CASE REPORTS
Inflow Venous Occlusion for IntracardiacResection of an Occluding Right VentricularTumorDeanna Rae Worley, DACVS-SA, E. Christopher Orton, DACVS, Kevin Thomas Kroner, DVM*
ABSTRACT
Use of normothermic venous inflow occlusion enabled removal of an intracardiac tumor in a 4 yr old, 27 kg, spayed
female Airedale terrier with a history of appendicular osteosarcoma and recent exertional syncope. Inflow venous
occlusion via a median sternotomy thoracotomy without hypothermia was used to access the mineralized mass within
the right ventricular outflow tract. Duration of circulatory arrest was 70 s for this beating heart surgery. A circumscribed
intracardiac chondrosarcoma tumor was marginally resected in this dog, successfully alleviating exertional syncope and
restoring a normal echogenic appearance of the right heart. Asymptomatic intracardiac chondrosarcoma recurrence
and pulmonary metastasis was detected at 309 days and cardiopulmonary arrest occurred 372 days following
intracardiac surgery. Use of inflow occlusion is a viable technique for select intracardiac tumors in dogs with
preoperative planning. (J Am Anim Hosp Assoc 2016; 52:259–264. DOI 10.5326/JAAHA-MS-6318)
IntroductionThe prevalence of intracardiac neoplasia is well established in
veterinary medicine.1–3,10–18 The most common types of cardiac
neoplasia include hemangiosarcoma, chemodectoma, ectopic thyroid
carcinoma, and lymphoma.3,12,16,17 The location of the mass within
the heart, size of the mass, and invasiveness determines the symptoms
and the potential options for treatment. Clinical signs associated with
right ventricular outflow tract obstructions are variable, but they can
include exertional syncope, congestive heart failure, and anasarca.1,18
The removal of intracardiac masses has frequently been described
using techniques of cardiopulmonary bypass and systemic hypother-
mia.6 Cardiopulmonary bypass surgery uses an extracorporeal system
to provide oxygenated blood to the lungs and tissues with the aid of
hypothermia induced bradycardia or cardiac arrest.19 The benefits of
this technique are that it allows for extended time periods of open-
heart surgery and that it provides a motionless and clean operative
field.19 The drawbacks of this procedure include hemodilution,
initiation of a systemic inflammatory response, coagulatory derange-
ment from thrombocytopenia, acquired platelet dysfunction, dilu-
tional coagulopathy, and hemorrhage. In addition, it requires the
availability and use of specialized and expensive equipment, advanced
monitoring, and an extensive surgical team.5 Deep hypothermia
involves inducing an ambient body temperature between 218 and
388C.5 The problems associated with this procedure are related to the
detrimental effects on the cardiac myofibers, which are subjected to
low temperatures and include ischemic necrosis and hypoxic
damage.19 The use of inflow occlusion in removing intracardiac
masses poses a feasible alternative to such techniques without the
need for extracorporeal systems and systemic hypothermia. The
principle advantages are the simplicity; the lack of need for specialized
equipment; and the minimal cardiopulmonary, metabolic, and
hematologic derangements after surgery.2,9 Limitations of this
procedure are related to the brief period of access to the intracardiac
structures while performing surgery on a beating heart; a total
duration of 4 to 8 min has previously been described for total venous
From the Department of Clinical Sciences (D.R.W., E.C.O.), Flint
Animal Cancer Center (D.R.W.), and Veterinary Teaching Hospital
(K.T.K.), Colorado State University, Fort Collins, CO.
Correspondence: [email protected] (D.R.W.)
The online version of this article (available at www.jaaha.org) contains
supplementary data in the form of one video.
*K. T. Kroner’s present affiliation is School of Veterinary Medicine,
University of Wisconsin–Madison, Madison, WI.
Q 2016 by American Animal Hospital Association JAAHA.ORG 259
inflow occlusion in dogs.2 In addition, there is the possibility of
significant hemorrhage if the entry incision is not closed swiftly or if
there is inadequate occlusion of the azygous or caudal vena cava
vessels. Use of inflow occlusion for removal of right ventricular
cardiac tumors has been reported, but those prior cases were aided
with the use of hypothermia techniques and cardioplegic solu-
tion.4,8,18 We report the use of inflow occlusion for removal of an
obstructing right ventricular tumor without the use of intentional
hypothermia or of cardioplegic solution.
