang telah bersedia membantu penulis dalam memfasilitasi dan membimbing sampai
terselesaikannya kajian pustaka ini.

DAFTAR PUSTAKA
An S, Park J, Mok J, Kim A, Han C, Song JH, dan Lee HC. 2021. Imaging Diagnosis of Dilated
Cardiomyopathy in a Maltese Dog. Journal of veterinary clinics, 38(3): 163-168.
Martin M, Stafford Johnson M, Strehlau G, King J. 2010. Canine dilated cardiomyopathy: a
retrospective study of prognostic findings in 367 clinical cases. J Small Anim Pract 51:
428- 436.
Saito T, Suzuki R, Yuchi Y, Yasumura Y, Teshima T, Matsumoto H, dan Koyama H. 2022. A
Case of a Small-Breed Dog with Diet-Related Dilated Cardiomyopathy Showing Marked
Improvements in Cardiac Morphology and Function after Dietary Modification. Veterinary
Sciences, 9(11): 593.
Shimizu K, Suzuki R, Ikeda Y, Mochizuki Y, Teshima T, Michishita M, dan Koyama H. 2022. A
case of juvenile form of dilated cardiomyopathy in a 6-month-old Shiba Inu dog. The
Canadian Veterinary Journal, 63(2): 152.
Tidholm A. 2006. Survival in dogs with dilated cardiomyopathy and congestive heart failure
treated with digoxin, furosemide and propranolol: A retrospective study of 62 dogs. J Vet
Cardiol 8: 41-47.
Case Report

JV
pISSN 1598-298X • eISSN 2384-
0749 J Vet Clin
2021;38:163-168
https://doi.org/10.17555/jvc.2021.38.3.163

J ourna l

of Veterin
C ary Clinics

Imaging Diagnosis of Dilated Cardiomyopathy in


a Maltese Dog

Soyon An1 Copyright © The Korean Society of Veterinary Clinics

Junghyun Park1
Jinsu Mok1
Areum Kim1
Changhee
Han1
Joong Hyun Song2
Dohyeon Yu1
Tae Sung
Hwang1 Hee-
Chun Lee1,*

1
Institute of Animal Medicine,
Department of Veterinary Medical
Imaging, College of Veterinary Medicine,
Gyeongsang National University, Jinju
52828, Korea
2
Ulsan S Animal Medical Center,
Ulsan 44726, Korea

*Correspondence: lhc@gnu.ac.kr

ORCID
Soyon An:
https://orcid.org/0000-0002-9994-8760
Junghyun Park:
https://orcid.org/0000-0003-3354-5990
Jinsu Mok:
https://orcid.org/0000-0002-0620-5555
Areum Kim:
https://orcid.org/0000-0003-4048-8744
Changhee Han:
https://orcid.org/0000-0003-4018-445X
Joong Hyun Song:
https://orcid.org/0000-0001-9961-6451
Dohyeon Yu:
https://orcid.org/0000-0001-7645-6926
Tae Sung Hwang:
https://orcid.org/0000-0001-6730-6061
Hee-Chun Lee:
https://orcid.org/0000-0001-5936-9118
Abstract A 6-year-old, spayed generalized four chambers without remarkable findings of valvular degen-
female, Maltese dog with eration. M-mode echocardiography showed decreased left ventricular
tachypnea and dry cough was fractional shortening and enlarged left ventricular internal diameter at both
presented to Gyeongsang end-systolic and end-diastolic. Color-flow Doppler imaging revealed eccentric
National University Veterinary turbulent flow starting below the left ventricular outflow tract and extending
Medical Teaching hospital. On into the left atrium during systole. Spectral Doppler recordings revealed a high
physical examination, its velocity flow through the mitral, tricuspid, aorta, and pulmonic regurgitation.
respiration rate was 132 per Restrictive transmitral flow revealed high E-wave velocity, short E-wave
min- ute. Decreased partial deceleration time, and reduced A-wave velocity. There was also low ejection
pressure of oxygen, partial velocity thorough left ventricular out tract flow. Based on echocardiographic
pressure of carbon dioxide, and examination, dilated cardiomyopathy was the tentative diagnosis. The dog was
hyperlactatemia were found on medicated with inotropes, angiotensin converting enzyme inhibitor, and
arterial blood gas analysis. Its diuretics. At the 10-day following-up, the dog died suddenly. This report
diastolic blood pres- sure was 80 describes echocardiographic diagnosis and prognosis of dilated cardiomyopathy
mmHg. Auscultation revealed rarely reported in small breed dogs.
arrhythmia. Electrocardiogram
revealed P pulmonale, P mitrale,
Key words dilated cardiomyopathy, echocardiography, small breed, dog.
and ventricular premature
complexes. Thoracic radiographs
revealed mild enlargement of
both atrium and moderate
enlargement of the left
ventricular. There was also a
moderate alveolar pattern in the
right and caudal part of the left
cranial lung lobe. Two-
dimensional echocardiography
showed enlarge- ment of
Received July 9, 2020 / Revised February 23, 2021 / Accepted March 18, 2021

This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/
by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

www.ksvc.or.kr 163
Soyon An, et al.

Introduction Case Report


Dilated cardiomyopathy (DCM) is characterized by A 6-year-old spayed female Maltese dog weighting 4.95
im- paired contraction and dilation of both ventricles or the kg with dry cough and tachypnea was referred to
left ventricle (19). It is the most common myocardial Gyeongsang National University Veterinary Medical
disease in dogs (5,19,17,18,26). Causes of DCM in Teaching Hospital. She had dry cough for one month and
humans are mostly genetic factors. Myocardial ischemia, severe tachypnea for the previous two days. In physical
hypertension, toxins, infections, and metabolic disorders examination, auscultation revealed arrhythmia. Its
can also be causes of DCM (1,3,9,15,22,24). Feline DCM is respiratory rate was 132 per min and its diastolic blood
not common. It is usual- ly caused by taurine deficiency pressure was 80 mmHg. Electrocardio- gram revealed
(9,17,18,26). Primary DCM in dogs is an idiopathic tall and wide P wave that described atriums enlargement.
myocardial disease. It is not related to any secondary Ventricular premature complexes were detect- ed (Fig. 1).
disorder such as taurine or L-carnitine deficien- cy Complete blood cell count showed mild elevation of
(7,9,17,18,22,26). The diagnosis of DCM requires an active neutrophil and low levels of tT4 and fT4. Arterial Blood
exclusion of other congenital diseases, acquired cardiac Gas Analysis revealed a low partial pressure of oxygen and
dis- eases, systemic disease, and pulmonary diseases that a partial pressure of carbon dioxide.
might secondarily induce a similar phenotype (6). Thoracic radiographs revealed moderate
Although electrocardiogram (ECG) is essential for the enlargement of the left ventricle, mild bulging of
eval- uation of arrhythmias, the presence of ECG atrium, and moderate alveolar pattern in the right lung
abnormalities has limited value in the diagnosis of DCM lobe and the cranial part of left caudal lung lobe (Fig.
(8). Findings on thoracic radiography for DCM include 2). Two-dimensional echocar- diography showed a
cardiomegaly, often with enlargement of the left atrium, severely dilated left-side heart and a mildly enlarged
various degrees of pul- monary edema, venous right-side heart. The ratio of LA: Ao was 2.45 (reference
congestion, and sometimes ascites and pleural effusion range: <1.3). Color-flow Doppler echocardiogram showed
(8). However, these findings are not spe- cific for DCM (8). eccentric mitral regurgitation during systole (Fig. 3).
Echocardiography is the standard imaging technique for Transventricular time-motion echocardiography showed
the diagnosis of DCM (8). Diagnosing the pres- ence of an enlarged left ventricular wall during both diastole and
specific chamber enlargement and myocardial failure systole (LVIDd: 42 mm, reference range: 20-30 mm;
requires M-mode and two-dimensional (2D) LVIDs: 34 mm, reference range: 11-21 mm). FS (19.9%)
echocardiog- raphy (8). Echocardiographic findings was lower than the normal range (30-50%). Spectral
include increased left ventricular end-diastolic dimension, Doppler recordings revealed a high mitral regurgitation
end-systolic dimension, increased E-point septal separation velocity (5.96 m/s). Early diastolic mitral inflow velocity
(EPSS), and decreased fractional shortening (FS) (8). It has (0.88 m/s) was increased with an E:A ratio of 5.5.
been reported that echo- cardiography is useful for Reduced A-wave velocity (0.16 m/s) and short E-wave
prognostic evaluation of DCM in dogs (4). The restrictive deceleration time (48 ms) were also identified. Tissue
transmitral flow (TMF) pattern cor- relates well with high Doppler imaging (TDI) in LVW showed reversal E`/A` and
filling pressure and poor prognosis of dogs with DCM (4). E peak velocity (5.7 cm/s) (Fig. 4). TDI showed no reversal
DCM usually affects large breed of dogs. It rarely
E`/A` in LVW with E peak velocity of 3.7 cm/s. Tricuspid
affects
regurgita- tion velocity was 3.39 m/s and pulmonary
dogs weighing less than 12-15 kilograms (5,17,26). The
regurgitation was
pur- pose of this report was to describe radiographic
2.37 m/s (Fig. 5).
findings, echocardiographic features, and prognosis of a
Based on radiographic and echocardiographic examina-
small breed of Maltese dog with DCM.
tions, the tentative diagnosis was DCM accompanying
se- vere pulmonary hypertension. The dog was
medicated with pimobendan (0.25 mg/kg orally twice
daily), furosemide (2

Fig. 1. Electrocardiogram of the patient


showing tall and wide P wave with
ventric- ular premature complexes
(arrow).

164 https://doi.org/10.17555/jvc.2021.38.3.163
Imaging Diagnosis of DCM in a Dog

Fig. 2. Dorsoventral (A), right lateral (B), and left lateral (C)
thoracic radiographs of the patient revealing moderate enlargement
of the left ventricle (arrowhead) with mild bulging of the right (white
arrow head) and left (black arrow) atria. Moderate alveolar pattern
(asterisk) in the right lung lobe and cranial part of the left caudal
lung lobe are also de- tected.

mg/kg orally twice daily), ramipril (0.125 mg/kg orally


once daily), and taurine (500 mg/dog orally twice daily).
After 10 days of following-up, the dog had a sudden
death.

