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Ambreen Fatima Ali, MD, Cardiovascular Medicine Fellow, presents a rare care of constrictive pericarditis. Diagnostic testing including various imaging techniques and CT guided biopsy leads to the diagnosis of pericardial mesothelioma. An expert panel led by Dr. Allan Klein, Director of the Pericardial Center discuss this case and issues surrounding the topic.

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Pericardial Cases: A Bad Case of Constrictive Pericarditis

Podcast Transcript

Announcer:

Welcome to Cleveland Clinic Cardiac Consult, brought to you by the Sydell and Arnold Miller Family Heart, Vascular & Thoracic Institute at Cleveland Clinic.

Ambreen Fatima Ali, MD:

Good morning, everyone. I'm Ambreen, I'm one of the second-year general cardiology fellows. And today I'll be presenting a unique case of constrictive pericarditis, and then briefly talking about it towards the end. So let's get started.

Ambreen Fatima Ali, MD:

We'll just dive in. This is a 46-year-old female who presented initially in June of 2019 with shortness of breath and chest discomfort. This was to an outside facility. So the initial evaluation shows a large pericardial effusion. She undergoes pericardiocentesis of the effusion, 800 ccs of hemorrhagic fluid is removed. She's not on any blood thinners and no history of trauma. Analysis was unremarkable at the time and the psychology was negative. She does well through her short hospital stay and is discharged on colchicine for six months with plans to follow up in about three months.

Ambreen Fatima Ali, MD:

So briefly about her. Her prior history is significant only for hysterectomy for fibroids and history of shingles reactivation. Otherwise, she's fairly inactive. She has an office job and she lives independently. No prior cardiac history, no significant viral infections, no significant travel history. At this time the diagnosis was presumed maybe mild myocarditis versus there was some concern with the shingles that it might be related, but there was nothing solidified and the plan was to follow her.

Ambreen Fatima Ali, MD:

But before her three month follow-up, she comes back in again, this is one month from her original discharge time, and with recurrent pericardial effusion. So similar symptoms, and the echocardiogram shows another large pericardial effusion. She undergoes creation of the pericardial window at this time. The pericardial biopsy from the window shows mesothelial line, fibrous tissue with chronic inflammation. And that's negative for malignancy. Again, she's discharged on colchicine and prednisone this time, and the plan is to taper it slowly.

Ambreen Fatima Ali, MD:

She's seen in a follow-up about three months later and everything's going well. In about six months, they slowly taper off the medications and she does well. Again, the diagnosis is a little unclear as to why she had this, but she was doing okay. And so the plan was made to just follow up.

Ambreen Fatima Ali, MD:

And then 20, 21 months pass and she comes to us. Before this, she goes back to her outside physician with recurrence of symptoms for the prior two to three months, and he evaluates her and then refers her here to our Clinic, the Pericardial Clinic. She comes in, she's very short of breath. She's very evidently volume overloaded and has some chest discomfort. And based on her exam, her history, and her discomfort, she's admitted directly from clinic for diuresis and further assessment.

Ambreen Fatima Ali, MD:

When she arrived to the hospital, her blood pressure is 140/98 and heart rate's 95. So not very tachycardic, she's maintaining stats reasonably on room air. She's comfortable in a sitting up position, but she's unable to recline because it's just a discomfort she has with shortness of breath. And physical exam is remarkable. Very, very remarkable for volume overload, elevated JVT, abdominal distention, significant lower extremity edema, bilaterally, and just the overall sense of discomfort in her.

Ambreen Fatima Ali, MD:

She starts undergoing diuresis, and then we start with some diagnostics. So this is her EKG, basically the rates just under 100 in sinus. Nothing too remarkable here, maybe some T wave inversions, but other than that, nothing too dramatic. And then she has this chest X-ray on admission and here there's significant cardiomegaly. The cardiac silhouette is somewhat globular, but you also have a very large left sided effusion. It's hard to say on that side. And then you see that there's vascular congestion as well. So a lot of volume overload, big effusion, and then the cardiac or the mediastinal silhouette is a little enlarged.