Case ReportA 4 yr old intact female Airedale terrier presented for acute weakness,
fatigue, trembling, and collapse. An evaluation through a referral
center revealed a grade IV/VI systolic murmur and a large
intracardiac mass in the right ventricular outflow tract identified
with echocardiography. The dog was started on clopidogrel and
sildenafil with marked improvement of clinical signs. One week
following onset of clinical signs the dog was presented to the authors’
institution. Ten mo ago, the dog was treated for a chondroblastic
osteosarcoma in the right distal femur, at the same institution, with
hindlimb coxofemoral disarticulation amputation and adjuvant
chemotherapy of carboplatin, gemcitabine, and doxorubicin.
Three-view thoracic radiographs revealed a focal area of
stippled mineralization superimposed over the right ventricle and
just to the left of midline superimposed over the cardiac silhouette
at the level of the fourth intercostal space (Figure 1). The
pulmonary vasculature, mediastinal structures, and pleural space
appeared normal with no evidence of visible metastasis. Echocar-
diogram revealed a mineralized right ventricular mass causing
obstruction to the outflow tract with associated left ventricular
pseudohypertrophy and ventricular ectopy (Figure 2). The mass
appeared to extend from the tricuspid valve and invade the
interventricular septum. Thoracic and abdominal computed
tomography with arterial, venous, and delayed contrast imaging
revealed an ovoid, well-demarcated, mixed attenuating mass with
internal granular osseous attenuating regions within the right
ventricular outflow tract (Figure 3). The mass measured approx-
imately 6.0 cm x 3.0 cm and was well visualized as a filling defect on
FIGURE 1 Mineralized mass present within the right heart on a
left lateral thoracic radiograph. Arrow denotes mass.
FIGURE 2 Echodense mass within the right ventricular outflow
tract with acoustic shadowing as seen on a transverse two-dimensional
echocardiography through the ventricles. Arrow denotes mass.
FIGURE 3 Space occupying circumscribed mass within the right
ventricular outflow tract outlined on an arterial phase contrast
computed tomographic study. Arrow denotes mass.
260 JAAHA | 52:4 Jul/Aug 2016
arterial and venous phases. There was also a soft tissue attenuating,
multifocal, interstitial-to-mild alveolar pattern within the mid-to-
ventral aspect of the right cranial lung lobes, ventral aspect of the
cranial subsegment of the left cranial lung lobe, ventral aspect of
the right middle lung lobe, and ventral aspect of the caudal
subsegment of the left cranial lung lobe. As there was no evidence
of pulmonary metastasis or abdominal organ abnormalities and
taking into consideration the nature and location of the mass, the
decision was made to pursue surgical resection of the intracardiac
mass. Without attempt to relieve the physical obstruction within
the heart, the short-term prognosis was grave for this symptomatic
dog.
