- Email: [email protected]
Real-time three-dimensional echocardiographic study of a cardiac hemangiosarcoma in a dog
Journal Pre-proof Real-time three-dimensional echocardiographic study of a cardiac hemangiosarcoma in a dog Elisabetta Boz, DVM, Melissa Papa, DVM, Marta Claretti, DVM, Roberto Bussadori, DVM, Blanca Serrano Lopez, DVM, Cecilia Rossi, DVM, Laura Mazzoni, DVM, Danitza Pradelli, DVM, PhD, Claudio Maria Bussadori, DVM, MD, PhD PII:
S1760-2734(20)30007-2
DOI:
https://doi.org/10.1016/j.jvc.2020.02.001
Reference:
JVC 610
To appear in:
Journal of Veterinary Cardiology
Received Date: 12 April 2019 Revised Date:
7 January 2020
Accepted Date: 11 February 2020
Please cite this article as: Boz E, Papa M, Claretti M, Bussadori R, Lopez BS, Rossi C, Mazzoni L, Pradelli D, Bussadori CM, Real-time three-dimensional echocardiographic study of a cardiac hemangiosarcoma in a dog, Journal of Veterinary Cardiology, https://doi.org/10.1016/j.jvc.2020.02.001. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier B.V.
1
Real-time
three-dimensional
2
hemangiosarcoma in a dog.
echocardiographic
study
of
a
cardiac
3 4
Elisabetta Boz, DVM; Melissa Papa, DVM; Marta Claretti, DVM ; Roberto Bussadori,
5
DVM; Blanca Serrano Lopez, DVM; Cecilia Rossi, DVM; Laura Mazzoni, DVM; Danitza
6
Pradelli, DVM, PhD; Claudio Maria Bussadori, DVM, MD, PhD
7 8
Department of Cardiology of Clinica Veterinaria Gran Sasso, Via Donatello 26, 20131,
9
Milano, Italy
10 11 12 13
3D echo study of a cardiac tumor
14 15
Corresponding Author:
16
Dr. Elisabetta Boz
17
[email protected]
18 19 20
1
21
Abstract A 7-year-old Golden Retriever was presented for a second opinion regarding a
22 23
cardiac
mass.
Two-dimensional
transthoracic
echocardiography
24
presence of a mass in the area of the right atrium. The mass appeared adherent and
25
possibly infiltrative to the external wall of the right atrium. Three-dimensional
26
transthoracic echocardiography allowed better visualization of the neoplasia suggesting
27
that is was not infiltrative and contributed significantly to the decision to carry out the
28
surgical resection of the cardiac tumor. This case report demonstrates the utility of
29
three-dimensional transthoracic echocardiography in the diagnostic evaluation of
30
cardiac masses in dogs without the need for general anesthesia.
31 32
Keywords
33
Ultrasound; Imaging; heart; tumor; three-dimensional ultrasound
34 35
Abbreviation Table 2D TTE
two-dimensional transthoracic echocardiography
3D TTE
three-dimensional transthoracic echocardiography
CT
computed tomography
HSA
hemangiosarcoma
36 37 38 39 40 41 42 2
demonstrated
43 44 45 46 47 48
A 7-year-old intact male Golden retriever was presented to the emergency
49
service of another veterinary hospital for weakness, exercise intolerance and dyspnea.
50
Clinical examination, thoracic radiographs, echocardiography and abdominal ultrasound
51
demonstrated pericardial effusion with cardiac tamponade and a cardiac mass on the
52
right atrium. Serum biochemistry and hematology revealed leukocytosis (54.40 x 109/L ,
53
normal range: 6-17 x 109/L), neutrophilia (48 x 109/L, normal range: 4-12.6 x 109/L),
54
and elevated blood urea nitrogen level (55 mg/dL, normal range: 7-25 mg/dL),
55
creatinine (2.6 mg/dL, normal range: 0.5-1.4 mg/dL), alanine aminotransferase (54.0
56
uL/L, normal range: 14-43 uL/L) and aspartate aminotransferase (123 uL/L normal
57
range: 15-58 uL/L). Twelve-lead electrocardiography revealed sinus tachycardia, with a
58
heart rate of 180 beats per minute (bpm), regular R-R intervals, and narrow QRS
59
complexes (<70 msec).
60
Pericardiocentesis was performed.
61
hemopericardium.
62
identified residual pericardial effusion, a right atrial cardiac mass, absence of thoracic
63
and abdominal metastatic lesions. The cardiac mass appeared to infiltrate the right
64
atrial wall, and hence was deemed non-operable.
