Paracardiac Adenopathy: CT
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1 29 Paracardiac Adenopathy: CT Evaluation Steven K. Sussrnan1 2 Robert A. Halvorsen, Jr.3 4 Paul M. Silverman1 5 Mohsin Saee& To establish the normal CT appearance of lymph nodes In the paracardlac area, we reviewed the CT scans of 50 patients without known malignancy or benign causes of lymphadenopathy. Five patients (10%) showed soft-tissue densities in the paracardiac region. The largest of these measured 3.5 mm. No more than two rounded soft-tissue densities were seen in any of the normal CT studies. Forty-five patients with paracardiac adenopathy were subsequently evaluated. In 27 (60%) of these the masses were due to either carcinoma, sarcoma, or benign disease. In 40%, the cause of paracardiac adenopathy was lymphoma. Features that favor a diagnosis of lymphoma are bilateral disease, multiple nodes, nodes greater than 2 cm in diameter, a lobulated or matted appearance, and associated pericardial thickening/effusion. Chest radiographs obtamed within 2 weeks of the CT scans in 38 patients revealed only nine cases in which a paracardiac mass could be seen. This study suggests that I cm is the upper limit for the diameter of lymph nodes in the paracardiac region, and that paracardiac adenopathy may be caused by a wide variety of nonlymphomatous malignant and benign diseases in addition to lymphoma. Compared with CT, chest radiographs are insensitive for detecting paracardiac lymphnode enlargement. Received June 25, 1986; accepted after revision February 25, Department of Radiology, Box 3808, Duke University Medical Center, Durham, NC Address reprint requests to S. K. Sussman at Duke University. 2Pent address: Department of Radiology, Hartford Hospital, Hartford, CT Department of Radiology, Durham Veterans Administration Hospital, Durham, NC Present address: Department of Radiology, University of Minnesota Hospital and Clinic, Minneapolis, MN Present address: Department of Radiology, Georgetown University Hospital, Washington, DC AJR 149:29-34, July X/87/ C American Roentgen Ray Society Although the normal size of lymph nodes in the mediastinum has been documented [1], no size criteria are available for lymph nodes in the paracardiac region. To establish the normal CT appearance of the paracardiac area, we reviewed the CT scans of 50 patients who had no known cause for malignant or benign lymphadenopathy. A second purpose of this investigation was to study the appearance of paracardiac adenopathy with particular reference to etiologies other than Hodgkin s and non-hodgkin s lymphoma [2-5]. This part of the study was based on CT examinations of 45 patients with solid masses in the paracardiac region. Finally, we compared the relative abilities of chest radiography and CT to detect paracardiac lymphadenopathy. Materials and Methods The CT scans of 50 patients (26 women and 24 men, years old) with no known malignant or benign causes of lymphadenopathy were examined to assess the detectability and size of presumed normal lymph nodes in the paracardiac region. The CT scans evaluated were either chest or abdominal scans obtained with 1-cm contiguous slices in which the paracardiac region was well seen. Any soft-tissue density was noted in the cardiophrenic angles, along the cardiac silhouette, or in the most inferior portion of the internal mammary lymph-node chain. The size and number of these nodes, as well as their sites, were recorded. were classified as either anterior prepencardiac or lateropericardiac (or posterior), on the basis of the anatomic classification of Rouviere [6]. The anterior group of nodes is subdivided into right, middle, and left components, whereas the posterior group has a left and a right component (Fig. 1). In addition, all CT scans obtained over a 4-year period in 45 patients (17 women and 28 men, years old) with solid masses in the paracardiac region were reviewed by two
2 30 SUSSMAN ET AL. AJR:149, July 1987 radiologists. Any single soft-tissue density in the paracardiac region 1 cm or larger was considered abnormal. Three or more solidappearing masses in the paracardiac area, even if less than 1 cm in diameter, were considered abnormal. Specific note was made of mass size, location, and multiplioty. Associated findings such as pleural effusions, other associated adenopathy, and pericardial effusion/thickening were noted. Patients with purely cystic and fatty paracardiac masses were excluded. The masses were seen at the time of abdominal CT in 27 patients, chest CT in 12 patients, and combined chest and abdominal CT in six patients. Chest CT scans were obtained with 1-cm collimation at 1-cm intervals, and abdominal CT scans were obtained with 1-cm collimation at either 1-cm (22 patients) or 2-cm (1 1 patients) intervals. Most patients received IV contrast material as a bolus followed by a rapid drip infusion. All scanning was performed on eithera GE 8800 or 6E 9800 CT scanner. All patients underwent posteroanterior and lateral chest radiographs. The mean interval between chest radiograph and CT scan was 8.8 days (range, 0-52 days). In the majority (30 patients) the time interval was less than 1 week. In all patients who had chest radiographs within 2 weeks of the CT scan (38 patients), the chest radiograph reports were reviewed to determine if a paracardiac mass had been described. Two authors reviewed the chest radiographs togetherand ratedthefilmsona 1-3scale: 1 = no paracardiac mass seen, 2 = equivocal, and 3 = paracardiac mass seen. The scores were arrived at by consensus. Direct pathologic proofofthe CT finding of paracardiac adenopathy (that is, biopsy or surgical removal of the mass itself) was available in 1 1 patients (three lymphomas, two colon carcinomas, one neurofibrosarcoma, one osteosarcoma, one breast carcinoma, one neuroblastoma, one endometrial carcinoma, and one histoplasmosis). Biopsy material confirming the patient s underlying diagnosis from a site other than the paracardiac mass (the primary tumor in nonlymphoma patients and other involved nodal regions in lymphoma patients) was available in the other 34 patients. Results Fig. 1.