Cardiol Ther (2018) 7:107–117 https://doi.org/10.1007/s40119-018-0109-y CASE REPORT Pulmonary Embolism Following Incomplete Surgical Resection of a Right Ventricular Myxoma: A Case Report and Review of the Literature . . . Yazan Assaf Maher Nasser Hani Jneid David Ott Received: January 18, 2018 / Published online: April 17, 2018 The Author(s) 2018 Abstract: Right ventricular (RV) myxomas are Five months after surgery, the patient had PE, extremely rare, but may have dreadful clinical which could be due to tumor emboli or sequelae including pulmonary embolism (PE). thromboemboli. Since repeat surgical resection We present a case of a patient who had an RV was not feasible, the patient was started on myxoma that was attached to the tricuspid warfarin. The patient is doing well and has had valve, and therefore could not be resected no PE recurrence over the past 20 months of completely during surgery, and remnants of the follow-up. We have complemented the current tumor were seen on transthoracic echocardio- case report with a comprehensive literature gram during post-operative follow-up. search and review on RV myxomas associated with PE in order to shed light on this uncom- mon but potentially lethal disorder. We con- Enhanced digital features To view enhanced digital cluded that right-sided cardiac myxomas, features for this article go to https://doi.org/10.6084/ including RV myxomas, should be considered m9.ﬁgshare.6061451. while dealing with PE, particularly in young patients with no risk factors, and that follow-up Y. Assaf (&) with echocardiography after surgery is impor- Faculty of Medicine, Damascus University, tant due to the possibility of recurrence, espe- Damascus, Syria e-mail: email@example.com cially if complete resection was difﬁcult to perform. M. Nasser H. Jneid D. Ott Plain Language Summary: Plain language Baylor College of Medicine, Houston, TX, USA summary available for this article. M. Nasser Baylor St. Luke’s Medical Center, Houston, TX, USA Keywords: Myxoma; Pulmonary embolism; M. Nasser D. Ott Right ventricle; Right ventricular myxoma Texas Heart Institute, Houston, TX, USA M. Nasser Houston Methodist Hospital, Houston, TX, USA PLAIN LANGUAGE SUMMARY H. Jneid Myxomas are a type of tumor that may occur Michael E. DeBakey Veterans Affairs Medical Center, inside heart chambers. Myxomas located in the Houston, TX, USA right lower chamber of the heart (right ventri- D. Ott cle) are very rare. However, such tumors may University of Texas Health Science Center at fragment and travel to the lung blood vessels. Houston, Houston, TX, USA 108 Cardiol Ther (2018) 7:107–117 The patient in our case had a myxoma in the which he takes albuterol and cetirizine, pre- right ventricle. The tumor was attached to a sented to a cardiology clinic with shortness of valve in the heart. Partial removal of the tumor breath and palpitations for the last 3 months. was performed so as not to damage the valve. The patient reported feeling ‘the heart rubbing Imaging after surgery showed remaining parts against the chest while leaning forward’. He of the tumor. Five months later, the patient had denied chest discomfort or other cardiac symp- clots in the lung blood vessels (pulmonary toms. After auscultating his own chest, he heard embolism). The patient was treated with a blood a murmur for which he sought medical advice. thinner. He is doing well since then. We sear- Physical exam was normal except for a low- ched the medical literature for cases of myxo- grade holosystolic murmur best heard at the left mas in the right ventricle of the heart associated lower sternal border, tachycardia and tachypnea with pulmonary embolism. We present a review with a respiratory rate of 25. Electrocardiogram of these cases along with our case. We con- (ECG) showed sinus tachycardia with a heart cluded that myxomas of the right ventricle of rate of 112 beats per minute and right axis the heart may be considered as a cause of pul- deviation. Transthoracic echocardiogram (TTE) monary embolism. This is particularly true in revealed an RV mass (approximately 3 9 2 cm) young patients who do not have risk factors for attached to the interventricular septum by a pulmonary embolism. Our review also shows small pedicle, dilated right heart chambers, that imaging after surgery is important because moderate tricuspid