Analysis of the fluid was consistent with
Whole-body computed tomography (CT) with contrast agent
65
A second opinion was sought at the author’s referral hospital. At the clinical
66
examination, the dog was alert, with pink mucous membranes, capillary refill time < 2 s,
67
heart rate of 150 bpm, respiratory rate equal to 32 breaths per minute, body
68
temperature 38.7°C. Two-dimensional transthoracic e chocardiography (2D TTE) was 3
a
69
performed with Philips Epiq 7 echocardiograph
70
transducer
71
echocardiographic projection that allowed visualization of right atrium, right auricle, both
72
vena cavae and partial tricuspid valve was performed to visualize the mass [2]. The
73
presence of a round, capsulated mass with inhomogeneous echotexture was confirmed
74
on the dorsal aspect of the right atrium. The mass did not appear to infiltrate
75
atrioventricular junction and measured 3.8 cm X 2.8 cm (Fig. 1, Video 1). Real-time
76
three-dimensional transthoracic echocardiography (3D TTE) with single-beat acquisition
77
showed a small base of adherence to the right atrium that did not appear to infiltrate the
78
right appendage (Fig. 2, Fig. 3, Video 2). Single-beat 3D TTE acquisition allowed better
79
visualization of the mass and its relationships to cardiac structures compared to multi-
80
beat real-time 3D TTE which presented many artifacts. The remainder of the
81
echocardiographic examination was normal. Based on 3D TTE the cardiac mass was
82
considered non-infiltrative and amendable to surgical excision. The CT exam performed
83
prior to presentation did not establish the degree of infiltration of the cardiac mass
84
because the images were optimized for visualization of bone and not soft tissue. The
85
authors did not consider it necessary to carry out another CT exam because the
86
echocardiographic examinations were considered adequate for an accurate diagnosis.
87
Based on the 3D TTE examination surgery was recommended and the dog underwent
88
thoracotomy, pericardiectomy and a complete surgical excision of the cardiac mass.
89
Histological examination of the mass revealed hemangiosarcoma (HSA) tumor and mild
90
and diffuse fibrosis of the pericardium. The resection margins of the mass showed no
91
neoplastic infiltration.
b
equipped with a X5-1 x-matrix array
according to published recommendations [1].
Additionally an off-axis
92
Two weeks after surgery chemotherapy with doxorubicin administrated IV at 30
93
mg/m² every 21 days, and metronomic chemotherapy with cyclophosphamide
94
administrated IV at 30 mg/m² every 21 days. Subsequently the dog continued with 4
95
metronomic chemotherapy with cyclophosphamide, 10 mg/m2, PO, every 24h,
96
piroxicam 0.3 mg/kg, PO, every 24h and lansoprazole administrated orally at 1 mg/kg
97
q24h [3].
98
Nine months after surgery the dog was in good health, underwent regular check-ups,
99
and continued to receive metronomic chemotherapy. Pericardial effusion did not recur
100
and clinical signs related to heart disease were not apparent.
101 102 103
Discussion
104
Cardiac tumors are uncommon in dogs. The most complete retrospective study
105
includes a population of 729,265 dogs in which the patients affected by cardiac tumors
106
were 1383, resulting in an incidence of 0.19% [4]. The most common cardiac tumor in
107
dogs is HSA, which has the most frequent localization on the right atrium or on the right
108
appendage of the heart [5]. A higher incidence of HSA is in German shepherd dogs and
109
Golden retriever [5,6-8]: the mean age is 10 years [8]. In some studies, regarding
110
cardiac tumors in dogs, there is no gender predisposition [5]; however, in other studies,
111
there is a high prevalence in males [6,8], although it has been suggested that neutered
112
females may be at an increased risk [5,8]. When canine HSA is localized to right atrium
113
or right appendage, the most frequent clinical signs are pericardial effusion, cardiac
114
tamponade, right-sided congestive heart failure, that cause weakness, lethargy,
115
exercise intolerance, anorexia, dyspnea, cough, loss of consciousness, abdominal
116
effusion, weight loss [8]. Canine HSA may present as single cardiac mass or may be
117
associated with splenic neoplasia. The most recent studies report an incidence with
118
involvement of both localizations ranging from 8.7 to 25% [5]. Canine HSA is associated
119
with poor prognosis; studies of this topic refer a survival times less than 2 months from
120
the diagnosis [9]. A study performed by Dunning et al. compares the survival time of 5
121
canine patients who undergo pericardiectomy with the survival time of patients who do
122
not undergo therapy; results show similar survival time in both cases [10]. The survival
123
time differs in those canine cases where the mass is surgically removed and the dog
124
undergoes chemotherapeutic treatment; this situation is characterized by an increase in
125
the survival time that can reach 6 months [10-12]. Although echocardiography cannot
126
provide a histopathologic diagnosis or cardiac tumor classification, it can allow
127
assessment of the degree of infiltration of the mass which can help guide the decision
128
to pursue surgical or medical treatment. In a study by Yamamoto et al. [13], 2D TTE
129
was useful in the identification of lesions suggestive of HSA, but was less sensitivitive in
130
distinguishing lesions associated with the right atrial appendage compared to lesions
131
presenting with continuity with the right atrium.