During the procedure, a median sternotomy approach was
made to access the heart. After blunt dissection, the azygous,
cranial, and caudal vena cava were isolated using preplaced loosely
encircling 1 silk suture and 12 Fr red rubber Rommel tourniquets
(Figure 4). The pericardium was incised longitudinally and
retracted from the apex of the heart to the heart base. The
pericardium was sutured to the surrounding pectoralis muscles
using 2-0 coated braided polyestera as stay sutures. The heart and
right ventricular mass were palpated for preparation of incision
and four stay sutures of 2-0 coated braided polyester were placed
along the proposed incision line (Supplementary Video I). The
Rommel tourniquets were secured. A linear incision was made
along the right ventricle with a 10-blade scalpel. Once the right
ventricular outflow tract was incised, a large, approximately 1.5 3 3
cm, calcified, irregular mass at the right ventricular free wall below
the pulmonic valve annulus was briskly exteriorized and freed from
a narrow base using tangential vascular clamps and bone cutting
forceps (Figure 5). Once the mass was marginally excised, the
incision in the ventricle was loosely apposed with tangential
vascular forceps and flow to the heart was restored by removing the
red rubber catheters and silk sutures around the great veins. Air
was removed from the heart by administering a large breath,
loosening the tangential vascular forceps, and maintaining positive
the pressure in the lungs while the heart continued to beat, just
long enough to permit displacement of intracardiac air and to
minimize blood loss. The tangential vascular forceps were replaced
on the right ventricle, allowing internal flow and simultaneous
hemostasis. Total time of inflow occlusion was 70 s. The heart was
closed with medium sized pledgetsb on double-armed 4-0
polypropylenec with simple interrupted horizontal mattress sutures
(Figure 6). The incision was oversewn with a simple continuous
pattern of 2-0 coated braided polyester (Figure 7; Supplementary
Video I). The stay sutures were removed from the pericardium and
it was loosely apposed using 2-0 coated braided polyester to allow
for drainage while avoiding any herniation or tamponade. There
was a small area of the right cranial lung that experienced mild
iatrogenic air leakage, which was effectively repaired with a
thoracoabdominal stapler using vascular staplesd for a subtotal
lobectomy. A 20-fr chest tube was placed exiting the right lateral
thorax at the eighth intercostal space. The mediastinum, sternum,
and soft tissues were closed routinely. The dog recovered from the
procedure with no postoperative complications and was discharged
2 days postoperatively. Following surgery, adjuvant radiation
therapy was recommended, but it was not pursued since tumor
FIGURE 4 Preplaced Rommel tourniquets on the vena cava and
azygous vein and pericardial sling prior to surgical approach to the
right ventricular outflow tract. Patient orientation is cranial to the left
and caudal to the right. Arrows denote Rommel tourniquets.
FIGURE 5 Ex vivo chondrosarcoma resected from the right
ventricular outflow tract.
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Inflow Occlusion for Intracardiac Sarcoma Resection
resection was incomplete. Histopathology of the extirpated mass
revealed a grade 2 chondrosarcoma with neoplastic cells extending
into the natural tissue margins. This tumor was determined to be
histopathologically distinct from the chondroblastic osteosarcoma
diagnosed in the right distal femur. Recheck echocardiogram
completed 2 wk postoperatively revealed normal cardiac structures
and no evidence of any mass or outflow tract obstruction (Figure
8). Physical examination and thoracic radiographs were unremark-
able (Figure 9). A complete return to normal activity level was
noted by the owners, despite recommendation for longer
rehabilitation. Thoracic radiographs, echocardiograms, and phys-
ical examinations were recommended to occur every 2–3 mo for
disease monitoring. As the dog continued to be asymptomatic, the
owners delayed reevaluation until 309 days postoperatively, at
which point a recurrent mineralized mass, measuring 2.4 cm 3 2.2
cm with echocardiography, was detected in the right ventricular
outflow tract as well as a solitary pulmonary metastasis on thoracic
radiographs. Two mo later the dog exhibited progressive exertional
fatigue and collapse. The dog presented to the institution with
pronounced exertional fatigue and collapse and experienced fatal
cardiovascular arrest prior to any second thoracotomy attempt 372
days after cardiac surgery. Necropsy findings supported a cause of
FIGURE 6 Simple continuous oversew on the right ventricular
free wall following tumor removal. Pledgeted mattress sutures were
placed prior to removal of a tangential clamp. Patient orientation is
cranial to the left and caudal to the right.
FIGURE 7 Final appearance of the cardiotomy prior to
reapposition of the pericardium. Patient orientation is cranial to the
left and caudal to the right.
FIGURE 8 Two wk postoperative transverse two-dimensional
echocardiography through the ventricles with no visible echodense
mass within the right ventricular outflow tract.
FIGURE 9 Two wk postoperative image demonstrating absence of
a mineralized mass within the right heart on a left lateral thoracic
radiograph.
262 JAAHA | 52:4 Jul/Aug 2016
death due to recurrent chondrosarcoma at the right ventricle with
metastasis to kidney and lungs (Figure 10).