regurgitation, and severe myxomas may recur. pulmonary hypertension (systolic pulmonary artery pressure [ 60 mmHg) (Fig. 1). Cardiac magnetic resonance (MR) conﬁrmed the pres- INTRODUCTION ence of a well-circumscribed non-obstructive mass (2.4 9 1.9 9 1.2 cm) that appeared not to Primary cardiac tumors are infrequent . invade the surrounding cardiac structures loca- Myxoma is the most common type of such ted in the RV outﬂow tract, inferior to the pul- tumor in adults . Most myxomas arise in monary valve (Fig. 2). The patient denied a the left atrium. Those located in the right family history of cardiac tumors. ventricle are rare , and they are of a par- The patient underwent open heart surgery ticular concern because of the risk of pul- with median sternotomy and total cardiopul- monary tumor embolism. Right ventricular monary bypass. Right ventriculotomy was per- (RV) myxomas accompanied by pulmonary formed, and the incision was extended embolism (PE) are reported only in a limited superiorly and inferiorly. Traction sutures were number of studies in the medical literature placed on the right ventricle in order to [4–14]. Herein, we present a case of a young improve exposure. A large and soft RV mass man who suffered from PE after incomplete obstructing the RV outﬂow tract was identiﬁed surgical resection of an RV myxoma. To the in the right ventricle attached to the anterosu- best of our knowledge, this is the ﬁrst report perior and septal leaﬂets of the tricuspid valve in the literature of conﬁrmed PE following and partially attached to the interventricular incomplete surgical resection of an RV myx- septum. Based on the surgeon’s decision, the oma. We also present a review of the literature mass was partially excised without compromis- pertaining to RV myxomas associated with PE ing the integrity of the tricuspid valve (Fig. 3). in an effort to provide an insightful under- TEE was used to evaluate the valve function and standing of such cases. revealed mild tricuspid regurgitation. The patient had uneventful surgical recovery and was discharged following a 5-day hospitaliza- CASE PRESENTATION tion period. The pathology report of the resected mass A 28-year-old male physician with no signiﬁ- (two specimens) conﬁrmed the diagnosis of cant past medical history except for asthma, for myxoma. The ﬁrst specimen consisted of three Cardiol Ther (2018) 7:107–117 109 Fig. 1 Transthoracic echocardiogram (TTE) views before surgery showing a right ventricular mass (approximately 3 9 2 cm) attached to the interventricular septum by a small pedicle and dilated right heart chambers Fig. 2 Cardiac magnetic resonance (MR) before surgery Fig. 3 The resected myxoma (predominantly tan–red revealing a well-circumscribed non-obstructive mass with focal yellow tissue measuring about 4 9 3 9 (2.4 9 1.9 9 1.2 cm) that appeared not to invade the 1.5 cm) surrounding cardiac structures located in the right ventricular outﬂow tract, inferior to the pulmonary valve Sectioning revealed a gray–white to yel- low–green, rubbery and friable cut surface. No fragments of tissue measuring 1.3 9 1 9 0.5 cm ﬁrm areas were identiﬁed. Microscopically, the in aggregate. One portion of tissue had a tan– majority of the ﬁrst specimen consisted of ﬁbrin white base with tan–red tissue attached and clot. There was a fragment of bland polygonal projecting from the base. Another portion of to spindle-shaped cells within a myxoid matrix. tissue was predominately tan–red with focal Factor VIII showed focal positivity within the yellow tissue, reminiscent of adipose tissue. The bland cells and was positive in capillaries. CD34 third portion of tissue was tan–red. The second was positive in capillaries. No entrapped cores specimen was an aggregate of pink–tan to of elastic tissue were seen on Verhoeff-Van gray–white, rubbery, ragged, and soft tissue Gieson stain (elastin stain). Trichrome stain fragments measuring 3.5 9 3.5 9 1.5 cm. 110 Cardiol Ther (2018) 7:107–117 elevated (0.9 mg/l). His chest X-ray was normal. A chest computerized tomography (CT) scan revealed multiple emboli in the right lower lobe segmental and subsegmental pulmonary arterial branches, as well as peripheral airspace disease in the right lower lobe suggestive of pulmonary infarction (Fig. 4). Venous Doppler ultrasound of the legs showed bilateral patent and com- pressible