132
A 2D TTE is a fundamental diagnostic method in the identification and study of
133
cardiac masses in the presence of pericardial effusion. However 2D TTE has
134
limitations. The visual field is limited by the two dimensions, and in some cases, this
135
may not facilitate the definition of the limits of the neoplasia. It also underestimates the
136
volume of the mass in 24% of cases [14]. Moreover, this type of study is limited in the
137
definition of the type of tissue that constitutes the mass. Several reports in human
138
patients suggest the diagnostic utility of three-dimensional echocardiography in the
139
study of cardiac tumors. Among the advantages linked to this technique are greater
140
accuracy for estimates of the tumor volume, more information on the type of tumor
141
facilitating the hypothesis on classification, and better assessment of the site of
142
continuity with the cardiac tissue and relationships with the surrounding intrathoracic
143
structures
144
echocardiography in the description of a papillary fibroelastoma was demonstrated in a
145
55-year-old
146
echocardiography suggested two masses at the level of the mitral valve. The 6
[14].
The
woman
importance
[15].
In
this
of
case
three-dimensional
two-dimensional
transesophageal
transesophageal
147
subsequent
three-dimensional transesophageal echocardiography investigation
148
showed the presence of only a single mass at the level of the mitral anterior leaflet
149
facilitating formulation of a surgical plan. In a study of 41 human patients, 3D TEE
150
provided additional information regarding cardiac masses in 37% of patients compared
151
to 2D TEE [16]. In this study, 3D TTE aided with the choice of the surgical approach for
152
the removal of the cardiac mass and provided information useful to the diagnostic
153
hypothesis of classification of the primary tumor type. In a case report of a 33-year-old
154
man, a presumptive diagnosis of myxoma was made based on 2D TTE images that
155
revealed a large, mobile, smooth, oval, non-lobulated pedunculated mass in the left
156
ventricle [17].Subsequent analysis of slicing sections of 3D TTE suggested of vascular
157
spaces and modified the presumptive diagnosis from myxoma to hemangioma, which
158
was subsequently confirmed by histological examination. Studies in veterinary medicine
159
on the use of three-dimensional echocardiography have mainly focused on mitral valve
160
morphology and volumetric ventricular quantification [16,18,19]. This case report
161
demonstrates the utility of three-dimensional echocardiography in the evaluation of
162
cardiac masses. Software allowed precise anatomical multi-planar reconstruction of the
163
mass and the relation between the mass and right atrium. This helped to confirm that
164
there was no infiltration of the surrounding tissues, which led to the formulation of a
165
therapeutic plan for surgical removal of the mass. This technique allowed for analysis of
166
structures in motion and relationships between the structures in the various phases of
167
the cardiac cycle. In this case, the 3D TTE technique was considered accurate enough
168
that it was not necessary to perform a transesophageal echocardiographic study or CT
169
exam, reducing the need for general anesthesia in a dog with pericardial effusion.
170
Three-dimensional study of cardiac tumors in veterinary medicine has been reported
171
through the use of magnetic resonance imaging in two dogs with tumors localized at the
172
heart base. This imaging technique helped in the three-dimensional visualization of the 7
173
mass and the study of the relationships of the neoplasia with the surrounding tissues
174
and the surrounding vascular structures [20]. However, magnetic resonance imaging in
175
veterinary medicine is associated with high costs and the patient must undergo on
176
general anesthesia. The present case report demonstrates the value of 3D TTE in the
177
study of cardiac tumors in canine patients.
178 179 180 181 182 183
References
184 185
[1] Thomas WP, Gaber CE, Jacobs GJ, et al. Recommendations for standards in
186
transthoracic two-dimensional echocardiography in the dog and cat. Echocardiography
187
Committee of the Specialty of Cardiology, American College of Veterinary Internal
188
Medicine. Journal of Veterinary internal medicine 1993;7:247-252.
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[2] Bussadori C, Pradelli D. Neoplasie cardiache. In: Santilli RA, Bussadori C, Borgarelli
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M, editor. Manuale di cardiologia del cane e del gatto. Milano: Elsevier; 2012, p. 269-
191
271.
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[3] Wendelburg KM, Price LL, Burgess KE, Lyons JA, Lew FH, Berg J, Survival time of
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dogs with splenic hemangiosarcoma treated by splenectomy with or without adjuvant
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chemotherapy: 208 cases (2001–2012). Journal of the American Veterinary Medical
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Association Vol 247, No. 4, August 15, 2015 [4] Ware WA, Hopper DL. Cardiac tumors
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in dogs: 1982-1995. Journal of veterinary internal medicine 1999;13:95-103.
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[4] Detweiler DK and Patterson DF. The prevalence and types of cardiovascular
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disease in dogs. Annals of the New York Academy of Sciences 1965; 127: 481–516. 8
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[5] Ware WA, Hopper DL. Cardiac tumors in dogs: 1982-1995. Journal of veterinary
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internal medicine 1999;13;95-103.
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[6] Brown NO, Patnaik AK, MacEwen EG. Canine hemangiosarcoma: retrospective
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analysis of 104 cases. Journal of the American Veterinary Medical Association
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1985;186;56-58.
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[7] Srebernik N, Appleby EC. Breed prevalence and sites of haemangioma and
205
haemangiosarcoma in dogs. The Veterinary record 1991;129;408-409.
206
[8] Yamamoto S, Hoshi K, Hirakawa A, et al. Epidemiological, clinical and pathological
207
features of primary cardiac hemangiosarcoma in dogs: a review of 51 cases. The
208
Journal of veterinary medical science 2013;75;1433-1441.