-Diagram of the diaphragm as viewed from above showing the location of the paracardiac lymph nodes. Anterior prepencardiac nodes (hatched), Iateropericardiac group (black); internal mammary nodes (retrosternal) and parietal pericardial nodes are not shown because they are located more cranially. Review of the CT scans in 50 patients with neither a known malignancy nor a known benign etiology for lymphadenopathy revealed rounded soft-tissue densities in the paracardiac region in only five patients (10%). In all five patients the softtissue densities were seen on only one CT slice. Two patients had single 2.0-mm-diameter rounded soft-tissue densities in the right anterior prepericardiac region. One patient had a single 3.5-mm-diameter rounded soft-tissue density in the mid anterior prepericardiac region (Fig. 2). Two patients had two rounded paracardiac soft-tissue densities each measuring 1.5 Fig. 2.-Normal-sized lymph node in patient without malignancy. Small 3.5-mm rounded soft-tissue density anterior to perlcardlum (arrow) presumably represents normal-sized anterior prepencardlac lymph node in patient with no underlying malignancy. Fi 3.-Right-sided large necrotic node (n) in Fi 4.-Left-sided lateropericardiac node in patient with metastatic colon carcinoma (biopsy- patient with colon carcinoma (arrow). Small hiaproved). Liver is also involved by metastatic dis- telhernia (h) Is noted incidentally. ease (arrowheads). Additional CT sections, as well as sonography, showed node to be separate from Nver.
3 AJR:149, July 1987 PARACARDIAC ADENOPATHY 31 mm in diameter. These were in the right and left anterior prepericardiac region in one patient and in the right and mid anterior prepericardiac region in the other. The other 45 patients showed no measurable soft-tissue densities in the paracardiac region. In 27 (60%) of the 45 patients with paracardiac adenopathy, the masses were nonlymphomatous in origin. Twenty-five (93%) of the 27 nonlymphoma patients with masses in the paracardiac region had known malignancies from a variety of carcinomas and sarcomas. Primary tumors included colon carcinoma (five patients) (Figs. 3 and 4), lung carcinoma (four patients) (Fig. 5), carcinoid (three patients), breast carcinoma (two patients), and a variety of other tumors encountered in one patient each (melanoma [Fig. 6J, hepatoma, neurofibrosarcoma [Fig. 7], neuroblastoma, somatostatinoma, renal cell carcinoma, osteosarcoma, endometrial carcinoma, ovarian carcinoma, transitional cell carcinoma, and adenocarcinoma of unknown primary). One patient with Aspergillus of the chest wall had multiple anterior bilateral nodes measuring about 1.5 cm in diameter. An isolated paracardiac lymph node that measured 1 cm in diameter was seen in the patient with histoplasmosis. In 18 (40%) of 45 patients paracardiac adenopathy was secondary to malignant lymphoma (Figs. 8 and 9). Seven patients had Hodgkin s lymphoma while the remainder were non-hodgkin s. Isolated right-sided anterior prepencardiac adenopathy was the most common site, occurring in 47% of patients. Isolated left anterior prepericardiac nodes and isolated midline anterior prepericardiac nodes were less common, occurring in 17% and 9% of patients, respectively. In 23% of patients, combinations of several sites were involved in the anterior prepericardiac group. Posterior nodes (lateropericardiac) were uncommon, present in only two patients (4%). Nodal size, multiplicity, and associated CT findings in the 45 patierts with paracardiac adenopathy are listed in Table 1. Paracardiac nodes varied in size from as small as 3 mm (in a patient with more than four masses, one of which was larger than 1 cm) to masses with a single dimension as large as 9 cm. In only two patients were the lymph nodes multiple and less than 1.0 cm in diameter: a patient with colon carcinoma had four detectable lymph nodes and a patient with lymphoma had five detectable lymph nodes, all less than 1.0 cm in size. In Fig. 5.-Multiple small lymph nodes in patient with metastatic lung carcinoma. A single node (arrowhead) measures 1 cm. There are at least three other discrete rounded soft-tissue densities (arrows) in right anterior prepericardiac region, all measuring less than 1 cm. Fig. 6.-Bilateral anterior prepericardiac nodes in patient with melanoma. There is associated pencardial thickening as well as subcutaneous tumor nodule (arrow) in right chest wall. Fig. 7.-Isolated right anterior prepericardiac node in patient with neurofibrosarcoma of chest wall. A, Large soft-tissue mass (m) involves right anterior chest wall. B, CT slice 6 cm lower shows right anterior prepericardiac node (arrow). Mild pericardial thickening is present.