Ambreen Fatima Ali, MD:

So we go into her echocardiogram and on the left there's the parasternal long axis. And the first thing, so going systematically, the chamber size grossly looks normal and the function also looks preserved with the mitral valve, which we can see looks normal and collapsing normally. But the big thing that you see here is this echodense surrounding structure just outside the myocardium, somewhat nodular or irregular around RVOT and also around the LV, and some fluid potentially in the pericardial space. Hard to say just in this view, but clearly there.

Ambreen Fatima Ali, MD:

And then you move to the right onto the short axis, and the same thing. The chamber size and chamber functions look adequate, but around the heart is basically what you see this echodense, irregular structure. And then here, the other thing that jumps out at me is the septal motion, what we call septal bounds or restrictive septal motion, where it goes towards the LV and then bounces back towards the RV in different phases at the end of beat.

Ambreen Fatima Ali, MD:

Moving on. So we have an apical four chamber view on the left here, and again, the same thing. The chamber sizes seemed adequate. However, there's this nodular, echodense structure around the heart. So very prominent, and then some fluid in the pericardial space there. And sorry about ... And then on the right, I don't know if there's something coming up on the screen here, give me one second. There we go. And on the right, we have a subcostal view. And again, the same thing, so I just won't belabor it, but basically what we see is we see the structure on all the views.

Ambreen Fatima Ali, MD:

Going into a little bit of flow here. So on the left we have the tricuspid inflow, and then on the right we have the mitral inflow. And basically we see significant variation. And even on the tricuspid side, you see a little bit, but I'll talk about the mitral first. That with inspiration, you have a decrease, and then with expiration, you see an increase, and that's this variation of flow across the mitral valve with regards to respiration. And on the tricuspid as well, although it's the opposite and it's not as pronounced there, but you see that.

Ambreen Fatima Ali, MD:

And then going into the Doppler. So on the left, we have the septal tissue Doppler and the lateral tissue Doppler, and the E prime on the lateral is slightly lower, but it's lower than the septal tissue Doppler, which is reversive and evidencing any revervise. And then lastly, we have the IVC, so a dilated plump IVC, about 2.5 centimeter here, and doesn't collapse with the sniff test. And there's reversal of hepatic vein flow with expiration, increased reversal. And then she also had the small sign where there was increased JVP with inspiration. So everything pointing towards the preliminary diagnosis of constrictive pericarditis.

Ambreen Fatima Ali, MD:

Just the same things here, normal LVRV with large effusion and an echodense mass around the heart, dilated IVC. Septal balance with septal shift and respiratory variation of tricuspid inflows.

Ambreen Fatima Ali, MD:

So before this, and before I let it play, so we go ahead and get a couple of imaging studies in quick succession. So I'll start with the CT here to get us in. And so basically that's what we see here. We see this heterogeneous almost mass around the heart, encasing from the great vessels all the way down to the apex and all around it circumferentially. And it's got some nodular areas, and then around the right atrium there's an area which seems like exudative pleural effusion. And we checked the Hounsfield units on this, and it's just about 50. So it's some sort of a soft tissue that's not fat, but that was pretty much what we got from this.

Ambreen Fatima Ali, MD:

And then moving on, we go towards the cardiac MRI. So this is just a quick stacked image to show the extent of the tumor really, that it starts from incasing the aorta, the main pulmonary artery, left and right pulmonary artery, the SVC, and then all the way around the heart, and then through the very end, just encasing it all over. And you see fluid there.

Ambreen Fatima Ali, MD:

So this is the cine axis sequence, and you see this heart trapped here, and hence the name heart encased, trapped here with that gritty, significant septal bounds and septal shift, but also the effusion around the right atrium is dispirited and the circumferential mass with heterogeneous appearance here on the MRI. Mixed elements there a little bit. And a large left sided effusion.

Ambreen Fatima Ali, MD:

And so this is a free-breathing sequence here. So patient's breathing throughout the cycle, and basically we see an increase of the septal shift with respirations. The same thing, you see that this heart is encased by this mass, and there's pretty significant constricted physiology secondary to that. And then we use the MRI to give us clues about what this could be. And so I'll just talk a little bit about it. So in the axial we just know that this is from the clip I showed, and this is ... We know that this is a heterogeneous mass with a little bit of fluid and perhaps a little bit of other elements, but predominantly soft tissue.