209
[9] Rajagopalan V, Jesty SA, Craig LE, et al. Comparison of presumptive
210
echocardiographic and definitive diagnoses of cardiac tumors in dogs. Journal of
211
veterinary internal medicine 2013;27;1092-1096.
212
[10] Dunning D, Monnet E, Orton EC, et al. Analysis of prognostic indicators for dogs
213
with pericardial effusion: 46 cases (1985-1996). Journal of the American Veterinary
214
Medical Association 1998;212;1276-1280.
215
[11] Weisse C, Soares N, Beal MW, et al. Survival times in dogs with right atrial
216
hemangiosarcoma treated by means of surgical resection with or without adjuvant
217
chemotherapy: 23 cases (1986-2000). Journal of the American Veterinary Medical
218
Association 2005;226;575-579.
219
[12] Aronsohn M. Cardiac hemangiosarcoma in the dog: a review of 38 cases. Journal
220
of the American Veterinary Medical Association 1985;187;922-926.
221
[13] Yamamoto S, Hoshi K, Hirakawa A, et al. Epidemiological, clinical and pathological
222
features of primary cardiac hemangiosarcoma in dogs: a review of 51 cases. The
223
Journal of veterinary medical science 2013;75;1433-1441.
9
224
[14] Asch FM, Bieganski SP, Panza JA, Weissman NJ. Real-time 3-dimensional
225
echocardiography
226
2006;23(3):218-24. [15] Suresh R, Boor PJ, Al-Dossari GA, et al. Utility of real-time
227
three-dimensional echocardiography in improved assessment of a mitral valve papillary
228
fibroelastoma. Clinical case reports 2017;5;1193-1195.
229
[16] Muller S, Feuchtner G, Bonatti J, et al. Value of transesophageal 3D
230
echocardiography as an adjunct to conventional 2D imaging in preoperative evaluation
231
of cardiac masses. Echocardiography (Mount Kisco, NY) 2008;25;624-631.
232
[17] Garg N, Kapur KK, Ganjoo A, et al. Case report: a rare case of pedunculated LV
233
hemangioma evaluated by 3D echocardiography and compared with myxoma.
234
Echocardiography (Mount Kisco, NY) 2016;33;1608-1610.
235
[18] LeBlanc NL, Scollan KF. Quantification of right ventricular volume measured by use
236
of real-time three-dimensional echocardiography and electrocardiography-gated 64-
237
slice multidetector computed tomography in healthy dogs. American journal of
238
veterinary research 2018;79;404-410.
239
[19] Menciotti G, Borgarelli M, Aherne M, et al. Comparison of the mitral valve
240
morphologies of Cavalier King Charles Spaniels and dogs of other breeds using 3D
241
transthoracic echocardiography. Journal of veterinary internal medicine 2018;32;1564-
242
1569.
243
[20] Mai W, Weisse C, Sleeper MM. Cardiac magnetic resonance imaging in normal
244
dogs and two dogs with heart base tumor. Veterinary radiology & ultrasound: the official
245
journal of the American College of Veterinary Radiology and the International Veterinary
246
Radiology Association 2010;51;428-435.
evaluation
of
intracardiac
247 248 249 10
masses.
Echocardiography
250
Footnotes
251
a Philips Epiq 7C, Philips SpA Healthcare, Monza (MB), Italy
252
b Philips X5-1, xMATRIX array transducer with PureWave crystal technology, Philips
253
SpA Healthcare, Monza (MB), Italy
254 255 256
Figure 1
257
Two-dimensional transthoracic echocardiography, right parasternal long axis view. The
258
right atrium is collapsed and a mass with mixed echotexture is in contact with the atrial
259
wall and appears to be in continuity with atrioventricular junction. LV: left ventricle; LA:
260
left atrium; TV: tricuspid valve; NPL: neoplasia.
261
Figure 2
262
Real-time three-dimensional transthoracic echocardiographic study of the right atrium
263
and right ventricle. The arrow indicates the tumor appears to be isolated from
264
atrioventricular junction. RV: right ventricle; TV: tricuspid valve; NPL: neoplasia.
265 266
Figure 3
267
Real-time three-dimensional echocardiographic study of the right atrium and the right
268
ventricle. The tricuspid valve is closed and the tumor is located in continuity with the
269
atrial wall. TV: tricuspid valve: RA: right atrium; RV: right ventricle.
270 271
Figure 4
272
Real-time three-dimensional echocardiographic study of the right atrium and the right
273
ventricle during diastolic and systolic phase. The first image (A) is recorded during atrial
274
contraction. Tricuspid valve is open and the tumor is visible near the right atrium. The
275
second image (B) is recorded during atrial diastole. Tricuspid valve is closed and the 11
276
normal internal atrial wall is seen with the outlet of the caudal vena cava. The third
277
image (C) is recorded during atrial diastole. Slight rotation was made for a better view of
278
the inner wall of the right atrium.