Discussion

Idiopathic DCM is commonly found in large and me-


dium sized breed dogs weighing more than 12-15 kilo-
grams (5,9,17,21,26) such as Doberman Pinscher,
Irish Wolfhound, Portuguese water dogs, and
Newfoundland (1,3,5,9,17,18,21,22,26). Small breed
canine patients with DCM are very rare, making it difficult
to determine its etiolo- gy. This is a very rare case of a
small Maltese dog weighting
4.95 kg with DCM.
Clinical signs of DCM include weakness, lethargy, Fig. 3. Echocardiography of the patient. Right parasternal long-axis
tachy- pnea or dyspnea, exercise intolerance, cough, (A, B) and short axis view (C) showing severe dilated left atrium (LA)
and left ventricle (LV). Color-flow Doppler echocardiogram (B)
anorexia, ab- dominal distension, ascites, and syncope
showing ec- centric mitral regurgitation during systole (arrow). The
(9,17,21,22,24,26). However, clinical signs may not be left atrial-aortic root ratio (LA/Ao) was 2.45 (C).
noticed until DCM is pro- gressed (9,17,21,22,24,26). The
present case also had severe cough and tachypnea for a could affect breeds such as Standard schnauzer (13)
month. Auscultation revealed arrhythmia. and Portuguese water dogs, especially Cocker Spaniels
Electrocardiography (ECG) findings for DCM include QRS (3,9,10- 12,14,17,18,20,22,24,26). In addition, DCM may
complex widening, P wave widening and notching, occur if a normal dog is supplied with less taurine and
uniform or multiform ventricular premature complex (VPCs), carnitine. Pro- viding taurine supplementation can
and par- oxysmal ventricular tachycardia (26). In the present improve their survival time (7,10,11). In the present
case, ECG revealed tall and wide P wave and VPCs. case, although the dog was treated with 500 mg taurine
Secondary DCM might be associated with toxic and L-carnitine BID for one day, the dog died suddenly.
change, infectious agents, endocrinopathies, and Hypothyroidism with hypercholesterolemia can occur in
nutritional disor- der (3,5,9,17,18,22,24). Previous
reports have shown that lower levels of taurine and
carnitine (5,9-11,17,18,20,26)
www.ksvc.or.kr 165
Soyon An, et al.

Fig. 4. Transventricular time-motion echocardiogram (A), spectral Doppler (B, C), and tissue Doppler imaging (D) of the patient. Doppler imaging
was taken from the left apical four-chamber view. (A, B) Low shortening fraction (19.9%) and mitral regurgitation velocity (5.96 m/s) were
identified.
(C) Early diastolic mitral inflow velocity (0.88 m/s) was increased with an E:A ratio of 5.5 and a short E-wave deceleration time (48 ms). (D) Tissue
Doppler imaging in LVW showing no reversal E`/A`.

Fig. 5. Continuous wave Doppler echocardiogram. Note tricuspid regurgitation (3.39 m/s) on the left long-axis of a four-chamber view (A) and
pul- monary regurgitation (2.37 m/s) on the left short axis view (B).

some dogs with DCM. However, most dogs with DCM ly low levels of tT4 and fT4. Therefore, it was unclear
have normal thyrotropin stimulating hormone and free T4 whether its DCM was caused by taurine deficiency or
concen- trations (2,9,17,24-26). Note that human is affected hypothyroidism. DCM refers to a myocardial disease
by hyper- thyroidism (27). In the present case, blood test characterized by a cardiac chamber dilation causing
revealed mild- myocardial systolic and
166 https://doi.org/10.17555/jvc.2021.38.3.163
Imaging Diagnosis of DCM in a Dog

diastolic dysfunction, especially in the left side of the


References
heart (3,5,8,9,16-18,21-23,24,26). Previously studies have
reported some methods for diagnosis DCM, such as left- 1. Alroy J, Rush JE, Freeman L, Amarendhra Kumar MS, Karuri
sided or four chamber dilatation and impaired left A, Chase K, et al. Inherited infantile dilated cardiomyopathy in
ventricular systolic func- tion (3,5,8,9,16-18,21-23,24,26). dogs: genetic, clinical, biochemical, and morphologic
Thoracic radiographs can reveal left atrial and left findings. Am J Med Genet 2000; 95: 57-66.
ventricular enlargement (may right atrial and right 2. Beier P, Reese S, Holler PJ, Simak J, Tater G, Wess G. The role
ventricle), pulmonary vein dilation, remark- able of hypothyroidism in the etiology and progression of dilated
pulmonary vasculature, and pulmonary edema due to left car- diomyopathy in Doberman Pinschers. J Vet Intern Med
sided congestive heart failure (21,23). Echocardiography is 2015; 29: 141-149.
the most useful assessment for diagnosing DCM. 2D and 3. Boon JA. Dilated cardiomyopathy. In: Boon JA, editor. Veterinary
M-mode evaluation in echocardiography showed dilated echocardiography. 2nd ed. Chichester: Wiley-Blackwell.
left atrial and ventricle, normal to thin left ventricular wall 2011: 381-395.
and in- traventricular septal, poor FS, and large EPSS. Color 4. Borgarelli M, Santilli RA, Chiavegato D, D'Agnolo G, Zanatta
Doppler evaluation show mitral insufficiency secondary to R, Mannelli A, et al. Prognostic indicators for dogs with dilated
dilation of mitral annulus. Syslitoc dysfunction is significant. car- diomyopathy. J Vet Intern Med 2006; 20: 104-110.
Low aortic velocity is a consequence of reduced cardiac 5. Chetboul V. Canine dilated cardiomyopathy and other
output. DCM may show diastolic dysfunction and cardiomy- opathies. In: de Madron E, Chetboul V, Bussadori C,
increased E wave in mi- tral inflow studies editors. Clini- cal echocardiography of the dog and cat. St. Louis:
(3,5,16,21,23,26). Elsevier. 2016: 181-194.
Many radiographic and echocardiographic studies on 6. Cobb MA. Idiopathic dilated cardiomyopathy: advances in
DCM aeti- ology, pathogenesis and management. J Small Anim Pract
are limited to large breed dogs. The present case shows 1992; 33: 113-118.
typ- ical findings in thoracic radiography and 7. Delaney SJ, Kass PH, Rogers QR, Fascetti AJ. Plasma and
echocardiography such as left-side heart enlargement, whole blood taurine in normal dogs of varying size fed
pulmonary edema, poor FS, high mitral regurgitation, and commercially prepared food. J Anim Physiol Anim Nutr (Berl)
high E peak. 2003; 87: 236- 244.
Restrictive TMF pattern is one of indicators for predicting 8. Dukes-McEwan J, Borgarelli M, Tidholm A, Vollmar AC,
poor prognosis of dogs with DCM. This restrictive pattern Hägg- ström J. Proposed guidelines for the diagnosis of canine
is characterized by a high E-wave velocity, a short E-wave idiopathic dilated cardiomyopathy. J Vet Cardiol 2003; 5: 7-19.
de- celeration time (rapid filling in early diastole), and a 9. Ettinger SJ. Myocardial diseases. In: Ettinger S, Feldman E, Cote
reduced A-wave velocity (minimal filling during atrial E, editors. Textbook of veterinary internal medicine expert
systole) (4). The present patient also showed high E- consult. 8th ed. St. Louis: Elsevier. 2017: 3071-3091.
wave velocity, short E-wave deceleration time, and 10. Fascetti AJ, Reed JR, Rogers QR, Backus RC. Taurine deficiency
reduced A-wave velocity as features of a restrictive TMF in dogs with dilated cardiomyopathy: 12 cases (1997-2001). J
pattern. Thus, its prognosis was expected to be poor. Am Vet Med Assoc 2003; 223: 1137-1141.
Severe DCM can proceed to pulmonary artery 11. Freeman LM, Stern JA, Fries R, Adin DB, Rush JE. Diet-
hyperten- sion secondary to left-sided heart failure (3,9,16- associated dilated cardiomyopathy in dogs: what do we
18,21,24,26). Previous reports have shown that the know? J Am Vet Med Assoc 2018; 253: 1390-1394.
presence of pulmonary hypertension concomitant with 12. Gavaghan BJ, Kittleson MD. Dilated cardiomyopathy in an Amer-
poor right ventricular func- tion is associated with a ican cocker spaniel with taurine deficiency. Aust Vet J 1997;
worse prognosis for both human and dogs with DCM 75: 862-868.
(3,15-18,22,24,26). If symptoms indi- cate congestion 13. Harmon MW, Leach SB, Lamb KE. Dilated cardiomyopathy
heart failure, the prognosis is often poor in standard schnauzers: retrospective study of 15 cases. J Am
(3,9,17,18,21,22,26). This dog also had severe pulmonary Anim Hosp Assoc 2017; 53: 38-44.
hy- pertension with a sudden death. 14. Kittleson MD, Keene B, Pion PD, Loyer CG. Results of the
multi- center spaniel trial (MUST): taurine- and carnitine-
Conclusions responsive di- lated cardiomyopathy in American cocker spaniels
with decreased plasma taurine concentration. J Vet Intern
This case describes echocardiographic diagnosis of a Med 1997; 11: 204-
dilat- ed cardiomyopathy rarely reported in small breed
dogs. We should consider a poor prognosis if restrictive TMF
pattern and pulmonary artery hypertension are found in
dogs with DCM.
www.ksvc.or.kr 167
Soyon An, et al.