venous systems and no evidence of thrombus. TTE and transesophageal echocar- diogram (TEE) were done and reported dilation of the inferior vena cava (IVC), right atrium and right ventricle and a mass (approximately 2 9 1.5 cm) attached to the base of the RV wall just below the insertion of the anterior tricuspid leaﬂet (Fig. 5). The tricuspid jet was insufﬁcient Fig. 4 Chest computerized tomography (CT) after sur- to calculate pulmonary pressure. Cardiac MR gery scan showing multiple emboli in the right lower lobe showed a small residual tissue (9 9 9 mm) segmental and subsegmental pulmonary arterial branches, adjacent to the interventricular septum and as well as peripheral airspace disease in the right lower lobe another residual tissue (7 9 9 mm) attached to suggestive of pulmonary infarction the RV free wall (Fig. 6). The patient was diag- nosed with PE, due to either tumor emboli or showed no laminated elastic ﬁbers within the thromboemboli, and was started on warfarin. matrix. The morphologic and immunohisto- On further follow-up (20 months following PE), chemical ﬁndings were compatible with cardiac he had no recurrent PE. myxoma. The microscopic examination of the Informed consent was obtained from the second specimen showed myxoma cells with an patient for being included in the study. oval nucleus which were forming ring structures around small thin-walled blood vessels. An accompanying mononuclear inﬂammatory cell inﬁltrate was present. Hemosiderin-laden mac- rophages were also present. A myxoid back- ground was focally present. The majority of the tissue showed secondary changes of ﬁbrosis and calciﬁcation which obscured the underlying nature of the lesion. The myxoma was attached to a portion of benign cardiac muscle. Two weeks after surgery, a follow-up TTE showed a residual RV mass (approximately 2 9 1.5 cm) attached to the interventricular septum. Five months after surgery, the patient pre- sented to the emergency department with right- sided pleuritic chest pain and upper abdominal discomfort. The patient took 15 airplane ﬂights Fig. 5 Transesophageal echocardiogram (TEE) after sur- over the previous 2 months, some of which gery revealing dilation of the inferior vena cava (IVC), were very long. He was tachypneic (22 breaths/ right atrium and right ventricle and a mass (approximately min), and his ECG showed sinus tachycardia 2 9 1.5 cm) attached to the base of the right ventricular with a heart rate of 118 bpm and right bundle wall just below the insertion of the anterior tricuspid branch block (RBBB). Serum D-dimer was leaﬂet Cardiol Ther (2018) 7:107–117 111 Fig. 6 Cardiac magnetic resonance (MR) views after surgery showing a small residual tissue (9 9 9 mm) adjacent to the interventricular septum and another residual tissue (7 9 9 mm) attached to the right ventricular free wall after excising the mass. We think that the mass DISCUSSION was distorting the tricuspid valve. Most cardiac myxomas are sporadic. Only In the 18th century, the French physician, De- about 7% of them are hereditary and occur Senac, stated, ‘‘The heart is an organ too noble along with skin pigmentation and to be attacked by a primary tumor’’ [15, 16]. We endocrinopathy in an autosomal dominant now know that primary tumors of the heart do disorder called Carney Complex . Our exist, although they are rare with a frequency of patient denied any family history of cardiac just about 0.02% . Secondary tumors of the tumors. heart are approximately 30-fold more common Three-quarters of cardiac myxomas are loca- than primary ones . Around 75% of primary ted in the left atrium. Most of the rest occur in cardiac tumors are benign. Myxomas, which the right atrium. RV myxomas were reported in constitute about half of the benign cardiac just 3–4% of cardiac myxoma cases . Myxo- tumors, are the most common primary tumors mas range between 1 and 15 cm in diameter of the heart in adults, while rhabdomyomas weighing between 15 and 180 g . Cardiac predominate in children [2, 18]. Myxomas are myxomas are usually pedunculated and have a more common in women and are usually diag- smooth, villous or friable surface. Smooth nosed between the third and sixth decades of myxomas are known for obstructive complica- life . Both TTE and TEE play important roles tions, whereas villous and friable ones tend to in the initial