Ambreen Fatima Ali, MD:

And then this is the blood sequence. And you basically see whether there's any blood in the mass or blood around. And you don't really see the blood because it's all black, but you don't really see anything in that pericardial space. This is the T2-STIR sequence. Basically looking for edema, and you do see the myocardium a little bit dark there. And then beyond that, quite a lot of edema and inflammation in that space around the heart.

Ambreen Fatima Ali, MD:

And then lastly, the late gadolinium enhancement. Here was a little bit of a surprising element, which is all the highly metabolic or vascular tumors will have significant uptake of gadolinium contrast, but here you actually don't see it. You see a little bit in the periphery in the pericardium, but not a whole lot within the mass itself. So narrowing down our diagnoses to a couple of tumors, like lymphoma being the first one, and then epithelioid tumors being up there with it.

Ambreen Fatima Ali, MD:

This is basically everything I talked about. So just this was the final read on it, talking about the IVC, the effusion and the extent of the mass with the significant constrictive physiology. The one thing that we did not find was any infiltrative process in the myocardium. So you don't see a lot of late enhancement within the myocardium. So at this time we thought that it was all in the pericardial space.

Ambreen Fatima Ali, MD:

So we go ahead and get a PET scan, a full body PET. We just want to show this. So it lights up like the sun and such a remarkable scan here. So the entire body of the mass just lights up. And she doesn't have a lot of lymph nodes that light up in the mediastinum or anywhere else which were picked up earlier on the scan, but this entire mass lights up. I just thought this was a very remarkable imaging study here.

Ambreen Fatima Ali, MD:

So after this, we speak to the surgical team, the oncology team and the consensus is we need to know what this is, and to go for mass biopsy. We speak to IR and they said they can attempt an anti-mediastinal CD-guided biopsy of the mass. And so we go for that. And before I actually give you the read, I'm going to invite Dr. Mukhopadhyay to speak about the histopathology a little bit here.

Sanjay Mukhopadhyay, MD:

Thank you, Ambreen. Can you hear me? Is it ...

Ambreen Fatima Ali, MD:

Yeah. Yeah, doctor. Yeah. We can hear you.

Sanjay Mukhopadhyay, MD:

Okay. Thank you. So this is a picture of the biopsy, and you can see that it's a needle biopsy. And this is from anterior mediastinum slash pericardial mass. The black arrows are actually pointing to neoplastic cells. So there are tumor cells here. They have an infiltrative and very complex growth pattern. In fact, at the lower right, there are little papillary finger-like formations that support a neoplastic interpretation. The red arrow point points to the stroma, and the stroma is actually showing a desmoplastic response, which means that it's reacting to the infiltrating tumor. Next, please.

Sanjay Mukhopadhyay, MD:

So this is a high magnification of the same thing. The lower black arrow actually points to one of these papillary structures that supports the malignant interpretation. And the reason I'm mentioning this is that the most difficult part of the interpretation is actually to prove that this is malignant. The type of tumor cells is actually easier to show by immunochemistry. Again, the red arrow points to the stroma. Next, please.

Sanjay Mukhopadhyay, MD:

Now, what exactly are these infiltrating cells? Here's where immunohistochemistry is very helpful because we have immunohistochemical markers for mesothelial cells and non-mesothelial malignancies. The highest on the differential is really an adenocarcinoma. So here's a mesothelial marker named calretinin. This is positive both in the nuclei and cytoplasm of the tumor cells. So one mesothelial marker positive. Next, please. Next slide, please.

Sanjay Mukhopadhyay, MD:

The common mesothelial marker that we use in addition to this is called WT1, and that's a nuclear marker, and you can see that it's beautifully positive in these neoplastic cells. So two mesothelial markers are positive. Next one.

Sanjay Mukhopadhyay, MD:

And then there's a cytoplasmic marker called cytokeratin 5/6, which is also characteristically a mesothelial marker. So there's very, very strong evidence here that these are actually mesothelial cells, and combined with the morphologic interpretation that these are infiltrative, this makes it very strong evidence for mesothelioma. Now next, please.