279
ventricle; CVC: caudal vena cava; NPL: neoplasia.
TV: tricuspid valve: RA: right atrium; RV: right
280 281 282 283 284 285 Video 1
Two-dimensional view of the neoplasia
Two-dimensional transthoracic echocardiography, apical four chamber view. A large mass with mixed echogenicity is visible located at the level of right atrium. NPL: neoplasia; RV: right ventricle.
Video 2
Real-time threedimensional view of the neoplasia
Real-time three-dimensional echocardiographic study of the right atrium and the right ventricle. The margins of the mass are independent from the atrioventricular junction. The cardiac mass is not always visible and in some
12
phases of the cardiac cycle the right atrial cavity is observed. RV: right ventricle; TV: tricuspid valve; NPL: neoplasia.
286 287 288 289 290 291 292
13
S1760-2734(20)30007-2
DOI:
https://doi.org/10.1016/j.jvc.2020.02.001
Reference:
JVC 610
To appear in:
Journal of Veterinary Cardiology
Received Date: 12 April 2019 Revised Date:
7 January 2020
Accepted Date: 11 February 2020
Please cite this article as: Boz E, Papa M, Claretti M, Bussadori R, Lopez BS, Rossi C, Mazzoni L, Pradelli D, Bussadori CM, Real-time three-dimensional echocardiographic study of a cardiac hemangiosarcoma in a dog, Journal of Veterinary Cardiology, https://doi.org/10.1016/j.jvc.2020.02.001. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier B.V.
1
Real-time
three-dimensional
2
hemangiosarcoma in a dog.
echocardiographic
study
of
a
cardiac
3 4
Elisabetta Boz, DVM; Melissa Papa, DVM; Marta Claretti, DVM ; Roberto Bussadori,
5
DVM; Blanca Serrano Lopez, DVM; Cecilia Rossi, DVM; Laura Mazzoni, DVM; Danitza
6
Pradelli, DVM, PhD; Claudio Maria Bussadori, DVM, MD, PhD
7 8
Department of Cardiology of Clinica Veterinaria Gran Sasso, Via Donatello 26, 20131,
9
Milano, Italy
10 11 12 13
3D echo study of a cardiac tumor
14 15
Corresponding Author:
16
Dr. Elisabetta Boz
17
[email protected]
18 19 20
1
21
Abstract A 7-year-old Golden Retriever was presented for a second opinion regarding a
22 23
cardiac
mass.
Two-dimensional
transthoracic
echocardiography
24
presence of a mass in the area of the right atrium. The mass appeared adherent and
25
possibly infiltrative to the external wall of the right atrium. Three-dimensional
26
transthoracic echocardiography allowed better visualization of the neoplasia suggesting
27
that is was not infiltrative and contributed significantly to the decision to carry out the
28
surgical resection of the cardiac tumor. This case report demonstrates the utility of
29
three-dimensional transthoracic echocardiography in the diagnostic evaluation of
30
cardiac masses in dogs without the need for general anesthesia.
31 32
Keywords
33
Ultrasound; Imaging; heart; tumor; three-dimensional ultrasound
34 35
Abbreviation Table 2D TTE
two-dimensional transthoracic echocardiography
3D TTE
three-dimensional transthoracic echocardiography
CT
computed tomography
HSA
hemangiosarcoma
36 37 38 39 40 41 42 2
demonstrated
43 44 45 46 47 48
A 7-year-old intact male Golden retriever was presented to the emergency
49
service of another veterinary hospital for weakness, exercise intolerance and dyspnea.
50
Clinical examination, thoracic radiographs, echocardiography and abdominal ultrasound
51
demonstrated pericardial effusion with cardiac tamponade and a cardiac mass on the
52
right atrium. Serum biochemistry and hematology revealed leukocytosis (54.40 x 109/L ,
53
normal range: 6-17 x 109/L), neutrophilia (48 x 109/L, normal range: 4-12.6 x 109/L),
54
and elevated blood urea nitrogen level (55 mg/dL, normal range: 7-25 mg/dL),
55
creatinine (2.6 mg/dL, normal range: 0.5-1.4 mg/dL), alanine aminotransferase (54.0
56
uL/L, normal range: 14-43 uL/L) and aspartate aminotransferase (123 uL/L normal
57
range: 15-58 uL/L). Twelve-lead electrocardiography revealed sinus tachycardia, with a
58
heart rate of 180 beats per minute (bpm), regular R-R intervals, and narrow QRS
59
complexes (<70 msec).
60
Pericardiocentesis was performed.
61
hemopericardium.
62
identified residual pericardial effusion, a right atrial cardiac mass, absence of thoracic
63
and abdominal metastatic lesions. The cardiac mass appeared to infiltrate the right
64
atrial wall, and hence was deemed non-operable.