211.
BSAVA Manual of canine and feline thoracic imaging.
15. Martin MW, Stafford Johnson MJ, Strehlau G, King JN.
Quedgeley: British Small Animal Veterinary Association. 2008:
Canine dilated cardiomyopathy: a retrospective study of
135-138.
prognostic find- ings in 367 clinical cases. J Small Anim Pract
22. Simpson S, Edwards J, Ferguson-Mignan TF, Cobb M,
2010; 51: 428-436.
Mongan NP, Rutland CS. Genetics of human and canine dilated
16. Mattoon JS. Cardiomyopathy. In: Mattoon J, Nyland T,
cardiomy- opathy. Int J Genomics 2015; 2015: 204823.
editors. Small animal diagnostic ultrasound. 3rd ed. St. Louis:
23. Thrall DE. Cardiomyopathy. In: Thrall D, editor. Textbook of
Elsevier. 2015: 310-311.
veter- inary diagnostic radiology. 7th ed. St. Louis: Elsevier.
17. Nelson RW. Myocardial diseases of the dog. In: Nelson R,
2018: 702- 703.
Couto CG, editors. Small animal internal medicine. 5th ed. St.
24. Tidholm A, Häggström J, Borgarelli M, Tarducci A. Canine
Louis: Else- vier. 2014: 130-144.
idio- pathic dilated cardiomyopathy. Part I. Aetiology, clinical
18. Oyama MA. Canine cardiomyopathy. In: Smith FWK, Tilley
charac- teristics, epidemiology and pathology. Vet J 2001;
LP, Oyama M, Sleeper MM, editors. Manual of canine and
162: 92-107.
feline car- diology. 5th ed. St. Louis: Elsevier. 2016: 139-150.
25. Tidholm A, Häggström J, Hansson K. Effects of dilated
19. Richardson P, McKenna W, Bristow M, Maisch B, Mautner B,
cardio- myopathy on the renin-angiotensin-aldosterone
O’Connell J, et al. Report of the 1995 World Health
system, atrial natriuretic peptide activity, and thyroid hormone
Organization/ International Society and Federation of Cardiology
concentrations in dogs. Am J Vet Res 2001; 62: 961-967.
Task Force on the Definition and Classification of
26. Ware WA. Myocardial diseases of the dog. In: Ware W,
cardiomyopathies. Circulation 1996; 93: 841-842.
editor. Cardiovascular disease in small animal medicine. London:
20. Sanderson SL. Taurine and carnitine in canine
Manson Publishing Ltd. 2007: 280-292.
cardiomyopathy. Vet Clin North Am Small Anim Pract 2006;
27. Watanabe E, Ohsawa H, Noike H, Okamoto K, Tokuyama A,
36: 1325-1343, vii-viii.
Kanai M, et al. Dilated cardiomyopathy associated with
21. Schwarz T. Myocardial diseases. In: Schwarz T, Johnson V,
hyperthyroid- ism. Intern Med 1995; 34: 762-767.
editors.
168 https://doi.org/10.17555/jvc.2021.38.3.163
Case Report Rapport de cas

A case of juvenile form of dilated cardiomyopathy in a 6-month-old


Shiba Inu dog
Koichi Shimizu, Ryohei Suzuki, Yoshitaka Ikeda, Yohei Mochizuki, Takahiro Teshima,
Masaki Michishita, Hirotaka Matsumoto, Hidekazu Koyama

Abstract — A 6-month-old Shiba Inu dog was brought to the Veterinary Medical Teaching Hospital because
of a cough, exercise intolerance, and pulmonary edema. The dog had a Levine 2/6 systolic murmur.
Transthoracic echocardiography revealed left atrial and ventricular dilatation (left atrium to aortic ratio: 2.8),
mitral and tricuspid valve regurgitation, and severe left ventricular myocardial hypokinesia (fractional shortening
was 11.8%). Bubble contrast echocardiography did not reveal a congenital shunt; therefore, the dog was
clinically diagnosed with early onset dilated cardiomyopathy. From the first visit, the dog was treated with
pimobendan, taurine, torasemide, and isosorbide dinitrate. After 435 days, echocardiography revealed that
systolic function had not improved. On Day 465, atrial fibrillation was confirmed via electrocardiogram, and
treatment with diltiazem hydrochloride was initiated. The dog continued to appear clinically stable thereafter,
until it died suddenly 1087 days after the initial visit. A postmortem histopathological examination identified
severe enlargement of the left atrial and ventricular chambers as well as attenuated wavy fibers in the ventricular
myocardium, which confirmed dilated cardiomyopathy in a juvenile. This is the first report of a juvenile form of
dilated cardiomyopathy in a Shiba Inu dog. This case report provides evidence that the extended prognosis of
this dog differed from that in previously reported cases of dilated cardiomyopathy in young dogs.
Key clinical message:
This is the first reported case of a juvenile form of dilated cardiomyopathy in a Shiba Inu dog. This report
provides evidence that the prognosis of this dog differed from that in previously reported cases of dilated
cardiomyopathy in young dogs.

Résumé — Un cas de forme juvénile de cardiomyopathie dilatée chez un chien Shiba Inu de 6 mois. Un
chien Shiba Inu de 6 mois a été amené à l’hôpital universitaire de médecine vétérinaire en raison d’une toux,
d’une intolérance à l’exercice et d’un œdème pulmonaire. Le chien avait un souffle systolique Levine 2/6.
L’échocardiographie transthoracique a révélé une dilatation auriculaire et ventriculaire gauche (rapport
oreillette gauche sur aorte : 2,8), une régurgitation des valves mitrale et tricuspide et une hypokinésie
myocardique ventriculaire gauche sévère (raccourcissement fractionnel de 11,8 %). L’échocardiographie de
contraste par microbulles n’a pas révélé de shunt congénital; par conséquent, le chien a reçu un diagnostic
clinique de cardiomyopathie dilatée d’apparition précoce. Dès la première visite, le chien a été traité avec du
pimobendane, de la taurine, du torasémide et du dinitrate d’isosorbide. Après 435 jours, l’échocardiographie a
révélé que la fonction systolique ne s’était pas améliorée. Au jour 465, la fibrillation auriculaire a été confirmée
par électrocardiogramme et un traitement par le chlorhydrate de diltiazem a été instauré. Le chien a continué à
apparaître cliniquement stable par la suite, jusqu’à ce qu’il meure subitement 1087 jours après la visite initiale.
Un

Veterinary Medical Teaching Hospital, Nippon Veterinary and Life Science University, 1-7-1 Kyonan-cho, Musashino-shi,
Tokyo 184-8602, Japan (Shimizu); Laboratory of Veterinary Internal Medicine, School of Veterinary Medicine, Faculty of Veterinary
Medicine, Nippon Veterinary and Life Science University, 1-7-1 Kyonan-cho, Musashino-shi, Tokyo 184-8602, Japan (Suzuki,
Teshima, Matsumoto, Koyama); Keyaki Animal Hospital. 1-1-48-1F Tsuruse-higashi, Fujimi-shi, Saitama 354-0024, Japan
(Ikeda); Faculty of Veterinary Medicine, Okayama University of Science, 1-3 Ikoinooka, Imabari-shi, Ehime 794-8555, Japan
(Mochizuki); Laboratory of Veterinary Pathology, School of Veterinary Medicine, Faculty of Veterinary Medicine, Nippon
Veterinary and Life Science University, 1-7-1 Kyonan-cho, Musashino-shi, Tokyo 184-8602, Japan (Michishita).
Address all correspondence to Dr. Ryohei Suzuki; email: ryoheisuzuki0130@gmail.com
Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the
CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.
152 CVJ / VOL 63 / FEBRUARY 2022
examen histopathologique post mortem a identifié une hypertrophie sévère des cavités auriculaire et
ventriculaire gauche ainsi que des fibres ondulées atténuées dans le myocarde ventriculaire, ce qui a confirmé
une cardiomyopathie dilatée chez un juvénile. Il s’agit du premier rapport d’une forme juvénile de
cardiomyopathie dilatée chez un chien Shiba Inu. Ce rapport de cas fournit des preuves que le pronostic
prolongé de ce chien différait de celui des cas précédemment rapportés de cardiomyopathie dilatée chez les
jeunes chiens.
Message clinique clé :
Il s’agit du premier cas rapporté d’une forme juvénile de cardiomyopathie dilatée chez un chien Shiba Inu. Ce
rapport fournit des preuves que le pronostic de ce chien différait de celui des cas précédemment rapportés de
cardiomyopathie dilatée chez les jeunes chiens.

beats/min) and widening of


Can Vet J 2022;63:152–156

D ilated cardiomyopathy (DCM) is a major myocardial


dis- ease, characterized by cardiac chamber enlargement and
severe systolic dysfunction (1,2). Several reports have shown
that DCM mainly affects large-breed dogs, such as the
Doberman pinscher, Great Dane, Irish wolfhound, and
Scottish deerhound. The common age at diagnosis is 6 to 8 y
(1); however, some dogs develop DCM as juveniles and die
within a few months. Thus far, the juvenile form of dilated
cardiomyopathy has been reported in only 3 breeds:
Doberman pinscher, Portuguese water dog, and toy
Manchester terrier (3–6). No definitive diagnosis has
previously been reported in Shiba Inu dogs, and the clinical
course of early-onset DCM has not been described in detail. In
the present case, we report clinical findings of DCM,
pathologically confirmed by a postmortem examination, in a
juvenile Shiba Inu dog.

Case description
A 6-month-old intact, 6.2 kg, female Shiba Inu dog was
brought to the Veterinary Medical Teaching Hospital of
Nippon Veterinary and Life Science University.
At the referring hospital, the dog exhibited a cough and
exer- cise intolerance. Left-sided heart failure was suspected
because of pulmonary edema on thoracic radiography and
cardiac dila- tation on echography. Therefore, pimobendan
(Pimobe Heart; Kyoritsu Seiyaku, Tokyo, Japan), 0.2 mg/kg
body weight (BW), PO, q12h and torasemide (Luprac;
Mitsubishi Tanabe Pharma., Osaka, Japan), 0.16 mg/kg BW,
PO, q12h were administered to treat the left-sided congestive
heart failure.
Upon initial visit to our hospital (Day 1), physical
examina- tion revealed a heart rate (HR) of 127 bpm and a
Levine 2/6 systolic murmur at the left parasternal region. The
systolic, diastolic, and mean blood pressure (BP) measured
via the oscillometric method (BP 100 DII; Fukuda M-E,
Tokyo, Japan) were 136 mmHg [reference range (RR):
121 to 139 mmHg], 57 mmHg (RR: 67 to 71 mmHg), and 81
mmHg (RR: 88 to 92 mmHg), respectively (7). The complete
blood (cell) count was within the normal range. Serum
biochemical analysis indicated hyperglycemia (162 mg/dL)
and hypokale- mia (3.1 mmol/L). Other measurements,
including thyroxin concentration (3.21 mg/dL), were within
reference ranges. Electrocardiography revealed a sinus
rhythm with ventricu- lar premature complexes (14
(Traduit par Dr Serge Messier) (10). The left ventricular end diastolic volume, end systolic
volume, and ejection fraction, measured by single plane
method of disks using apical 4-chamber view, were 42 mL, 31
mL, and 27% (ref- erence value: 66.5 6 6.4%), respectively
(11). With body sur- face area normalized, the end diastolic
the P wave duration (50 ms) (Figure 1). Thoracic radiogra- volume and end systolic volume were 124 mL/m2 (reference
value: 47.6 6 8.4 mL/m2)