Sanjay Mukhopadhyay, MD:

We do try to also look at the alternative. So is there any evidence for carcinoma? So here's a marker of lung adenocarcinomas, TTF1, and that is negative. Next, please. And here's a broad spectrum marker of carcinomas from many organs, including from the lung, which is called carcinoma embyronic antigen, or CEA, and that's negative. So we have no evidence that this is a carcinoma and very strong evidence that this is mesothelioma. Next, please.

Sanjay Mukhopadhyay, MD:

Nowadays, a new marker that emerged is the so-called BAP1, and the BAP1 is helpful only when it is lost. So here, for example, in this case, the nuclear expression of BAP1 is retained. So that's not very helpful because loss of expression is only seen in about half of mesotheliomas. So if it is lost, it's very helpful because it's very specific. Loss is not seen in benign lesions, but retention of expression is not that helpful, as in this case. Next, please.

Sanjay Mukhopadhyay, MD:

So the diagnosis based on the biopsy was malignant mesothelioma, epithelial type since the neoplastic cells are epithelial in appearance. Subsequent to this, next slide, we also received pleural fluid cytology, which also showed similar cells as those seen in the biopsy, which was read as consistent with mesothelioma. Of course, as you know, in fluids, the diagnosis is very, very difficult because you don't see infiltration, but based primarily on the preexisting biopsy diagnosis, this was read as consistent with mesothelioma. And that's it for me.

Ambreen Fatima Ali, MD:

Thank you so much.

Sanjay Mukhopadhyay, MD:

Any questions, Ambreen? Anything I can address?

Ambreen Fatima Ali, MD:

No, thank you so much, Dr. Mukhopadhyay. Thank you. Thanks a lot. That was very helpful.

Sanjay Mukhopadhyay, MD:

Thank you.

Ambreen Fatima Ali, MD:

Thank you. So moving on. So she gets this diagnosis of primary pericardial mesothelioma and we go back and start talking to the team. So we speak to the cardiac and thoracic surgery team and our oncology team here. And the first thing we want to talk about is whether there's any possibility of surgical resection, and that's deemed impossible, given the extent of tumor and the encasement of the great vessels. It's impossible to go in.

Ambreen Fatima Ali, MD:

So we speak to oncology and they start the patient on a chemotherapy regimen with carboplatin and pemetrexed. And with the understanding that the outcomes for this tumor are not great to begin with. And especially without any degree of surgical resection or debulking, the chemo can only do so much. Since then ... Actually, before we move on, Dr. Stevenson, do I have you on the line? I don't think. We'll just go on.

Ambreen Fatima Ali, MD:

So unfortunately, since then, she's had repeated admissions with the complicated heart failure, as the mass has not responded favorably to chemotherapy, and recently she's been starting a palliative radiotherapy for symptom control. So talking a little bit, just take a few minutes and talk about it, but this is a repeat echocardiogram from just very recently, and this is after a couple of cycles of chemo. Basically we don't see a whole lot of difference. We kind of still see the mass around the heart. And in this view, maybe you could argue that it's less nodular or less irregular, but overall there's not been much difference and she's continued to do, unfortunately, rather poorly.

Ambreen Fatima Ali, MD:

So talking about primary pericardial mesothelioma. So again, an exceedingly rare but lethal primary tumor of the pericardium. It's less than 1% of all mesothelioma. Nevertheless, 50% of the primary pericardial tumors, because most of the pericardial tumors are actually secondary tumors and not primary. So of the few that are primary, it takes a big chunk, but overall exceedingly rare. There were 103 published cases in the last 20, this is years or so. But in total there've been about 150 cases and that's about it.

Ambreen Fatima Ali, MD:

Median age at diagnosis is 55 years and survival of less than six months. And asbestos exposure is associate with pleural and peritoneal mesothelioma, so it's also hypothesized to increase risk. We went back and asked the lady, she's had no history of asbestos exposure.

Ambreen Fatima Ali, MD:

Treatment, so the two modalities, whether you can resect the mass or not, whether you can use chemo or not. And whether you do both of these, with or without radiation. And basically the only thing shown to have a modest survival benefit was the chemotherapy. And the surgery, it's not really worked. Because I think of these 150, maybe only two or three cases actually underwent complete resection. This was in younger people. Everybody else, by the time the tumor's identified, the tumor's weighted structures around the great vessel to something, and only partial pericardectomy be performed. And so it's more with the palliative intent or with the intent of just debulking the tumor.