Analysis of the fluid was consistent with
Whole-body computed tomography (CT) with contrast agent
65
A second opinion was sought at the author’s referral hospital. At the clinical
66
examination, the dog was alert, with pink mucous membranes, capillary refill time < 2 s,
67
heart rate of 150 bpm, respiratory rate equal to 32 breaths per minute, body
68
temperature 38.7°C. Two-dimensional transthoracic e chocardiography (2D TTE) was 3
a
69
performed with Philips Epiq 7 echocardiograph
70
transducer
71
echocardiographic projection that allowed visualization of right atrium, right auricle, both
72
vena cavae and partial tricuspid valve was performed to visualize the mass [2]. The
73
presence of a round, capsulated mass with inhomogeneous echotexture was confirmed
74
on the dorsal aspect of the right atrium. The mass did not appear to infiltrate
75
atrioventricular junction and measured 3.8 cm X 2.8 cm (Fig. 1, Video 1). Real-time
76
three-dimensional transthoracic echocardiography (3D TTE) with single-beat acquisition
77
showed a small base of adherence to the right atrium that did not appear to infiltrate the
78
right appendage (Fig. 2, Fig. 3, Video 2). Single-beat 3D TTE acquisition allowed better
79
visualization of the mass and its relationships to cardiac structures compared to multi-
80
beat real-time 3D TTE which presented many artifacts. The remainder of the
81
echocardiographic examination was normal. Based on 3D TTE the cardiac mass was
82
considered non-infiltrative and amendable to surgical excision. The CT exam performed
83
prior to presentation did not establish the degree of infiltration of the cardiac mass
84
because the images were optimized for visualization of bone and not soft tissue. The
85
authors did not consider it necessary to carry out another CT exam because the
86
echocardiographic examinations were considered adequate for an accurate diagnosis.
87
Based on the 3D TTE examination surgery was recommended and the dog underwent
88
thoracotomy, pericardiectomy and a complete surgical excision of the cardiac mass.
89
Histological examination of the mass revealed hemangiosarcoma (HSA) tumor and mild
90
and diffuse fibrosis of the pericardium. The resection margins of the mass showed no
91
neoplastic infiltration.
b
equipped with a X5-1 x-matrix array
according to published recommendations [1].
Additionally an off-axis
92
Two weeks after surgery chemotherapy with doxorubicin administrated IV at 30
93
mg/m² every 21 days, and metronomic chemotherapy with cyclophosphamide
94
administrated IV at 30 mg/m² every 21 days. Subsequently the dog continued with 4
95
metronomic chemotherapy with cyclophosphamide, 10 mg/m2, PO, every 24h,
96
piroxicam 0.3 mg/kg, PO, every 24h and lansoprazole administrated orally at 1 mg/kg
97
q24h [3].
98
Nine months after surgery the dog was in good health, underwent regular check-ups,
99
and continued to receive metronomic chemotherapy. Pericardial effusion did not recur
100
and clinical signs related to heart disease were not apparent.
101 102 103
Discussion
104
Cardiac tumors are uncommon in dogs. The most complete retrospective study
105
includes a population of 729,265 dogs in which the patients affected by cardiac tumors
106
were 1383, resulting in an incidence of 0.19% [4]. The most common cardiac tumor in
107
dogs is HSA, which has the most frequent localization on the right atrium or on the right
108
appendage of the heart [5]. A higher incidence of HSA is in German shepherd dogs and
109
Golden retriever [5,6-8]: the mean age is 10 years [8]. In some studies, regarding
110
cardiac tumors in dogs, there is no gender predisposition [5]; however, in other studies,
111
there is a high prevalence in males [6,8], although it has been suggested that neutered
112
females may be at an increased risk [5,8]. When canine HSA is localized to right atrium
113
or right appendage, the most frequent clinical signs are pericardial effusion, cardiac
114
tamponade, right-sided congestive heart failure, that cause weakness, lethargy,
115
exercise intolerance, anorexia, dyspnea, cough, loss of consciousness, abdominal
116
effusion, weight loss [8]. Canine HSA may present as single cardiac mass or may be
117
associated with splenic neoplasia. The most recent studies report an incidence with
118
involvement of both localizations ranging from 8.7 to 25% [5]. Canine HSA is associated
119
with poor prognosis; studies of this topic refer a survival times less than 2 months from
120
the diagnosis [9]. A study performed by Dunning et al. compares the survival time of 5
121
canine patients who undergo pericardiectomy with the survival time of patients who do
122
not undergo therapy; results show similar survival time in both cases [10]. The survival
123
time differs in those canine cases where the mass is surgically removed and the dog
124
undergoes chemotherapeutic treatment; this situation is characterized by an increase in
125
the survival time that can reach 6 months [10-12]. Although echocardiography cannot
126
provide a histopathologic diagnosis or cardiac tumor classification, it can allow
127
assessment of the degree of infiltration of the mass which can help guide the decision
128
to pursue surgical or medical treatment. In a study by Yamamoto et al. [13], 2D TTE
129
was useful in the identification of lesions suggestive of HSA, but was less sensitivitive in
130
distinguishing lesions associated with the right atrial appendage compared to lesions
131
presenting with continuity with the right atrium.