DiscussionThe use of cardiopulmonary bypass is well described in veterinary
medicine and, although there are many indications for the
procedure, the potential complications warrant investigation of
alternative techniques in certain circumstances.5 This case exem-
plifies the novel application of non-bypass inflow occlusion as an
acceptable technique for the removal of a right ventricular outflow
tract obstruction. The reported decrease in postoperative compli-
cation rates and recovery times, as well as lower surgical costs,
makes inflow occlusion an appealing alternative to cardiopulmo-
nary bypass. There were minimal intraoperative and postoperative
complications associated with this procedure and it resulted in the
successful removal of the mass with durable palliation postoper-
atively. Potential risks that could have been encountered in this
procedure include: (1) a cardiac mass that may not have been
resectable; (2) brain hypoxemia and/or cardiac arrest if inflow
occlusion exceeded an estimated 4 min or a heart that did not
respond following occlusion; (3) intracardiac visualization reveal-
ing the mass to actually involve cordae tendineae, the tricuspid
valve, intraventricular septum, or aortic wall; (4) iatrogenic bundle
branch block if the bundle of His were incised; (5) an intracardiac
hole if too deep of a resection was made for tumor removal; (6) air
embolism; or (7) massive intraoperative blood loss. Other
previously described techniques utilized to remove masses within
the right ventricle without the need for cardiopulmonary bypass
include the use of cardiopledgia solution, aortic cross clamping,
and systemic hypothermia.4 In addition to the absence of
cardioplegia, intentional hypothermia, and aortic cross clamping,
the surgical approach through the ventricle is a unique attribute of
this technique with previously described approaches involving the
pulmonary artery and right atrium.1,8,11 The necessity for cardiac
arrest in other procedures increases the risk of surgical complica-
tions, such as reperfusion injury, hypoxemia, hemorrhage,
thrombosis formation, and failure to successfully restart the heart.
In comparison, recent studies completed have reported decreased
rates of hemodynamic, metabolic, and neurologic complications in
dogs undergoing total venous occlusion.7,9,19 Similar comparisons
between cardiopulmonary bypass procedures and inflow occlusion
in human medicine have concluded less patient morbidity related
to inflow occlusion and a decrease in the use of blood transfusion
with this procedure.9 In addition to these potential patient benefits,
the required materials for inflow occlusion are more readily
accessible when compared to cardiopulmonary bypass, making its
application more realistic for more surgeons.
The histopathologic finding of chondrosarcoma and location
of the mass within the right ventricle are of clinical significance as it
indicates two distinct primary malignant neoplasms occurring in a
middle-aged dog. Primary cardiac chondrosarcoma is rare in
veterinary medicine and canine chondrosarcoma normally occurs
in locations on the appendicular skeleton, but the presence in
several other sites has been reported with an incidence of 1–13%.20
This tumor likely arises from the cartilaginous tissues that compose
the cardiac skeleton, such as the valves or chordae tendineae, but it
may also arise from primitive mesenchymal cell differentiation of
several tissue types.20,21
Cardiac surgery requires a therapeutic approach tailored to an
individual patient. Proper presurgical planning and case selection
are critical when considering the use of total venous inflow
occlusion to intracardiac mass removal. Advanced imaging, such as
computed tomography, magnetic resonance, and echocardiogra-
phy, are valuable modalities for determining resectability of masses
in such procedures.5,18 The combination of echocardiography and
computed tomography provided vital information in identifying
the precise location of this mass within the right ventricular
outflow tract and aided in surgical planning.
ConclusionThis case report offers another option for removal of right ventricular
outflow tract masses with minimal resulting complication. The
decreased morbidity and simplicity of inflow occlusion make this
technique an appealing alternative to conventional cardiopulmonary
bypass for intracardiac mass removal in select patients.
VIDEO I Intraoperative video of right ventricular outflow tract being
prepared for incision, removal of the intracardiac chondrosarcoma, de-
airing of the heart, and ventricular wall closure. Patient orientation is
cranial to the top and caudal to the bottom of the image.
FIGURE 10 Postmortem images of the intracardiac mass from
necropsy.
JAAHA.ORG 263
Inflow Occlusion for Intracardiac Sarcoma Resection
FOOTNOTESa
Ti�Cron; Covidien, Mansfield, MAb
PTFE polymer pledgets (3 mm x 7 mm x 1.5 mm); Covidien, Mansfield,
MAc
Surgipro II; Covidien, Mansfield, MAd
TA premium 30 V3 (2.5 mm) single loading unit; Covidien, Mansfield,
MA
REFERENCES
1. Bright JM, Toal RL, Blackford LA. Right ventricular outflow
obstruction caused by primary cardiac neoplasia. Clinical features in
two dogs. J Vet Intern Med 1990;4:12–16.