4 32 SUSSMAN ET AL. AJR:149, July 1987 Fig. 8.-Multiple discrete nodes (arrowheads) Fig. 9.-Adenopathy mimics cardlomegaly in patient with Hodgkin s disease. encircle right heart border in patient with Hodg- A, Chest radiograph shows enlarged cardiac silhouette as well as prominent azygous and right kin s disease. paratracheal regions. B, CT scan shows multiple matted nodes with lobulated appearance (arrowheads). 6 months later, after therapy, cardiac silhouette returned to normal, coinciding with resolution of paracardiac adenopathy detected on CT. TABLE 1: Ancillary CT Findings in 45 Patients with Paracardiac CT Findings Lymphoma (n=18) No. of Patients Nonlymphoma (n=27) Multiple nodes 10 6 Bilateral nodes 6 3 Node size: 2cm 6 22 >2cm 12 5 Lobulated nodes 6 3 Other associated adenopathy 10 9 Pericardial thickening or effusion 5 2 neither of these two cases was biopsy proof obtained directly from these nodes. The mean lymph-node size for Hodgkin s lymphoma was 5.3 cm, and the mean size for non-hodgkin s lymphoma was 2.5 cm. A retrospective review of all chest radiographs obtained within 2 weeks of the CT scan is presented in Table 2. In only nine cases could a paracardiac mass be seen. In four of these cases, this finding was not mentioned in the original interpretation. The mean size of the largest node detected by CT in these nine cases was 5.4 cm, compared with a mean size of 2.6 cm in the patients with no mass detected on chest radiographs. Discussion Paracardiac lymph nodes is a general term for lymph nodes surrounding the heart. These lymph nodes consist of (1) nodes in the cardiophrenic angles, (2) nodes in the most caudal portion of the internal mammary chain, and (3) nodes along the pericardium [3]. Paracardiac adenopathy is somewhat misleading, as these nodes do not drain the myocardium. The lymphatics of the heart preferentially drain into anterior mediastinal nodes at the level of the transverse aortic arch [7]. The cardiophrenic-angle nodes were originally classified by Rouviere [6] and were described further by Castellino and Blank [8]. More recently, Glazer et al. [9] have added superior diaphragmatic nodes to the American Thoracic Society classification of regional nodes. These are nodes seen within 2 cm of the diaphragm, and they can be considered the equivalent to cardiophrenic-angle nodes. The cardiophrenic-angle nodes consist of two major groups, an anterior prepericardiac group and a lateropericardiac group (Fig. 1). The anterior prepencardiac group has a medial retroxiphoid component as well as paired lateral components. The anterior prepericardiac-node groups drain the diaphragm, liver, pleura, and antenor abdominal wall and empty into the internal mammary chain. The paired lateral component of the anterior prepericardiac group are the nodes that, when enlarged, produce a characteristic cardiophrenic-angle mass seen on frontal chest radiographs. The Iateropericardiac group is located in the cardiophrenic angle more posteriorly at the position of the phrenic nerves. These nodal groups drain the diaphragm, liver, pleura, and pencardium and empty into the anterior mediastinal chain [3]. The internal mammary-lymph-node chain parallels the internal mammary vessels, extending up from the level of the diaphragm. Although the internal mammary lymph nodes are sparse near the diaphragm [1 0], the most inferior aspect of this chain should be considered paracardiac nodes. CT cannot consistently distinguish adenopathy in the most inferior aspect of the internal mammary chain from adenopathy in the
5 AJR:149, July 1987 PARACARDIAC ADENOPATHY 33 TABLE 2: Retrospective Review of Chest Radiographs in 38 Patients with Paracardiac Adenopathy and Chest Radiographs Obtained within 2 Weeks of CT Scan Radiographic Rating No. of Patients No. with Multiple Single Mean Size of Largest Node (cm) C T Findings Small (s2 cm) Intermediate (>2 cm, <4 cm) Large (4 cm) Note-i = no paracardiac mass seen; 2 = equivocal, that is, a paracardiac mass could not be exdudod because of oveilying structures (such as effusion, collapse, and consolidation); 3 = paracardiac mass detected. medial retroxiphoid component of the anterior prepericardiac group. Therefore, we group these nodes together as anterior prepericardiac nodes. In addition, lymph nodes sometimes may be present on the surface of the parietal pericardium and drain the central portion