Ambreen Fatima Ali, MD:

I don't know if that's a fair comparison, but yeah, for now at least, we don't think surgery's done much. But that is very sparse because of the very, very few cases. But the suggestion is to use combination carboplatin and pemetrexed therapy. 35 patients were reviewed in this paper who received combination chemotherapy and had some survival benefit with this. Gemcitabine, which was used previously, is not associated with survival benefit. And the true prognostic factors were metastasis was worse and chemotherapy with a little bit of survival benefit. Surgery, which was mostly partial pericardectomy and radiotherapy did not impact survival.

Ambreen Fatima Ali, MD:

When I look at this case, the question that I ask myself is, was this a missed opportunity for diagnosis the first two times that she presented? And looking into the literature for this, it's kind of variable. This kind of tumor can mimic signs of constrictive pericarditis recurrent effusions until a much later stage when it organizes into tumor form. So it's hard to pick it up on imaging early, which was the case here. The false negative rates of pericardial fluid cytology pericardial biopsy in all tumors with malignant pericardial effusions have been variable. So it can be with the cytology, a false negative up to 15%. And with the biopsy, up to 40, 45%, which is pretty high.

Ambreen Fatima Ali, MD:

The sensitivity of cytologies that diagnose malignancies is very high when you do have it. But in her, both the prior times, we had cytology which was negative and a pericardial biopsy which was negative. So it's very unfortunate. And looking through the literature, there's been multiple cases like this where people have presented late with the mass. And then earlier on, looking back, there was no evidence of it on diagnostic studies.

Ambreen Fatima Ali, MD:

So before I end, just talking a little bit about cardiac mass. This is about intra and extra cardiac masses both, but basically judging the mass by the company it keeps and guilt by association. So suspicious characteristics for any mass that you see would be broad-based attachment, loss of tissue planes, traversing the cardiac chambers, pericardial involvement and tissue heterogeneity. And here, except for traversing the cardiac chambers, we had everything in this mass.

Ambreen Fatima Ali, MD:

And MRI being the gold standard for getting characteristics of the mass. So looking through, and I won't label this, but a couple of things here would be the delayed gadolinium enhancement is pretty high with malignant tumors. However, this one, we did not have a lot of late gadolinium enhancement. And that was probably because it's not a very vascular tumor. And other than that, the MRI imaging characteristic of common cardiac masses, again, the lymphoma and mesothelioma are the ones with low an minimal uptake. So-

James Stevenson, MD:

Dr. Ali.

Ambreen Fatima Ali, MD:

Yeah? Hello?

James Stevenson, MD:

Hey, this is James Stevenson. Are you able to hear me?

Ambreen Fatima Ali, MD:

Yeah, I can. Thank you.

James Stevenson, MD:

I'm sorry. I was having problems muting myself, but I'm happy to add a little commentary if still needed.

Ambreen Fatima Ali, MD:

No, absolutely. Thank you so much.

James Stevenson, MD:

Okay.

Allan Klein, MD:

So Jamie, could you come on the treatment of this patient?

James Stevenson, MD:

Yes. As you heard, the mainstay of treatment for all mesotheliomas which aren't surgical candidates, of which really the pleural mesotheliomas are kind of the paradigm that is given the most common type of mesothelioma that tends to be followed. And this is where we get all of our clinical trials data from are really pleural mesothelioma patients. And really only about 10% or less of pleural mesothelioma patients are going to consider for surgical resection. So mesothelioma, as in the case with pericardial mesos, is really not a surgical disease, except peritoneal mesos are a bit different in that surgery is more of a mainstay of treatment for them.

James Stevenson, MD:

So it wasn't uncommon for this woman not to be a surgical candidate, because really only in the case of a more localized pericardial meso would surgical resection probably add benefit. Again, the data that we have to go on are from case series or reviews where the largest review was just over a hundred patients published a few years ago. And I don't even think, in terms of the number of pericardial patients that I've seen in just over 20 years of seeing thoracic oncology, I don't even know that it's in double digits. So these are very rare. And in terms of responsiveness to systemic therapy, it does appear that, as Dr. Ali mentioned, that there can be some survival improvement with chemotherapy.

