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: DWorley@ColoState.edu (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.

JAAHA.ORG 261

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