ORT
CAS E R E P
phy in the dorsoventral and right lateral position showed an
enlarged left atrium and ventricle. The vertebral heart size and 90 mL/m2 (reference value: 15.9 6 3.9 mL/m2), respec-
was enlarged (10.5 v) (8). Although cranial pulmonary tively (11). Sphericity index of the left ventricle at diastole
venous enlargement was shown, pulmonary edema was not and systole were 1.2 and 1.1 (reference value: . 1.65),
observed (Figure 2). A 2-dimensional transthoracic and respec- tively (12). E-point to septal separation of the mitral
Doppler echocar- diographic study was performed using Vivid valve leaflet was 14 mm (reference value: , 6.5 mm) (12).
7 echocardiographic equipment (GE Healthcare, Tokyo, Transmitral E and A wave velocities were 0.9 m/s (RR: 0.58
to 1.17 m/s) and
Japan). The left atrium was enlarged, and the left atrium-to-
0.4 m/s (RR: 0.39 to 0.86 m/s), respectively (13). The aortic
aortic root diameter ratio was
velocity was 1.2 m/s (RR: 0.92 to 1.88 m/s) (13). These
2.8 (RR: 0.69 to 1.27) (9). The end diastolic left ventricular
exami- nations confirmed that the systolic function of the left
dimension (LVDd), end systolic left ventricular dimension
ventricle was decreased. This was accompanied by thinning
(LVDs), end diastolic interventricular septum thickness, and
of the left ventricular wall and dilation of the left ventricle.
end diastolic left ventricular posterior wall thickness
There was no degeneration or prolapse of the mitral and
were
tricuspid valve leaf- lets, but color flow Doppler showed a
42.3 mm (RR: 22.0 to 31.0 mm), 37.3 mm (RR: 12.0 to
central jet signal of mild mitral and tricuspid valve
22.0 mm), 4.8 mm (RR: 4.0 to 9.0 mm), and 4.1 mm (RR: 4.0
regurgitation. A contrast-enhanced echocardiogram with a
to 9.0 mm), respectively, and fractional shortening (FS) was
microbubble test was performed to care- fully evaluate the
11.8% (RR: 25.3 to 49.9%) (Figure 3) (9,10). With body
presence of congenital shunts. Based on these findings, the
weight normalized, the end diastolic left ventricular interior
dog was clinically diagnosed with DCM.
dimension (LVIDDN) was 2.5 (reference value: , 1.7)

CVJ / VOL 63 / FEBRUARY 2022 153


Figure 1. Electrocardiography in lead II shows a heart
rate of 157 bpm and multifocal ventricular premature
complexes (14 bpm) which is a wide QRS wave without
a P wave and occur prematurely compared to the
underlying
rhythm. Also, the P wave is wide. The variation in R-R interval
is associated with the breathing movements (respiratory sinus
arrhythmia). Therefore, a respiratory sinus arrhythmia with
multifocal ventricular premature complexes was diagnosed.
Paper speed = 50 mm/s; Gain = 5 mm/mV.

On Day 1, the dog was treated with oral pimobendan Reportedly, the dog was not brought to the referral animal
(Pimobe Heart; Kyoritsu Seiyaku, Tokyo, Japan), 0.2 mg/kg hospital with clinical
BW, PO, q12h; sustained release isosorbide dinitrate (Nitrol
R capsule; Eisai, Tokyo, Japan), 1 mg/kg BW, PO, q12h;
taurine (Taurine powder 98% “Taisho”; Taisho Pharma.,
Tokyo, Japan), 500 mg/head, PO, q12h; and torasemide
(Luprac; Mitsubishi Tanabe Pharma., Osaka, Japan), 0.15
mg/kg BW, PO, q12h. On Day 34, although
echocardiography revealed no improve- ment in FS
(11.9%), LVDd (45.7 mm), LVIDDN (2.55),
and LVDs (40.3 mm), the dog showed an improved exercise
tolerance; HR was 116 bpm. On Day 74, coughing ceased,
and exercise intolerance symptoms were not seen.
Radiography revealed no pulmonary edema, pleural effusion,
or ascites. The left atrium-to-aortic root diameter ratio
decreased to 2.5. However, the ventricular premature
complexes increased to 30 bpm. The FS value had slightly
decreased, as well as the HR, LVDd, LVIDDN, and LVDs,
which were 103 bpm, 44.7 mm, 2.52, and 41.6 mm,
respectively.
The prescribed dose of pimobendane, therefore, was
increased to 0.36 mg/kg, and carvedilol (Artist; Daiichi
Sankyo, Tokyo, Japan), 0.05 mg/kg BW, PO, q12h was
added to the treatment regimen. On Day 159, the dog showed
no clinical signs, such as dyspnea, cough, syncope, or
exercise intolerance, and body weight increased to 7.4 kg,
despite the presence of 12% FS. There was no accumulation
of ascites or pleural effusion, and the body condition score
was 5/9 (14), which was the same as at Day 1. On Day 465,
the dog collapsed suddenly while walking.
Electrocardiography results revealed atrial fibrillation, and
diltiazem hydrochloride (Hemarekeat; Tsuruhara Pharma.,
Osaka, Japan), 1 mg/kg BW, PO, q8h was prescribed. On
Day 502, echocardiography revealed an FS of 14.1%.
Although the dog showed no clinical signs, LVDd, LVIDDN,
and LVDs were 53.9 mm, 2.95, and 46.3 mm, respectively,
and the left ventricular dimensions had worsened. The dog was
subsequently followed up by the referring veterinarian.
and congenital aortic and/or mitral dysplasia were identified.
The thicknesses of the right ventricular wall, ventricular sep-
tum, and left ventricular free wall were 8.0, 8.0, and 6.0 mm,
respectively, and dilation of the left ventricle chamber was
severe.
RAP P ORT DE CAS

Figure 2. Dorsoventral (A) and right lateral radiograph (B)


taken on Day 1. Although obvious pulmonary edema was not
seen, left atrial and left ventricular enlargement as well as cranial
pulmonary venous enlargement were shown. The figure also
revealed an increased vertebral heart size (10.5 v; standard
value: 9.8 6 0.45 v).

signs of heart failure, and cardiac examinations were not


per- formed at the referring practice. The dog was prescribed
diltia- zem hydrochloride, pimobendan, and torasemide.
However, on Day 1087, the dog died suddenly.
Necropsy revealed a heart weight-to-body weight ratio of
13.51 g/kg (RR: 5.8 to 9.4 g/kg) (15). No congenital shunts

154 CVJ / VOL 63 / FEBRUARY 2022


Figure 3. Right parasternal short-axis view (A — Diastolic phase, B —
Systolic phase) on Day 1. Images reveal an end diastolic left ventricular
dimension of
42.3 mm, an end diastolic interventricular septum dimension of 4.8 mm, and
an end diastolic left ventricular posterior wall thickness of 4.1 mm, as well as
fractional shortening of 11.8%.

Histologically, myocardial fibers had an atrophied, euthanized at 11 wk of age due to a decrease in FS (4). A
attenuated, and wavy appearance. Furthermore, vacuolar study showed that Portuguese
degeneration of cardiomyocytes, fatty infiltration, growth of
collagen, and mild to moderate edema were also apparent
(Figure 4).

Discussion
Dilated cardiomyopathy is a myocardial disease,
characterized by cardiac chamber enlargement, ventricular
wall thinning, and decreased contractile function (1,2).
Canine DCM mainly affects large-breed dogs and the
common age at diagnosis is 6 to 8 y (1). In addition,
parvovirus infection, which may cause sudden death or death
within a few weeks with gastroenteri- tis, leukopenia,
dehydration, and lethargy, may cause cardiac enlargement in
young dogs (16,17).
In this case, the 6-month-old dog was referred to our
hospital for evaluation of a cough and exercise intolerance.
Echocardiography showed left atrial dilation, left ventricular
dilation, and contractile dysfunction. Shunting of blood flow,
and hypothyroidism that may cause pathologies similar to
DCM were not observed. Parvoviral infection was eliminated
as a diagnosis based on the clinical history, clinical
presentation, and laboratory findings. The dog was fed a
general commercial diet consisting of appropriate calories.
Oral taurine administration did not improve left ventricular
contraction; therefore, the clini- cal diagnosis of early-onset
idiopathic DCM was established, and the dog was treated
medically. In accordance with the his- topathological findings
at necropsy, the diagnosis was confirmed as a juvenile form of
DCM (18).
Dilated cardiomyopathy with early onset of heart failure,
reported as juvenile DCM, has only been observed 3 dog breeds:
Doberman pinscher, Portuguese water dog, and toy
Manchester terrier (3–6). Furthermore, most juvenile dogs
with DCM die suddenly without any signs of heart disease or
die within a few days due to refractory congestive heart
failure (3–6). In a report of Doberman pinschers, 2/6 dogs
diagnosed with DCM died of acute pulmonary edema at 10
and 19 d of age, 3 were euthanized at 4 wk of age due to the
advanced progression of congestive heart failure, and 1 was
water dogs died suddenly between the ages of 2 and 32 wk
after birth or died within 5 d of showing acute left-sided heart
failure and no response to medical treatment (5). A report
describes that toy Manchester terriers with DCM died
suddenly between 10 and 58.3 wk of age (6).

ORT
CAS E R E P
In our case, the clinical course was different from those in
previous reports, and the dog survived longer; the treatment
included oral pimobendan from Day 1. The dose was
increased from 0.2 to 0.36 mg/kg after exercise intolerance
recurred. Despite no improvement in echocardiographic
findings, clinical signs, such as exercise intolerance, improved
and the dog herein survived until the age of 3 y. A previous
report suggested that the administration of pimobendan
improved the prognosis of a Doberman pinscher with DCM
(19).
Figure 4. Histological image of the left ventricular
myocardium (hematoxylin and eosin staining, 2003) showing
Genetic predisposition to juvenile DCM has been
attenuated and wavy myocardial fibers with atrophy and reported (3,5). Segregation analysis demonstrated that DCM
thinning. In addition, stromal edema is evident. Bar = 100 in juvenile Portuguese water dogs is an autosomal recessive
mm.
disorder (3,5); therefore, a similar gene mutation may exist in
Shiba Inu dogs. However, the dog reported in this case could