132
A 2D TTE is a fundamental diagnostic method in the identification and study of
133
cardiac masses in the presence of pericardial effusion. However 2D TTE has
134
limitations. The visual field is limited by the two dimensions, and in some cases, this
135
may not facilitate the definition of the limits of the neoplasia. It also underestimates the
136
volume of the mass in 24% of cases [14]. Moreover, this type of study is limited in the
137
definition of the type of tissue that constitutes the mass. Several reports in human
138
patients suggest the diagnostic utility of three-dimensional echocardiography in the
139
study of cardiac tumors. Among the advantages linked to this technique are greater
140
accuracy for estimates of the tumor volume, more information on the type of tumor
141
facilitating the hypothesis on classification, and better assessment of the site of
142
continuity with the cardiac tissue and relationships with the surrounding intrathoracic
143
structures
144
echocardiography in the description of a papillary fibroelastoma was demonstrated in a
145
55-year-old
146
echocardiography suggested two masses at the level of the mitral valve. The 6
[14].
The
woman
importance
[15].
In
this
of
case
three-dimensional
two-dimensional
transesophageal
transesophageal
147
subsequent
three-dimensional transesophageal echocardiography investigation
148
showed the presence of only a single mass at the level of the mitral anterior leaflet
149
facilitating formulation of a surgical plan. In a study of 41 human patients, 3D TEE
150
provided additional information regarding cardiac masses in 37% of patients compared
151
to 2D TEE [16]. In this study, 3D TTE aided with the choice of the surgical approach for
152
the removal of the cardiac mass and provided information useful to the diagnostic
153
hypothesis of classification of the primary tumor type. In a case report of a 33-year-old
154
man, a presumptive diagnosis of myxoma was made based on 2D TTE images that
155
revealed a large, mobile, smooth, oval, non-lobulated pedunculated mass in the left
156
ventricle [17].Subsequent analysis of slicing sections of 3D TTE suggested of vascular
157
spaces and modified the presumptive diagnosis from myxoma to hemangioma, which
158
was subsequently confirmed by histological examination. Studies in veterinary medicine
159
on the use of three-dimensional echocardiography have mainly focused on mitral valve
160
morphology and volumetric ventricular quantification [16,18,19]. This case report
161
demonstrates the utility of three-dimensional echocardiography in the evaluation of
162
cardiac masses. Software allowed precise anatomical multi-planar reconstruction of the
163
mass and the relation between the mass and right atrium. This helped to confirm that
164
there was no infiltration of the surrounding tissues, which led to the formulation of a
165
therapeutic plan for surgical removal of the mass. This technique allowed for analysis of
166
structures in motion and relationships between the structures in the various phases of
167
the cardiac cycle. In this case, the 3D TTE technique was considered accurate enough
168
that it was not necessary to perform a transesophageal echocardiographic study or CT
169
exam, reducing the need for general anesthesia in a dog with pericardial effusion.
170
Three-dimensional study of cardiac tumors in veterinary medicine has been reported
171
through the use of magnetic resonance imaging in two dogs with tumors localized at the
172
heart base. This imaging technique helped in the three-dimensional visualization of the 7
173
mass and the study of the relationships of the neoplasia with the surrounding tissues
174
and the surrounding vascular structures [20]. However, magnetic resonance imaging in
175
veterinary medicine is associated with high costs and the patient must undergo on
176
general anesthesia. The present case report demonstrates the value of 3D TTE in the
177
study of cardiac tumors in canine patients.
178 179 180 181 182 183
References
184 185
[1] Thomas WP, Gaber CE, Jacobs GJ, et al. Recommendations for standards in
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transthoracic two-dimensional echocardiography in the dog and cat. Echocardiography
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[2] Bussadori C, Pradelli D. Neoplasie cardiache. In: Santilli RA, Bussadori C, Borgarelli
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M, editor. Manuale di cardiologia del cane e del gatto. Milano: Elsevier; 2012, p. 269-
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[3] Wendelburg KM, Price LL, Burgess KE, Lyons JA, Lew FH, Berg J, Survival time of
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dogs with splenic hemangiosarcoma treated by splenectomy with or without adjuvant
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Association Vol 247, No. 4, August 15, 2015 [4] Ware WA, Hopper DL. Cardiac tumors
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in dogs: 1982-1995. Journal of veterinary internal medicine 1999;13:95-103.
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[4] Detweiler DK and Patterson DF. The prevalence and types of cardiovascular
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disease in dogs. Annals of the New York Academy of Sciences 1965; 127: 481–516. 8
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[5] Ware WA, Hopper DL. Cardiac tumors in dogs: 1982-1995. Journal of veterinary
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[6] Brown NO, Patnaik AK, MacEwen EG. Canine hemangiosarcoma: retrospective
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[7] Srebernik N, Appleby EC. Breed prevalence and sites of haemangioma and
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haemangiosarcoma in dogs. The Veterinary record 1991;129;408-409.
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[8] Yamamoto S, Hoshi K, Hirakawa A, et al. Epidemiological, clinical and pathological
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features of primary cardiac hemangiosarcoma in dogs: a review of 51 cases. The
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[9] Rajagopalan V, Jesty SA, Craig LE, et al. Comparison of presumptive
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echocardiographic and definitive diagnoses of cardiac tumors in dogs. Journal of
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veterinary internal medicine 2013;27;1092-1096.