diagnosis of cardiac myxomas, cause embolic complications . The myxoma with CT and cardiac MR being supplemental in the case we are presenting was friable . It was remarkable that preoperative TTE in according to the pathology report. This, in our case revealed severe pulmonary hyperten- addition to the absence of deep vein thrombo- sion. We believe that could be due to recurrent sis, favors the diagnosis of tumor emboli in our pulmonary emboli that went unnoticeable. patient. Postoperative TTE in our case revealed dilation Location, size, and mobility of cardiac myx- of the IVC, right atrium and right ventricle, omas determine their clinical presentation. which we believe could be due to the mild TR Embolism, obstruction, and constitutional revealed on the TEE done during the surgery symptoms are common manifestations. 112 Cardiol Ther (2018) 7:107–117 Embolism occurs in 30–40% of cases. Systemic right-sided chambers, is safe and can accurately embolism is much more common than PE, as provide histopathological diagnosis. Such an most myxomas are predominantly located in approach may therefore mitigate the need for the left atrium. Only few cases of RV myxomas surgical excisional biopsy and potentially alter associated with PE were reported [4–14]. clinical management in a large number of Once a cardiac myxoma is diagnosed, it patients . should be surgically resected to avoid its asso- We conducted a search of published cases ciated complications. Recurrence rate is less describing RV myxomas associated with PE in than 3% in sporadic cases, but ranges between PubMed using the following search terms: pul- 12 and 22% in familial ones. Factors associated monary embolism, myxoma, ventricular, right with recurrence include multicentricity, young ventricular myxoma. The search yielded 29 age, familial cases, and incomplete surgical articles, 11 of which were pertaining to RV resection. Follow-up is usually done after sur- myxomas associated with PE. We present a gery using echocardiography . In our case, review of these 11 cases along with the case we the tumor could not be completely resected due are presenting (Table 1). to its attachment to the tricuspid valve. The oldest case was published in 1971 , Pulmonary tumor emboli and thromboem- and the most recent one, apart from ours, in boli are not easily differentiable. CT scans and 2016 . Singh el al. reported two cases of car- pulmonary angiograms are often nonspeciﬁc for diac masses in his article, however only one of tumor emboli. Tumor emboli usually display a them was conﬁrmed as a myxoma and included more peripheral distribution in the subseg- in our review . Eight of the 11 cases were mental arteries (as likely occurred in our reported in English language [4–8, 10, 12, 13]. patient) . On the other hand, thromboem- Urina Triana et al. reported their case in Spanish boli are associated with long and multiple air- language. We included it since we could trans- plane ﬂights . Therefore, the fact that the late the entire article . The case reported by patient in the case we are reporting had taken Vernant et al. was in French language. We numerous and long ﬂights before he suffered translated and included the abstract of that from PE raises the possibility that thromboem- article as it was the only part we found . bolism contributed to the PE. Thromboemboli Tatebayashi et al. reported their case in Japanese are also correlated with elevation of serum language. We only included the abstract of that D-dimer , which was high when the PE was article since it was available in English language diagnosed in the case we are reporting. Never- . theless, the elevation in D-dimer was slight and The number of male and female patients was lower extremities venous Doppler showed no equal. The mean age of patients was approxi- evidence of thrombi. Pulmonary thromboem- mately 33 years, and while the youngest patient boli are more frequently correlated with higher was 12 years old , the oldest one was 76 serum D-dimer levels . years old . However, most patients were in Conﬁrmation of pulmonary tumor emboli their 20 or 30s. require a lung biopsy procedure, which can be Although the presentation was not the same done with either open-lung or transbronchial for all the cases, eight cases showed that pul- approaches . A deﬁnitive diagnosis of pul- monary embolism