CVJ / VOL 63 / FEBRUARY 2022 155


not be followed up for familial information; therefore, we 8. Sleeper MM, Buchanan JW. Vertebral scale system to measure heart size
could not ascertain an inherited predisposition. The in growing puppies. J Am Vet Med Assoc 2001;219:57–59.
accumulation of familial and genetic factors and drug 9. Donald JB, John ER, John MG, James NR JR, Barbara B, William
MR. M-mode echocardiographic ratio indices in normal dogs, cats,
responsivity data is neces- sary to assess the cause and and horses: A novel quantitative method. J Vet Intern Med 2003;17:
prognosis of a juvenile form of DCM in Shiba Inu dogs. To 653–662.
achieve this, surveys and description of similar cases and 10. Cornell CC, Kittleson MD, Torre PD, et al. Allometric scaling of
RAP P ORT DE CAS

m-mode cardiac measurements in normal adult dogs. J Vet Intern


their families are required. Med 2004;18:311–321.
This report describes a juvenile case of DCM in a 6- 11. Serres F, Chetboul V, Tissier R, et al. Comparison of 3 ultrasound
month- old Shiba Inu dog, which had a different clinical meth- ods for quantifying left ventricular systolic function:
Correlation with disease severity and prognostic value in dogs with
course than that previously reported in cases of DCM in mitral valve disease. J Vet Intern Med 2008;22:566–577.
young dogs. 12. Holler PJ, Wess G. Sphericity index and E-point-to-septal-separation
(EPSS) to diagnose dilated cardiomyopathy in Doberman Pinschers.
Acknowledgment J Vet Intern Med 2014;28:123–129.
13. Chetboul V, Sampedrano CC, Concordet D, et al. Use of quantitative
We thank Editage (www.editage.com) for English language two-dimensional color tissue doppler imaging for assessment of left
editing. CVJ ventricular radial and longitudinal myocardial velocities in dogs. Am
J Vet Res 2005;66:953–961.
14. Chu JL, Bang HT, Ji SY, et al. A simple method to evaluate body
References con- dition score to maintain the optimal body weight in dogs. J
1. Oyama MA. Canine cardiomyopathy. In: Smith FWK Jr, ed. Manual Anim Sci Technol 2019;61:366–370.
of Canine and Feline Cardiology. 5th ed. St. Louis, Missouri: 15. Turk JR, Root CR. Necropsy of the canine heart: A simple technique
Elsevier, 2015:141–151. for quantifying ventricular hypertrophy and valvular alterations. Comp
2. Guglielmini C. Cardiovascular diseases in the ageing dog: Cont Ed Pract Vet 1983;5:905–906.
Diagnostic and therapeutic problems. V Res Commun 2003;27:555– 16. Carpenter JL, Roberts RM, Harpster NK, King NW, Jr. Intestinal and
560. cardiopulmonary forms of parvovirus infection in a litter of pups. J
3. Sleeper MM, Henthorn PS, Vijayasarathy C, et al. Dilated cardiomy- Am Vet Med Assoc 1980;176:1269–1273.
opathy in juvenile Portuguese Water Dogs. J Vet Intern Med 17. Liu SK. Myocarditis and cardiomyopathy in the dog and cat. Heart
2002;16: 52–56. Vessels 1985;1:122–126.
4. Vollmar A, Fox PR, Meurs KM, Liu SK. Dilated cardiomyopathy in 18. Tidholm A, Häggström J, Jönsson L. Prevalence of attenuated wavy
juvenile doberman pinschers. J Vet Cardiol 2003;5:23–27. fibers in myocardium of dogs with dilated cardiomyopathy. J Am
5. Dambach DM, Lannon A, Sleeper MM, Buchanan J. Familial dilated Vet Med Assoc 1998;212:1732–1734.
cardiomyopathy of young Portuguese water dogs. J Vet Intern Med 19. Fuentes VL, Corcoran B, French A, Schober KE, Kleemann R, Justus C.
1999;13:65–71. A double-blind, randomized, placebo-controlled study of
6. Legge CH, López A, Hanna P, Côté E, Hare E, Martinson SA. Histo- pimobendan in dogs with dilated cardiomyopathy. J Vet Intern Med
logical characterization of dilated cardiomyopathy in the juvenile toy 2002;16: 255–261.
Manchester terrier. Vet Pathol 2013;50:1043–1052.
7. Koyama H, Fukushima R, Yoshii Y, et al. Measurement of blood
pressure using a new automatic-system of sphygmomanometer in dogs.
Advances in Animal Cardiology 2002;35:41–47.
156 CVJ / VOL 63 / FEBRUARY 2022
veterinary
sciences

Case Report

A Case of a Small-Breed Dog with Diet-Related Dilated


Cardiomyopathy Showing Marked Improvements in Cardiac
Morphology and Function after Dietary Modification
Takahiro Saito, Ryohei Suzuki * , Yunosuke Yuchi , Yuyo Yasumura , Takahiro Teshima
, Hirotaka Matsumoto and Hidekazu Koyama

Laboratory of Veterinary Internal Medicine, School of Veterinary Science, Faculty of Veterinary Medicine,
Nippon Veterinary and Life Science University, Tokyo 180-8602, Japan
* Correspondence: ryoheisuzuki@nvlu.ac.jp; Tel.: +81-422-31-4151 (ext. 3435)

Simple Summary: Dilated cardiomyopathy is a cardiac disorder most commonly observed in specific
dog breeds and is characterized by diffuse left ventricular systolic dysfunction and left ventricular
enlargement. Recent studies have reported a potential connection between diet and dilated car-
diomyopathy, and some studies have shown a positive effect of diet change on cardiac function
and prognosis in dogs with diet-related dilated cardiomyopathy. However, these reports were
from large-breed dogs and did not include detailed assessments of myocardial function, such as
two-dimensional speckle-tracking echocardiography. We report an overview of our experience in
a small-breed dog with a clinical diagnosis of dilated cardiomyopathy, in which dietary
modification resulted in improved cardiac enlargement and myocardial dysfunction evaluated by two-
dimensional speckle-tracking echocardiography. We suggest that it is necessary to suspect a
Citation: Saito, T.; Suzuki, R.; dietary association with dilated cardiomyopathy, even in small-breed dogs. Furthermore, the
Yuchi, Y.; Yasumura, Y.; Teshima, prognosis for diet-related dilated cardiomyopathy in small-breed dogs may also be as good as in
T.; Matsumoto, H.; Koyama, H. A previous reports of large-breed dogs when changing to appropriate diets.
Case of a Small-Breed Dog with
Diet- Related Dilated Abstract: An 11-year-old intact female Papillion weighing 2.1 kg was referred to our institution
Cardiomyopathy Showing Marked with the main complaint of shallow, rapid breathing. At the first visit (day 0), although clinical
Improvements in Cardiac signs improved due to the use of medication from the primary hospital, transthoracic radiography
Morphology and Function after and echocardiography revealed left heart enlargement and left ventricular dysfunction. A clinical
Dietary Modification. Vet. Sci.
diagnosis of dilated cardiomyopathy (DCM) was made and oral administration of pimobendan,
2022, 9, 593. https://doi.org/
temocapril, and taurine was initiated. However, on day 10, the respiratory status worsened and
10.3390/vetsci9110593
furosemide was prescribed. On day 54, no significant improvement in heart size was observed.
Academic Editor: Patrick Butaye Additionally, the diet that this patient received met the recommendation for diet-related DCM by
the U.S. Food and Drug Administration, and the patient’s diet was changed from a grain-free diet
Received: 30 August 2022
to a grain-containing diet. On day 1191, the patient’s respiratory status was stable and no clinical
Accepted: 26 October 2022
signs were observed. Transthoracic radiography and echocardiography revealed an improvement in
Published: 27 October 2022
left heart size. Additionally, improvements in the left and right ventricular myocardial strains
Publisher’s Note: MDPI stays neutral were observed after changing the diet. We suggest that it may be necessary to suspect a dietary
with regard to jurisdictional claims in
association with dilated cardiomyopathy, and a good prognosis might be expected by dietary
published maps and institutional affil-
modification, even in small-breed dogs.
iations.

Keywords: grain; myocardial function; strain; two-dimensional speckle-tracking echocardiography

Copyright: © 2022 by the authors.


Licensee MDPI, Basel, Switzerland.
1. Introduction
This article is an open access article
distributed under the terms and Dilated cardiomyopathy (DCM) is a cardiac disorder most commonly observed in
conditions of the Creative Commons specific dog breeds and is characterized by diffuse left ventricular (LV) systolic dysfunc-
Attribution (CC BY) license (https:// tion and LV enlargement [1]. Genetic background is suspected to be the etiology of the
creativecommons.org/licenses/by/
4.0/).

Vet. Sci. 2022, 9, 593. https://doi.org/10.3390/vetsci9110593 https://www.mdpi.com/journal/vetsci


Vet. Sci. 2022, 9, 593 2 of 9

disease, but other outbreaks due to nutrient deficiencies [2,3] and concurrent diseases,
such as endocrinopathies [4], myocarditis [5], and chronic tachycardia [6], have also been
reported. In 2018, the United States Food and Drug Administration released a report on the
potential association between diet and DCM. Although a relationship between nutrients
and cardiomyopathy has been reported, there have been recent reports of improved cardiac
function in dogs with DCM due to dietary changes [7]. However, most of the dogs in these
reports were large-breed dogs, and there are few reports on small-breed dogs [8], which
account for a large proportion of dogs in Japan. We report an overview of our experience
in a small-breed dog with DCM-like pathology, in which a change in diet significantly
im-proved cardiac morphology and function.

2. Case Presentation
An 11-year-old intact female Papillion weighing 2.1 kg was examined in the primary
hospital with the main complaint of shallow, rapid breathing. At that time, there was no
heart murmur; however, a radiographic examination revealed an enlarged heart and an
area of increased radiographic opacity in the posterior lobe of the right lung. Echocardiog-
raphy revealed mitral regurgitation (MR). After treatment with furosemide (1.5 mg/kg),
prednisolone (1.0 mg/kg), and enrofloxacin (5.0 mg/kg), dyspnea and increased lung field
opacity on transthoracic radiography improved, but the patient came to our institution for
a thorough examination. At the first visit (day 0), clinical signs improved and respiratory
status was stable. Auscultation revealed a systolic murmur (Levine II/VI), but electro-
cardiography and noninvasive blood pressure measurements (systolic blood pressure,
139 mmHg) were normal. Transthoracic radiography revealed a slightly increased opacity
in the lung field. The vertebral heart size (VHS) was 13.2 vertebrae, indicating cardiac
enlargement (Figure 1). Conventional 2D and Doppler examinations were performed
using Vivid 7 or Vivid E95 Ultra Edition echocardiographic systems (GE Healthcare) with a
transducer of 3.5–6.9 MHz. The dog was manually restrained in the right and left lateral
recumbent positions without sedation. The results of the echocardiographic measurement
are summarized in Table 1. Echocardiography revealed MR and reduced regurgitation
velocity, left atrial and LV enlargement, LV wall thinning, and reduced LV contractility.
Transmitral early diastolic and late diastolic wave velocities (E and A, respectively) showed
a restrictive pattern. The aortic blood velocity showed a high pre-ejection period to ejection
time ratio (PEP/ET). Based on these findings, we suspected DCM and made a clinical
diagnosis using a previously reported DCM diagnostic scoring system [1]. In this scoring
system, a score of 3 points is given for matching one major criterion and 1 point for match-
ing one minor criterion, with a total score of ≥6 points indicating a strong suspicion of
DCM. The major criteria were defined as follows: systolic or diastolic LV dilatation, de-
creased sphericity index (≤1.65), and decreased fractional shortening (FS) (≤20–25%). The
minor criteria were defined as follows: ventricular arrhythmia, atrial fibrillation, increased
E-point-to-septal-separation (EPSS) (≥8.0 mm), increased PEP/ET (>0.4), mildly decreased
FS (Figure 2), and enlargement of left atrial or biatrial enlargement. The LV end-diastolic
volume index (EDVI) and LV end-systolic volume index (ESVI) measured by the modified
Simpson method increased, indicating enlargement of the left ventricle. Furthermore, the
ejection fraction (EF) decreased in the modified Simpson method. The LV sphericity index
was low, indicating that the ventricle was more spherical than normal. The EPSS was within
the reference range but close to the upper limit. Based on the above, three major criteria and
two minor criteria were applicable in this case, with a total score of 11 points, suggesting
a strong suspicion of DCM. Cardiac troponin I (cTnI) was measured and showed a high
value of 1.105 ng/mL (normal range, 0.000–0.129 ng/mL). Therefore, a clinical diagnosis
of DCM was made, and pimobendan (0.3 mg/kg BID), temocapril (0.1 mg/kg BID), and
taurine (250 mg/head BID) were administered orally. However, on day 10, the respiratory
status worsened and furosemide (2.0 mg/kg BID) was also prescribed.
Vet. Sci. 2022, 9, 593 3 of 9

Figure 1. Changes in transthoracic radiography on day 0, day 54 and day 1191. Left figures represent
the dorsoventral views, and right figures represent right lateral views.