James Stevenson, MD:

She also had, before her most recent admission, had been on immunotherapy, which is a relatively new treatment for mesothelioma that, again, with pleural mesothelial, we had evidence of a survival benefit in a randomized trial. But again, unfortunately in her case, she really did not respond to either chemotherapy or immunotherapy. She had no radiographic improvement and had clinical deterioration throughout the course of both of these treatments.

James Stevenson, MD:

And she just recently started radiotherapy, which is technically difficult. And our thoracic radiation oncologist, this was, given the rarity of these cases, this was something that they really had to plan carefully. And that's where she is right now in her treatment course.

James Stevenson, MD:

Again, these are difficult cases, and especially, obviously with the pericardium being involved, there's just not as much room for these tumors to grow as opposed to the pleura, where, obviously, we have two lungs over the abdomen where the the compartment is a little bit different. So that's why her clinical course has been so complicated with admissions and symptoms. And it's just been a very difficult case for this poor woman.

Allan Klein, MD:

Okay. That's great. Thanks, Jamie. May I ask the panel very briefly, we have Dr. Jellis and Dr. Kwon, and Wilson Tang. Any comments, Christine?

Christine Jellis, MD, PhD:

Firstly, just thank you for sharing that case, because I think as we've heard, that is such a rare condition and many of us will see very few of these in our lifetime. So I think being able to recognize the characteristics is really important. I won't labor the point, but I think you showed nicely on the multimodality imaging, how we can use that for tissue characterization to really tease out how much of that is soft tissue mass versus fluid. Is the fluid organized? Is it not organized? Is there tethering? All those sorts of things.

Christine Jellis, MD, PhD:

I think you showed with the MRI in particular, that you can really come to a fairly robust conclusion of what you're dealing with before you have the tissue sample. Obviously, we want to confirm the pathology, but I think just all these modalities are so complementary, and obviously the extent of disease and the spread and those characteristics that would tease out benign versus malignant and so forth. So thank you for sharing. It was a great case.

Ambreen Fatima Ali, MD:

Thank you.

Allan Klein, MD:

Debbie, any comments?

Deborah Kwon, MD:

Yeah. Just want to echo the same comments, phenomenal presentation and case.

Ambreen Fatima Ali, MD:

Thank you.

Deborah Kwon, MD:

The PET actually was the one that struck me the most. As you said, lit up like a sun. I'm a huge proponent of MRI, but I think the PET was really the most striking. Because I think with MRI, we can often tell you, yeah, we think it's malignant, or we think it's benign, but the PET really helps to definitively say that. And also with MRI, while we have those good table of characteristics, we can't really definitively tell you what the final diagnosis is. So again, I think this is a nice case showing how imaging helped to bring it to, this is malignant, but the tissue diagnosis was absolutely necessary. Thank you for showing such a great case.

Ambreen Fatima Ali, MD:

Thank you.

Allan Klein, MD:

Dr. Tang from heart failure, she's on torsemide 100 bit currently.

Wilson Tang, MD:

Yeah. I think contrary to most people actually, heart failure docs always like to think about how can we not encounter this scenario? So I actually kept on thinking as you're presenting, should we have a lot more vigilance early on? You did tap some blood. I remember when you come out, and that got me to think all the persistent pericardial effusion cases, whether multimodality imaging has some bearing to have earlier diagnosis before the heart gets encased.

Wilson Tang, MD:

Obviously this is some opportunity that we need to think about as we kind of put some of these malignancies in a differential, as we work up these cases.

Allan Klein, MD:

The only comment I would make is that the patient presented with typical constriction with a very, very unusual cause. So I think we did a handheld echo as well, and we were struck by some of the findings, and that led to some of the investigation. But it had all the features of the construction, but not the most common cause in this, and unfortunate the lady's going through all this heart. But Dr. Ali, that was an excellent case. That's worthy of publication as well. Well, thank you so much.

Ambreen Fatima Ali, MD:

Thank you.

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