2. Hunt GB, Malik R, Bellenger CR, et al. Total venous inflow occlusion in
the normothermic dog: a study of haemodynamic, metabolic and
neurological consequences. Res Vet Sci 1992;52:371–7.
3. Hayashi S, Isobe M, Hayashi M, et al. Successful resection of
intracardiac invasive thymoma with right ventricular inflow tract
occlusion. Internal Medicine 2000;39:139–42.
4. Rioja E, Beaulieu K, Holmberg DL. Anesthetic management of an off-
pump open-heart surgery in a dog. Veterinary Anaesthesia and
Analgesia 2009;36:361–8.
5. Kanemoto I, Taguchi D, Yokoyama S, et al. Open heart surgery with
deep hypothermia and cardiopulmonary bypass in small and toy dogs.
Vet Surg 2010;39:674–9.
6. Uechi M, Mizukoshi T, Mizuno T, et al. Mitral valve repair under
cardiopulmonary bypass in small-breed dogs: 48 cases (2006-2009). J
Am Vet Med Assoc 2012;240:1194–1201.
7. Singh J, Dhaliwal RS, Biswal S, et al. Inflow occlusion in the era of
modern cardiac surgery. J Thorac Cardiovasc Surg 2006;132:1246–7.
8. Gordon SG, Nelson DA, Achen SE, et al. Open heart closure of an atrial
septal defect by use of an atrial septal occluder in a dog. J Am Vet Med
Assoc 2010;236:434–9.
9. Gokalp O, Yurekli I, Yilik L, et al. Comparison of inflow occlusion on
the beating heart with cardiopulmonary bypass in the extraction of a
mass lesion or a foreign body from the right heart. Eur J Cardiothorac
Surg 2011;39:689–92.
10. Schelling SH, Moses BL. Primary intracardiac osteosarcoma in a dog. J
Vet Diagn Invest 1994;6:396–8.
11. Warman SM, McGregor R, Fews D, et al. Congestive heart failure
caused by intracardiac tumours in two dogs. J Small Anim Pract 2006;
47:480–3.
12. Almes KM, Heaney AM, Andrews GA. Intracardiac ectopic thyroid
carcinosarcoma in a dog. Vet Pathol 2008;45:500–4.
13. Bracha S, Caron I, Holmberg DL, et al. Ectopic thyroid carcinoma
causing right ventricular outflow tract obstruction in a dog. J Am Anim
Hosp Assoc 2009;45:138–41.
14. Boes K, Messick J, Green H, et al. What is your diagnosis? Impression
smear from an intracardiac mass in a dog. Vet Clin Pathol 2010;39:119–
20.
15. Di Palma S, Lombard C, Kappeler A, et al. Intracardiac ectopic thyroid
adenoma in a dog. Vet Rec 2010;167:709–10.
16. Thompson DJ, Cave NJ, Scrimgeour AB, et al. Haemangiosarcoma of
the interventricular septum in a dog. N Z Vet J 2011;59:332–6.
17. Ware WA, Hopper DL. Cardiac tumors in dogs: 1982-1995. J Vet Intern
Med 1999;13:95–103.
18. Chanoit G, Mathews KG, Keene BW, et al. Surgical treatment of a
pulmonary artery vascular hamartoma in a dog. J Am Vet Med Assoc
2012;240:858–62.
19. Orton EC. Cardiac Surgery In: Tobias KM,Johnston SA, eds. Veterinary
Surgery: Small Animal. 1st ed. St. Louis: Elsevier Saunders; 2012:1813–
44.
20. Cohen L, Dank G, Milgram J. Non-skeletal multicentric chondrosar-
coma in the hindlimb of a dog. J Small Anim Pract 2010;51:553–7.
21. Albers TM, Alroy J, Garrod LA, et al. Histochemical and ultrastructural
characterization of primary cardiac chondrosarcoma. Vet Pathol 1997;
34:150–1.
264 JAAHA | 52:4 Jul/Aug 2016