could be the ﬁrst presenta- monary tumor emboli through invasive proce- tion of RV myxomas [4–9, 11, 12]. This indicates dures was not pursued in our patient since the signiﬁcance of performing echocardiogra- surgery was already done, and the patient was phy in cases of unexplained PE especially in started on warfarin. The fact that no recurrence young patients who do not have risk factors of of PE happened during the follow-up may favor PE. but does not conﬁrm that the emboli were A summary of the most frequent ﬁndings of thrombotic in origin. the cases in our review, including our case, is Echo-guided percutaneous trans-catheter shown in Table 2. biopsy of intracardiac masses, especially in the Cardiol Ther (2018) 7:107–117 113 Table 1 Review of the literature related to right ventricular myxomas associated with pulmonary embolism including the case we are presenting Case Authors, Age Presentation Vital signs Physical examination ECG Abnormal labs Echocardiogram Follow-up Recurrence Notes no. year of in after surgery publication years, sex 1 Singh et al., 26, F Dyspnea and left Normal BP, Narrow split of S2 Sinus Leukocytosis 2 RA myxomas Yes, No Elevated JVP 2016  precordial pain tachycardia, with loud P2 and a tachycardia and 1 RV echocardiogram with and pan-systolic grade and right myxoma 6 months after prominent ‘v’ tachypnea III/VI murmur axis surgery was wave along LSB deviation normal 2 Ahmad- 26, M Episodes of brisk NA Normal NA NA 2 RV myxomas NA NA All areas affected Zarghami hemoptysis and tumoral by the tumor et al., posterior cusp were removed 2007  of the tricuspid valve 3 Moyassakis 21, M PE and palpitations NA Murmur NA NA RA myxoma and Yes, normal Yes, two Possible et al., RV myxoma recurrences ‘pretumoral 2005  in multiple tissue foci’ locations 4 Segal et al., 34, M Episodes of NA NA NA NA RV myxoma NA Yes Mass was 2000  pleuritic chest densely pain adherent to the RV wall 5 Zuber et al., 27, F PE, weight loss, High BP A grade III/VI systolic Incomplete NA RV myxoma Yes, follow-up of No Long work-up 1997  fatigue, murmur and a thrill RBBB 1 year was and multiple exertional with maximum normal presentations dyspnea, and intensity over the till myxoma recurrent pulmonary region was diagnosed supraventricular arrhythmias 6 Tatebayashi 76, F Cough, dyspnea, NA NA NA High serum IL-6 RV myxoma NA NA Surgery showed et al., and clear RV 1993  constitutional cavity symptoms of myxoma 7 Singh et al., 30, F Breathlessness on Normal BP, Wide split of S2 with Right-axis NA RV myxoma and NA NA 1992  exertion normal HR, a loud P2, a grade deviation ASD and II/VI ejection and RVH tachypnea systolic murmur along the LSB and an RV heave 8 Urina Triana 17, F Pleuritic chest pain Normal HR Slightly loud P2 and a Sinus Microcytic RV myxoma NA No et al., sometimes with and fever grade II/IV systolic tachycardia hypochromic 1987  dry cough, fever, ejection murmur in and anemia, chills, profuse the second and incomplete leukocytosis, sweating and third left intercostal RBBB and high ESR palpitations space 114 Cardiol Ther (2018) 7:107–117 Table 1 continued Case Authors, Age Presentation Vital signs Physical examination ECG Abnormal labs Echocardiogram Follow-up Recurrence Notes no. year of in after surgery publication years, sex 9 Boulafendis 46, M Left-sided chest NA Loud S3, a systolic Sinus NA RV myxoma NA NA et al., pain and SOB murmur with a tachycardia 1984  thrill along LSB, and RVH and a very prominent RV impulse ´ Microcytic RV myxoma Patient died No 10 Gonzalez 12, M SOB, tachypnea, Normal BP, Wide split of S2 with Sinus et al., and cyanosis, and tachycardia, loud P2, a tachycardia hypochromic 1980  episodes of fever, tachypnea midsystolic and anemia, anorexia, and and fever murmur along the incomplete leukocytosis, general malaise LSB and an RV RBBB and high ESR heave 11 Vernant 49, F PE NA NA NA Eosinophilia NA Yes, follow-up of No et al., 20 months was 1971  normal 12 Current 28, M SOB, palpitations, Tachycardia A low-grade Sinus Elevated serum RV myxoma Yes Yes, 2 residual Myxoma was study pleuritic chest and holosystolic tachycardia D-dimer masses after attached to pain and upper tachypnea murmur best heard and right- incomplete the tricuspid abdominal at the left lower axis surgical valve discomfort sternal border deviation resection and RBBB F female, M male, PE pulmonary