Figure 2. Changes in left ventricular internal diameter on day 0 and day 1191.
Vet. Sci. 2022, 9, 593 4 of 9

Table 1. Changes in conventional 2D and Doppler examinations on day 0 and day 1191.

Variables Day 0 Day 1191


LVIDd (mm) 28.6 23.2
LVIDdN (cm/kg0.294) 2.3 1.8
LVIDs (mm) 23.2 15.1
LVIDsN (cm/kg0.294) 1.9 1.2
FS (%) 18.8 35.1
LA/Ao 2.4 1.3
E (m/s) 1.2 0.6
A (m/s) 0.3 0.9
E/A 4.1 0.7
PEP/ET 0.5 0.2
MR velocity (m/s) 4.6 5.9
EDVI (mL/m2) 108 36.6
ESVI (mL/m2) 75 19.6
Sphericity index 1.1 1.7
EPSS (mm) 0.7 0.3
EF (%) 30.5 46.3
LV, left ventricular; LVIDd, end-diastolic LV internal diameter; LVIDdN, LVIDd normalized by body weight;
LVIDs, end-systolic LV internal diameter; LVIDsN, LVIDs normalized by body weight; FS, fractional
shortening; LA/Ao, left atrial-to-aortic ratio; E/A, peak velocity of the early diastolic wave-to-peak velocity of the
late diastolic wave ratio; PEP/ET, pre-ejection period to ejection time ratio; MR, mitral regurgitation; EDVI, LV
end-diastolic volume index; ESVI, LV end-systolic volume index; EPSS, E-point-to-septal-separation; EF,
ejection fraction.

On day 54, respiratory status improved, but radiographic examination in the primary
hospital did not show a significant change in VHS (12.7 vertebrae). At that time, the diet 110
that the patient received met the criteria associated with diet-related DCM according to the
U.S. Food and Drug Administration [7], and the patient’s diet was changed from a grain-free
diet to a grain-containing diet. Ingredients in the product before the diet change mainly in-
cluded: cured venison meat, venison meal, tapioca, peas, pea flour, lentils, chickpeas, canola
oil, dried chicory root, dried rosemary, sodium chloride, potassium chloride, choline chlo-
ride, vitamins (vitamin A, vitamin D3, vitamin E, inositol, niacin, L Vitamin A, vitamin D3,
vitamin E, inositol, niacin, L-ascorbic acid-2-polyphosphate, calcium d-pantothenate, thi-
amine nitrate, beta-carotene, riboflavin, pyridoxine hydrochloride, folic acid, biotin, and
vitamin B12), minerals (zinc, copper, zinc oxide, manganese, copper sulfate, ferrous sulfate,
calcium iodate, manganese oxide, and selenium yeast), DL-methionine, and L-lysine. On
the other hand, the ingredients of the products after the diet change mainly included the
following: rice, animal fats, corn, soy protein, beet pulp, soybean oil, wheat flour, veg-
etable fiber, fish oil, fructo-oligosaccharide, marigold extract, amino acids (DL-methionine,
L-lysine, taurine, and L-carnitine), minerals (Ca, K, Cl, P, Na, Fe, Se, Zn, Mn, Mg, and I),
vitamins (choline, vitamin E, vitamin C, Biotin, vitamin A, calcium pantothenate, niacin,
vitamin B6, vitamin B12, vitamin B1, vitamin B2, vitamin D3, folic acid, and vitamin K3),
preservative (potassium sorbate), and antioxidants (mixed tocopherol). No legumes were
included in the products after the dietary change.
Subsequently, the patient was followed-up at the primary hospital. Approximately
3 years later, on day 1191, the patient was examined at our institution again. During
this period, visits to our institution were difficult because the owner’s address was far
away. The respiratory status was stable, and no clinical signs were observed.
Additionally, there were no changes in oral medications (pimobendane [0.3 mg/kg BID],
temocapril [0.1 mg/kg BID], taurine [250 mg/head BID] and furosemide [2.0 mg/kg BID])
since day 10. Physical examination, blood pressure measurements, and electrocardiogram
did not show significant changes, but there was a marked improvement in the cTnI level to
0.003 ng/mL. On radiographic examination, there were no obvious abnormalities in the
lung fields, and the VHS was markedly reduced to 9.2 vertebrae (Figure 1).
Echocardiography revealed marked improvements in the LV and left atrial diameters
and LV functional indicators (Table 1). The DCM diagnostic score for this patient did not
meet any criteria, resulting
Vet. Sci. 2022, 9, 593 5 of 9

in a total score of 0, which was below the diagnostic criteria for DCM. As improvement
in cardiac function was observed after diet change, a clinical diagnosis of diet-related
DCM was made, and the patient continued on a grain-containing diet. Regarding oral
medications, furosemide and taurine were discontinued, while temocapril and pimobendan
were continued in the same doses. The patient remained stable for 1262 days, with no
recurrence of heart failure.
We then reviewed the case and performed myocardial motion analysis using two-
dimensional speckle-tracking echocardiography (2D-STE). We measured the peak
global strains in the longitudinal and circumferential directions (SL and SC,
respectively) and the systolic strain rates in the longitudinal and circumferential
directions (SrL and SrC, respectively). SL and SrL were measured in the LV and right
ventricle (RV) using the left apical four-chamber view. SC and SrC were measured using the
right parasternal short-axis view at the level of the papillary muscle. The mean values of
the measurements for three consecutive cardiac cycles were used in these 2D-STE
variables. We also measured torsion and torsion rate. For torsional deformations, a right
parasternal short-axis view of the LV was used with recordings made at both the basal
and apical imaging planes. For torsion results, representative values were used instead
of continuous heartbeats. The observer variability of 2D-STE analysis in our laboratory
has previously been described [9–14]. The reference range was based on previous
reports [12,14–22]. On day 0, the SL and SC measured in the LV and RV were below
the reported reference range for each of the parameters. SrL measured in the LV and RV
was lower than each of the reference range. SrC was lower than the reference range.
Torsion and torsion rate were lower than the reference range as well. On day 1191,
these values showed improvement. In particular, substantial increases were observed in
RV-SL, RV-SrL, torsion, and torsion rate (Table 2 and Figure 3).

Figure 3. Changes in left ventricular longitudinal strain on day 0 and day 1191.
Vet. Sci. 2022, 9, 593 6 of 9

Table 2. Changes in conventional 2D-STE examinations on day 0 and day 1191.

Variables Day 0 Day 1191 Healthy Dogs [12,14,15]


LV-SL (%) −11.6 −13.9 −14.9 ± 4.7
LV-SC (%) −11.7 −13.1 −17.6 ± 2.5
RV-SL (%) −13.5 −18.6 −26.9 ± 7.8
Systolic LV-SrL (s−1) −1.1 −2.0 −1.9 ± 0.4
Systolic LV-SrC (s−1) −0.9 −2.0 −2.1 ± 0.5
Systolic RV-SrL (s−1) −1.2 −3.6 −4.2 ± 1.5
Systolic basal rotation (◦) −2.3 −3.7 −3.3 ± 3.4
Systolic basal rotation rate (◦/s) −55.6 −78.0 −119.9 ± 44.4
Systolic apical rotation (◦) 4.8 10.7 12.9 ± 6.0
Systolic apical rotation rate (◦/s) 65.7 89.8 181.4 ± 65.1
Systolic torsion (◦) 5.1 11.7 13.6 ± 5.8
Systolic torsion rate (◦/s) 74.6 136.8 154.7 ± 61.2
Data are expressed as mean ± standard deviation. LV, left ventricular; SL, peak global strain in the
longitudinal direction; SC, peak global strain in the circumferential direction; RV, right ventricular; SrL, strain
rate in the longitudinal direction; SrC, strain rate in the circumferential direction.