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[10] Dunning D, Monnet E, Orton EC, et al. Analysis of prognostic indicators for dogs
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with pericardial effusion: 46 cases (1985-1996). Journal of the American Veterinary
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[11] Weisse C, Soares N, Beal MW, et al. Survival times in dogs with right atrial
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hemangiosarcoma treated by means of surgical resection with or without adjuvant
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chemotherapy: 23 cases (1986-2000). Journal of the American Veterinary Medical
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Association 2005;226;575-579.
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[12] Aronsohn M. Cardiac hemangiosarcoma in the dog: a review of 38 cases. Journal
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of the American Veterinary Medical Association 1985;187;922-926.
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[13] Yamamoto S, Hoshi K, Hirakawa A, et al. Epidemiological, clinical and pathological
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features of primary cardiac hemangiosarcoma in dogs: a review of 51 cases. The
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Journal of veterinary medical science 2013;75;1433-1441.
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[14] Asch FM, Bieganski SP, Panza JA, Weissman NJ. Real-time 3-dimensional
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2006;23(3):218-24. [15] Suresh R, Boor PJ, Al-Dossari GA, et al. Utility of real-time
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three-dimensional echocardiography in improved assessment of a mitral valve papillary
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fibroelastoma. Clinical case reports 2017;5;1193-1195.
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[16] Muller S, Feuchtner G, Bonatti J, et al. Value of transesophageal 3D
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echocardiography as an adjunct to conventional 2D imaging in preoperative evaluation
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of cardiac masses. Echocardiography (Mount Kisco, NY) 2008;25;624-631.
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[17] Garg N, Kapur KK, Ganjoo A, et al. Case report: a rare case of pedunculated LV
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hemangioma evaluated by 3D echocardiography and compared with myxoma.
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[18] LeBlanc NL, Scollan KF. Quantification of right ventricular volume measured by use
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of real-time three-dimensional echocardiography and electrocardiography-gated 64-
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slice multidetector computed tomography in healthy dogs. American journal of
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veterinary research 2018;79;404-410.
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[19] Menciotti G, Borgarelli M, Aherne M, et al. Comparison of the mitral valve
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morphologies of Cavalier King Charles Spaniels and dogs of other breeds using 3D
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1569.
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[20] Mai W, Weisse C, Sleeper MM. Cardiac magnetic resonance imaging in normal
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245
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Radiology Association 2010;51;428-435.
evaluation
of
intracardiac
247 248 249 10
masses.
Echocardiography
250
Footnotes
251
a Philips Epiq 7C, Philips SpA Healthcare, Monza (MB), Italy
252
b Philips X5-1, xMATRIX array transducer with PureWave crystal technology, Philips
253
SpA Healthcare, Monza (MB), Italy
254 255 256
Figure 1
257
Two-dimensional transthoracic echocardiography, right parasternal long axis view. The
258
right atrium is collapsed and a mass with mixed echotexture is in contact with the atrial
259
wall and appears to be in continuity with atrioventricular junction. LV: left ventricle; LA:
260
left atrium; TV: tricuspid valve; NPL: neoplasia.
261
Figure 2
262
Real-time three-dimensional transthoracic echocardiographic study of the right atrium
263
and right ventricle. The arrow indicates the tumor appears to be isolated from
264
atrioventricular junction. RV: right ventricle; TV: tricuspid valve; NPL: neoplasia.
265 266
Figure 3
267
Real-time three-dimensional echocardiographic study of the right atrium and the right
268
ventricle. The tricuspid valve is closed and the tumor is located in continuity with the
269
atrial wall. TV: tricuspid valve: RA: right atrium; RV: right ventricle.
270 271
Figure 4
272
Real-time three-dimensional echocardiographic study of the right atrium and the right
273
ventricle during diastolic and systolic phase. The first image (A) is recorded during atrial
274
contraction. Tricuspid valve is open and the tumor is visible near the right atrium. The
275
second image (B) is recorded during atrial diastole. Tricuspid valve is closed and the 11
276
normal internal atrial wall is seen with the outlet of the caudal vena cava. The third
277
image (C) is recorded during atrial diastole. Slight rotation was made for a better view of
278
the inner wall of the right atrium.
279
ventricle; CVC: caudal vena cava; NPL: neoplasia.
TV: tricuspid valve: RA: right atrium; RV: right
280 281 282 283 284 285 Video 1
Two-dimensional view of the neoplasia
Two-dimensional transthoracic echocardiography, apical four chamber view. A large mass with mixed echogenicity is visible located at the level of right atrium. NPL: neoplasia; RV: right ventricle.
Video 2
Real-time threedimensional view of the neoplasia
Real-time three-dimensional echocardiographic study of the right atrium and the right ventricle. The margins of the mass are independent from the atrioventricular junction. The cardiac mass is not always visible and in some
12
phases of the cardiac cycle the right atrial cavity is observed. RV: right ventricle; TV: tricuspid valve; NPL: neoplasia.
286 287 288 289 290 291 292
13