embolism, SOB shortness of breath, BP blood pressure in mm Hg, HR heart rate in beats per minute, T temperature in Celsius, S2 second heart sound, P2 pulmonic component of the second heart sound, LSB left sternal border, RBBB right bundle branch block, RA right atrial, RV right ventricular, RVH right ventricular hypertrophy, IL-6 interleukin-6, ESR erythrocyte sedimentation rate, ASD atrial septal defect, JVP jugular venous pressure, NA data not available Cardiol Ther (2018) 7:107–117 115 Table 2 Most frequent ﬁndings of the cases in the review atrial mass and one RV mass in the third one , of literature including our case and one RV myxoma and atrial septal defect in the fourth one . Finding No. of cases that reported Recurrence of myxoma after surgical resec- the ﬁnding tion happened in the case reported by Moyas- Signs and symptoms sakis et al. Therefore, the patient underwent a a second surgical resection, after which recur- SOB 7 [4, 8–10, 12, 13] rence happened again . Segal et al. reported a CP 5 [4, 7, 11, 12] case in which the mass was densely adherent to the wall of the right ventricle. Surgical resection Palpitations 3 [6, 11] was performed, however recurrence occurred Vital signs . These two cases in addition to the case we are presenting show that recurrence of myxo- Tachypnea 4 [4, 10, 13] mas may happen. Recurrence seems to occur Tachycardia 3 [4, 13] particularly when complete resection of the Fever 2 [11, 13] mass is not possible. This emphasizes the importance of the follow-up including Physical examination echocardiography after surgery. It was Murmur 8 [4, 6, 8, 10–13] notable that only four of the 11 cases we reviewed reported follow-up [4, 6, 8, 14]. Loud P2 4 [4, 10, 11, 13] Zuber et al. reported a patient who presented RV heave 3 [10, 12, 13] with PE several times after a ligament recon- struction surgery. At ﬁrst, the patient was only Wide split of S2 2 [10, 13] treated with anticoagulation. Echocardiogra- ECG phy, which showed RV myxoma, was not per- Sinus tachycardia 5 [4, 11–13] formed until the patient presented for the third time . The case reported by Boulafendis et al. RBBB 4 [8, 11, 13] also shows that echocardiogram was performed Right axis deviation 3 [4, 11] during a second presentation after only giving anticoagulation therapy during the ﬁrst one RVH 2 [10, 12] . Gonzalez et al. reported the death of a Labs 12-year-old boy after failing to diagnose the myxoma early . These cases show that the Leukocytosis 3 [4, 11, 13] diagnosis of myxomas can be easily missed in Microcytic 2[11, 13] case of not suspecting them. hypochromic anemia Singh et al. reported an RV myxoma seen on echocardiogram. Nonetheless, the RV cavity High ESR 2 [11, 13] was clear during surgery. Severe right heart SOB shortness of breath, S2 second heart sound, P2 pul- failure occurred in the immediate postoperative monic component of the second heart sound, RBBB right period, and embolism of the tumor was sus- bundle branch block, RVH right ventricular hypertrophy, pected . ESR erythrocyte sedimentation rate Including our case CONCLUSIONS Echocardiography was remarkable in four Despite being rare, cardiac tumors including RV cases [4–6, 10]. It revealed two right atrial mas- myxomas should be included in the differential ses and one RV mass in the ﬁrst one , two RV of the occasional patient with unexplained PE. masses and tumoral posterior cusp of the tri- This is particularly important when there are no cuspid valve in the second one , one right risk factors or predisposing etiologies for PE and 116 Cardiol Ther (2018) 7:107–117 the patient is young. The presentation of RV REFERENCES myxomas does not seem to be speciﬁc, and the diagnosis is usually accidentally made on a TTE 1. Reynen K. Frequency of primary tumors of the obtained to examine RV strain or failure. Fur- heart. Am J Cardiol. 1996;77(1):107. thermore, following up patients with echocar- 2. Jain S, Maleszewski JJ, Stephenson CR, Klarich KW. diography after surgery is important since Current diagnosis and management of cardiac recurrence, which seems to be related to myxomas. Expert Rev Cardiovasc Ther. incomplete resection, could happen. 2015;13(4):369–75. 3. 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“My last article couldn't be possible without the platform @deepdyve that makes journal papers cheaper.”@JoseServera