3. Discussion
This patient was clinically diagnosed with DCM based on the clinical course and
scoring system [1]. The patient was treated with recommended medication for DCM,
such as pimobendan, angiotensin-converting enzyme inhibitor, and taurine; however,
no significant changes in cardiac size were observed. In contrast, a change to a grain-
containing diet resulted in significant improvement. These improvements were also
evident in the analysis of conventional echocardiography and precise myocardial
function assessed by 2D-STE [11,12,14]. Previous studies that analyzed the
composition of grain-free diets showed low levels of taurine and B vitamins, which are
components of carnitine, and high levels of compounds that inhibit carnitine
metabolism. Peas were also mentioned as the materials most associated with their
composition [23]. The diet that this patient had eaten until day 54 was a grain-free diet
consisting mainly of venison and legumes such as peas. Therefore, it is possible that this
case also had diet-related DCM, in which the grain-free diet induced a DCM-like
pathology.
The extensive and multidirectional myocardial dysfunction was observed on day 0
through 2D-STE analysis. The 2D-STE variables in this case were worse compared with
those in the previous study of Great Danes with idiopathic DCM [19], suggesting that the
diet-related DCM may have the remarkable myocardial dysfunction. In this case, dietary
modification caused improvement in myocardial dysfunction which did not improve
with conventional medical therapy. In particular, torsional motion and RV myocardial
deformation indicators, the precise myocardial performance indicator [9,10,15,24], showed
the substantial improvement. These results suggest that assessment of myocardial function
by 2D-STE may be useful to detect myocardial dysfunction induced by diet-related DCM, as
demonstrated in hypertrophic and restrictive cardiomyopathy in cats [13,25–27]. However,
2D-STE could not identify the myocardial functional characteristics specific to the diet-
related DCM to differentiate idiopathic DCM. Further studies that include a large
number of dogs with DCM of various causes are expected in the future.
In previous reports, the most common breeds of dogs with DCM were large-breed
dogs, such as Dobermans [28], but the dog in this case was a small-breed dog weighing
2.1 kg. Previous reports have stated that when DCM is diagnosed in atypical breeds,
such as small breeds, it is reasonable to suspect a nutritional etiology, especially when
dietary changes reversibly improve cardiac function [7]. Particularly in small breeds, there
are few reports of heritability. Therefore, diet-related involvement should be adequately
considered. In addition, current clinical diagnostic criteria do not include criteria related
to dietary content. In this case, we were unable to differentiate sufficiently between the
two until we confirmed the therapeutic response to the dietary changes. Therefore, the
patient’s diet should be included in the diagnosis and should be confirmed by a
thorough medical
Vet. Sci. 2022, 9, 593 7 of 9

interview. Furthermore, previous studies have reported that dogs with DCM on grain-
free diets have higher rates of congestive heart failure than those on grain-containing
diets [7]. Dogs with DCM fed a grain-free diet, such as the dog in this case, should be
considered at high risk for heart failure if diet modification is not made early enough
and should be carefully monitored. Meanwhile, it has been reported that dogs with DCM
with improved cardiac function after changing from a grain-free diet to an appropriate diet
have a better prognosis than dogs with DCM despite being on a grain-containing diet
[7]. In this case, a remarkable improvement in cardiac morphology and function was
observed after changing to a grain-containing diet, and the dog is still alive with no
recurrence of clinical signs 3 years and 5 months after the initial onset of heart failure.
Overall, diet-related DCM, as in this case, can be expected to have a good long-term
prognosis if managed with an appropriate diet.
There are limitations to this case report. The intervals between follow-ups have
been significantly longer, and multiple medications have been administered over a period
of approximately three years. These may have influenced the structural and functional
changes observed after approximately three years.

4. Conclusions
This is one of the few reports of diet-related DCM in a small dog. The 2D-STE could
detect the extensive and multidirectional myocardial dysfunction in dogs with diet-related
DCM. As mentioned in the beginning of this paper, various factors contribute to the
development of DCM. However, considering the recent diversification of dog diets, it
may be necessary to suspect a dietary association among small-breed dogs. Furthermore,
the prognosis for diet-related DCM in small-breed dogs may also be as good as in previous
reports of large-breed dogs, as long-term maintenance of the disease was achieved through
dietary modification in the present case.

Author Contributions: Formal analysis, T.S.; investigation, T.S.; resources, R.S.; data curation, T.S.;
writing—original draft preparation, T.S.; writing—review and editing, R.S., Y.Y. (Yunosuke Yuchi),
Y.Y. (Yuyo Yasumura), T.T., H.M. and H.K.; visualization, T.S.; supervision, R.S.; funding acquisition,
R.S. All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by the Japan Society for the Promotion of Science (JSPS) KAK-
ENHI, grant numbers 20K15667 and 22K05995.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Written informed consent authorizing the participation of dogs
in this study was obtained from the dog’s owner.
Data Availability Statement: The datasets used or analyzed during the current study are available
from the corresponding author upon reasonable request.
Acknowledgments: This study was conducted in the Laboratory of Veterinary Internal Medicine,
School of Veterinary Science, Faculty of Veterinary Medicine, Nippon Veterinary and Life Science
University, Tokyo, Japan.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Dukes-McEwan, J.; Borgarelli, M.; Tidholm, A.; Vollmar, A.C.; Hä ggströ m, J. Proposed Guidelines for the Diagnosis of Canine
Idiopathic Dilated Cardiomyopathy. J. Vet. Cardiol. 2003, 5, 7–19. [CrossRef]
2. Freeman, L.M.; Rush, J.E.; Brown, D.J.; Roudebush, P. Relationship between Circulating and Dietary Taurine Concentrations in
Dogs with Dilated Cardiomyopathy. Vet. Ther. 2001, 2, 370–378.
3. Backus, R.C.; Cohen, G.; Pion, P.D.; Good, K.L.; Rogers, Q.R.; Fascetti, A.J. Taurine Deficiency in Newfoundlands Fed Commer-
cially Available Complete and Balanced Diets. J. Am. Vet. Med. Assoc. 2003, 223, 1130–1136. [CrossRef] [PubMed]
4. Karlapudi, S.; Srikala, D.; Rao, D. Hypothyroidism—A Cause for Dilated Cardiomyopathy in Dogs; Four Year Study 2008–2011.
Vet. World 2012, 5, 742. [CrossRef]
Vet. Sci. 2022, 9, 593 8 of 9

5. Janus, I.; Noszczyk-Nowak, A.; Nowak, M.; Cepiel, A.; Ciaputa, R.; Pasławska, U.; Dzie˛giel, P.; Jabłon´ ska, K. Myocarditis in
Dogs: Etiology, Clinical and Histopathological Features (11 Cases: 2007–2013). Ir. Vet. J. 2014, 67, 28. [CrossRef] [PubMed]
6. Calvert, C.A.; Hall, G.; Jacobs, G.; Pickus, C. Clinical and Pathologic Findings in Doberman Pinschers with Occult
Cardiomyopathy That Died Suddenly or Developed Congestive Heart Failure: 54 Cases (1984–1991). J. Am. Vet. Med. Assoc.
1997, 210, 505–511.
7. Freid, K.J.; Freeman, L.M.; Rush, J.E.; Cunningham, S.M.; Davis, M.S.; Karlin, E.T.; Yang, V.K. Retrospective Study of Dilated
Cardiomyopathy in Dogs. J. Vet. Intern Med. 2021, 35, 58–67. [CrossRef] [PubMed]
8. Walker, A.L.; DeFrancesco, T.C.; Bonagura, J.D.; Keene, B.W.; Meurs, K.M.; Tou, S.P.; Kurtz, K.; Aona, B.; Barron, L.;
McManamey, A.; et al. Association of Diet with Clinical Outcomes in Dogs with Dilated Cardiomyopathy and Congestive Heart
Failure. J. Vet. Cardiol. 2022, 40, 99–109. [CrossRef] [PubMed]
9. Suzuki, R.; Matsumoto, H.; Teshima, T.; Koyama, H. Noninvasive Clinical Assessment of Systolic Torsional Motions by Two-
Dimensional Speckle-Tracking Echocardiography in Dogs with Myxomatous Mitral Valve Disease. J. Vet. Intern Med. 2013, 27,
69–75. [CrossRef] [PubMed]
10. Suzuki, R.; Matsumoto, H.; Teshima, T.; Mochizuki, Y.; Koyama, H. Dobutamine Stress Echocardiography for Assessment of
Systolic Function in Dogs with Experimentally Induced Mitral Regurgitation. J. Vet. Intern Med. 2014, 28, 386–392. [CrossRef]
[PubMed]
11. Suzuki, R.; Matsumoto, H.; Teshima, T.; Koyama, H. Influence of Heart Rate on Myocardial Function Using Two-Dimensional
Speckle-Tracking Echocardiography in Healthy Dogs. J. Vet. Cardiol. 2013, 15, 139–146. [CrossRef] [PubMed]
12. Suzuki, R.; Matsumoto, H.; Teshima, T.; Koyama, H. Effect of Age on Myocardial Function Assessed by Two-Dimensional
Speckle-Tracking Echocardiography in Healthy Beagle Dogs. J. Vet. Cardiol. 2013, 15, 243–252. [CrossRef] [PubMed]
13. Suzuki, R.; Yuchi, Y.; Kanno, H.; Teshima, T.; Matsumoto, H.; Koyama, H. Left and Right Myocardial Functionality Assessed
by Two-Dimensional Speckle-Tracking Echocardiography in Cats with Restrictive Cardiomyopathy. Animals 2021, 11, 1578.
[CrossRef]
14. Suzuki, R.; Matsumoto, H.; Teshima, T.; Koyama, H. Clinical Assessment of Systolic Myocardial Deformations in Dogs with
Chronic Mitral Valve Insufficiency Using Two-Dimensional Speckle-Tracking Echocardiography. J. Vet. Cardiol. 2013, 15, 41–
49. [CrossRef]
15. Yuchi, Y.; Suzuki, R.; Teshima, T.; Matsumoto, H.; Koyama, H. Right Ventricular Systolic and Diastolic Function Assessed by
Two-Dimensional Speckle Tracking Echocardiography in Dogs with Myxomatous Mitral Valve Disease. J. Vet. Med. Sci. 2021,
83, 1918–1927. [CrossRef]
16. Westrup, U.; McEvoy, F.J. Speckle Tracking Echocardiography in Mature Irish Wolfhound Dogs: Technical Feasibility,
Measure- ment Error and Reference Intervals. Acta Vet. Scand. 2013, 55, 41. [CrossRef]
17. Hamabe, L.; Fukushima, R.; Kawamura, K.; Shinoda, Y.; Huai-Che, H.; Suzuki, S.; Aytemiz, D.; Iwasaki, T.; Tanaka, R. Evaluation
of Changes in Left Ventricular Myocardial Function Observed in Canine Myocardial Dysfunction Model Using a Two-Dimensional
Tissue Tracking Technique. J. Vet. Sci. 2013, 14, 355–362. [CrossRef]
18. Kusunose, K.; Zhang, Y.; Mazgalev, T.N.; Thomas, J.D.; Popovic´, Z.B. Left Ventricular Strain Distribution in Healthy Dogs and
in Dogs with Tachycardia-Induced Dilated Cardiomyopathy. Cardiovasc. Ultrasound 2013, 11, 43. [CrossRef]
19. Pedro, B.; Stephenson, H.; Linney, C.; Cripps, P.; Dukes-McEwan, J. Assessment of Left Ventricular Function in Healthy Great
Danes and in Great Danes with Dilated Cardiomyopathy Using Speckle Tracking Echocardiography. J. Vet. Cardiol. 2017, 19,
363–375. [CrossRef]
20. Wess, G.; Keller, L.J.M.; Klausnitzer, M.; Killich, M.; Hartmann, K. Comparison of Longitudinal Myocardial Tissue Velocity,
Strain, and Strain Rate Measured by Two-Dimensional Speckle Tracking and by Color Tissue Doppler Imaging in Healthy
Dogs. J. Vet. Cardiol. 2011, 13, 31–43. [CrossRef]
21. Smith, D.N.; Bonagura, J.D.; Culwell, N.M.; Schober, K.E. Left Ventricular Function Quantified by Myocardial Strain Imaging in
Small-Breed Dogs with Chronic Mitral Regurgitation. J. Vet. Cardiol. 2012, 14, 231–242. [CrossRef] [PubMed]
22. Hamabe, L.; Mandour, A.S.; Shimada, K.; Uemura, A.; Yilmaz, Z.; Nagaoka, K.; Tanaka, R. Role of Two-Dimensional Speckle-
Tracking Echocardiography in Early Detection of Left Ventricular Dysfunction in Dogs. Animals 2021, 11, 2361. [CrossRef]
[PubMed]
23. Smith, C.E.; Parnell, L.D.; Lai, C.Q.; Rush, J.E.; Freeman, L.M. Investigation of Diets Associated with Dilated Cardiomyopathy in
Dogs Using Foodomics Analysis. Sci. Rep. 2021, 11, 15881. [CrossRef] [PubMed]
24. Chetboul, V.; Serres, F.; Gouni, V.; Tissier, R.; Pouchelon, J. Noninvasive Assessment of Systolic Left Ventricular Torsion by
2-Dimensional Speckle Tracking Imaging in the Awake Dog: Repeatability, Reproducibility, and Comparison with Tissue Doppler
Imaging Variables. J. Vet. Intern Med. 2008, 22, 342–350. [CrossRef]
25. Suzuki, R.; Mochizuki, Y.; Yoshimatsu, H.; Teshima, T.; Matsumoto, H.; Koyama, H. Determination of Multidirectional
Myocardial Deformations in Cats with Hypertrophic Cardiomyopathy by Using Two-Dimensional Speckle-Tracking
Echocardiography.
J. Feline Med. Surg. 2017, 19, 1283–1289. [CrossRef]
26. Spalla, I.; Boswood, A.; Connolly, D.J.; Luis Fuentes, V. Speckle Tracking Echocardiography in Cats with Preclinical
Hypertrophic Cardiomyopathy. J. Vet. Intern. Med. 2019, 33, 1232–1241. [CrossRef]
Vet. Sci. 2022, 9, 593 9 of 9

27. Saito, T.; Suzuki, R.; Yuchi, Y.; Teshima, T.; Matsumoto, H.; Koyama, H. Early Detection of Myocardial Dysfunction in a Cat
That Gradually Progressed to Endomyocardial Form of Restrictive Cardiomyopathy. BMC Vet. Res. 2021, 17, 274. [CrossRef]
28. Meurs, K.M.; Lahmers, S.; Keene, B.W.; White, S.N.; Oyama, M.A.; Mauceli, E.; Lindblad-Toh, K. A Splice Site Mutation in a Gene
Encoding for PDK4, a Mitochondrial Protein, Is Associated with the Development of Dilated Cardiomyopathy in the
Doberman Pinscher. Hum. Genet. 2012, 131, 1319–1325. [CrossRef]
LABORATORIUM ILMU PENYAKIT DALAM
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA

Kajian Pustaka:

Dilatasi Kardiomiopati
pada Anjing
Putu Intan Kusuma Wardani
NIM. 2209611066
Gelombang 21 Kelompok C
LABORATORIUM ILMU PENYAKIT DALAM
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA

Pendahuluan
• Dilatasi kardiomiopati atau dilated cardiomyopathy (DCM) adalah
penyakit miokard utama, ditandai dengan pembesaran ruang jantung
dan disfungsi sistolik yang parah.

• Beberapa laporan menunjukkan bahwa DCM terutama menyerang anjing


ras besar, seperti Doberman pinscher, Great Dane, Irish wolfhound,
dan Scottish deerhound.

• Tanda-tanda klinis DCM meliputi kelemahan, kelesuan, takipnea atau


dispnea, intoleransi olahraga, batuk, anoreksia, distensi perut, asites, dan
sinkop.

• DCM sekunder mungkin terkait dengan perubahan toksik, agen infeksius,


endokrinopati, dan gangguan nutrisi.
LABORATORIUM ILMU PENYAKIT DALAM
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA

Sinyalmen dan Anamnesis


Anjing kasus dengan ras Shiba Inu betina berusia 6
bulan, dengan berat badan 6,2 kg; ras Malta betina berusia
6 tahun, dengan berat badan 4,95 kg; dan ras Papillon
betina berusia 11 tahun, dengan berat badan 2,1 kg.

Ketiga anjing kasus rata-rata memiliki keluhan


utama yang sama yaitu mengalami batuk serta keluhan
nafas cepat dan dangkal.

Pemeriksaan klinis
Pada salah satu kasus didapatkan auskultasi aritmia, dengan
tingkat pernapasannya 132 per menit, dua dari tiga kasus pada
auskultasi terdengar suara murmur sistolik (Levine 2/6).
LABORATORIUM ILMU PENYAKIT DALAM
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA

Penunjang
Pemeriksaan
● Dua dari tiga kasus menyebutkan hasil pemeriksaan CBC yang menunjukkan hasil normal
dan peningkatan ringan neutrofil, dengan hasil biokimia darah menunjukkan hiperglikemia
(162 mg/dL) dan hipokalemia (3,1 mmol/L), dan konsentrasi tiroksin (3.21mg/dL) berada
dalam rentang normal

● Temuan EKG untuk DCM meliputi pelebaran kompleks QRS, pelebaran dan bentukan
gelombang P, kompleks prematur ventrikel seragam atau multiform (VPC), dan takikardia
ventrikel paroksismal. Dalam kasus ini, EKG mengungkapkan gelombang P dan VPC yang tinggi
dan lebar.
LABORATORIUM ILMU PENYAKIT DALAM
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA
Pemeriksaan Penunjang

● Radiografi toraks pada posisi dorsoventral dan lateral kanan menunjukkan atrium dan

Radiografiventrikel kiri yang membesar, meskipun pembesaran vena paru kranial ditunjukkan,
edema paru tidak diamati.

Dorsoventral (A) dan lateral kanan Radiografi toraks dorsoventral (A), lateral Radiografi toraks gambar kiri mewakili
(B) diambil pada Hari 1. Meskipun edema kanan (B), dan lateral kiri (C) menunjukkan
paru yang jelas tidak terlihat, pembesaran pembesaran moderat ventrikel kiri (kepala
atrium kiri dan ventrikel kiri serta panah) dengan penonjolan ringan pada atrium
pandangan dorsoventral, dan gambar kanan
pembesaran vena pulmonal kranial terlihat kanan (kepala panah putih) dan kiri (panah
hitam). Pola alveolar sedang (tanda bintang) di
lobus paru kanan dan bagian kranial lobus paru
kiri juga terdeteksi
LABORATORIUM ILMU PENYAKIT DALAM
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA

Pemeriksaan Penunjang

Ekokardiografi dua dimensi menunjukkan regurgitasi mitral


(MR), jantung sisi kiri yang sangat melebar dan jantung sisi kanan
yang sedikit membesar. Rasio LA:Ao adalah 2,45 (kisaran referensi:
<1,3). Dimensi akhir diastolik ventrikel kiri (LVDd) adalah 42,3 mm
(normal: 22,0-31,0 mm), dimensi akhir sistolik ventrikel kiri (LVD)
adalah 37,3 mm (normal: 12,0-22,0 mm), ketebalan septum
interventrikular akhir diastolik 4,8 mm (normal: 4,0-9,0 mm), dan
ketebalan dinding posterior ventrikel kiri akhir diastolic adalah 4,1
mm (normal: 4,0-9,0 mm), dan pemendekan fraksional (FS) adalah
11,8% (normal: 25,3%- 49,9%). Rekaman Doppler spektral
mengungkapkan kecepatan regurgitasi mitral yang tinggi (5,96
m/s).

Sumbu panjang parasternal kanan (A, B) dan tampilan sumbu


pendek (C) menunjukkan atrium kiri (LA) dan ventrikel kiri (LV)
yang melebar parah. Ekokardiogram Doppler aliran warna (B)
menunjukkan regurgitasi mitral eksentrik selama sistol (panah).
Rasio atrium kiri-aorta (LA/Ao) adalah 2,45 (C)
LABORATORIUM ILMU PENYAKIT DALAM
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA DiagnOsa

Diagnosa dari penyakit CDM didasarkan atas


temuan klinis, pemeriksaan radiografi dan
ekokardiografi. Pada ketiga kasus tersebut telah
dikonfirmasi bahwa anjing kasus didiagnosis
menderita penyakit dilatasi kardiomiopati

PrOgnOsis

Prognosis untuk anjing dengan DCM bervariasi


mulai dari hari ke tahun, tergantung pada banyak
variable. Waktu bertahan hidup diketahui terkait
dengan tanda-tanda klinis terkait jantung,
ekokardiografi atau kelainan listrik jantung. Jika
gejala menunjukkan gagal jantung kongesti,
prognosisnya seringkali buruk
LABORATORIUM ILMU PENYAKIT DALAM

Penanganan
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA

• Pengobatan pada ketiga kasus dilakukan dengan pemberian obat


ionotropik positif dan vasodilatator yaitu pimobendan (0,2 – 0,3
mg/kg BB), obat golongan diuretik yaitu furosemid (2 mg/kg BB),
torasemid (0,15 mg/kg BB), pemberian taurin (250 – 500 mg/ekor),
dan obat ACE-inhibitor ramipril (0,125 mg/kg BB), remocapril (0,1
mg/kg BB).

• Dari tiga kasus DCM yang telah mendapat pengobatan, dua


diantaranya mengalami kematian mendadak.
Gambar histologis miokardium ventrikel
kiri (pewarnaan HE) menunjukkan serat • Pada anjing kasus yang bertahan hidup, pola makan anjing kasus
miokard melemah dan bergelombang
dengan atrofi dan penipisan. Selain itu, diubah dari pola makan bebas biji-bijian menjadi pola makan yang
edema stroma terlihat
mengandung biji-bijian. Untuk pengobatan tidak ada perubahan
pada pengobatan oral oral (pimobendane [0,3 mg/kg BB],
temocapril [0,1 mg/kg BB], taurin [250 mg/ekor] dan furosemid
[2,0 mg/kg BB])
LABORATORIUM ILMU PENYAKIT DALAM
FAKULTAS KEDOKTERAN HEWAN
UNIVERSITAS UDAYANA

Saran

Anjing dengan kasus dilatasi kardiomiopati perlu


dilakukan pemantauan yang intensif karena terdapat
resiko kematian mendadak, serta harus rutin
memeriksakan anjing ke dokter hewan.
TERIMA KASIH

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