of the diaphragm [7]. We suggest 1 cm as an upper limit of normal for lymphnode size in the paracardiac region. Of the 50 patients studied who had neither an underlying malignancy nor a benign cause of lymphadenopathy, no patient showed a soft-tissue density greater than 3.5 mm in diameter. This conservative upper limit was chosen to decrease the number of false-positive examinations. Smaller nodes may be considered suspicious if multiple. A patient with colon carcinoma had a single 1 -cm node as well as multiple other smaller adjacent nodes that presumably were abnormal (Fig. 5). Also, nodes larger than 1 cm are not necessarily caused by malignant processes. The two patients in our series with benign causes of paracardiac adenopathy (a patient with Aspergillus and a patient with histoplasmosis) had 1.5- and 1.0-cm nodes, respectively. Paracardiac adenopathy is an uncommon finding, reported predominantly in patients with malignant Iymphoma, both Hodgkin s and non-hodgkin s [2-5]. Even within the subgroup of lymphoma patients, involvement in this area is said to occur in only 3%, although the incidence of paracardiac adenopathy during relapse may be somewhat higher [4, 8]. Reports of involvement of paracardiac lymph nodes by a process other than lymphoma are rare in the radiologic literature. Recently Vock and Houler [1 1] reported nine cases of nonlymphomatous Cardiophrenic-angle adenopathy. Before this, there had been only a single report of two cases of nonlymphomatous cardiophrenic-angle adenopathy [1 2]. Our series clearly emphasizes that paracardiac adenopathy is not limited to only lymphoma patients, as in 60% of our cases the cause was nonlymphomatous, encompassing a wide range of causes. On chest radiographs, the paracardiac area is difficult to evaluate, as detection of masses usually is possible only when a mass is large enough to project beyond the cardiac silhouette. In only five of the 38 patients in whom chest radiographs were obtained within 2 weeks of the CT scan was a paracardiac mass described on the original chest radiographic report. Retrospective review of the chest radiographs with specific attention to the paracardiac regions revealed another four patients in whom masses could be seen. This insensitivity of the chest radiograph was reiterated recently by Castellino et al. [1 3]; of 1 6 patients with Hodgkin s disease and cardiophrenic-angle adenopathy detected by CT, these nodes were detected on chest radiographs in only two patients. In our study there was a significant correlation between mass size and visibility on chest radiographs (Table 2). While larger masses are detected more frequently on chest radiographs, a small mass may be visible if positioned so that its edge is border-forming. Of the nine patients in whom paracardiac masses were seen in retrospect, three patients had masses measuring only 2 cm in diameter. On the other hand, the presence of a large mass does not ensure detection on chest radiographs-six of the 23 patients with normal paracardiac regions on chest radiographs had masses of 4 cm or greater in diameter on CT. In two of these patients large nodal masses blended with the cardiac silhouette mimicking cardiomegaly (Fig. 9) [1 4, 1 5]. All masses visible on chest radiographs were in the lateral components of the anterior prepencardiac group. No patients with only midline anterior prepericardiac or posterior nodes had masses visible on chest radiographs. Patients with Iymphoma and paracardiac adenopathy had a number of features that were helpful in differentiating them from patients with paracardiac adenopathy from nonlymphomatous causes (Table 1). Features favoring the diagnosis of lymphoma consisted of bilateral disease, multiple nodes greater than 2 cm in diameter, a lobulated appearance, and associated pencardial thickening/effusion. Recognizing the presence of paracardiac adenopathy can be significant in terms ofpatient care. Paracardiac adenopathy was the only sign of active disease in some patients. In seven of the 1 8 patients with lymphoma, the paracardiac site was the only site of nodal involvement detected on the CT scans (chest CT in three patients, abdominal CT in three patients, and both chest and abdominal CT in one patient). In two of the three patients with recurrent Carcinoid tumors, paracardiac adenopathy was the only evidence of disease detected by abdominal CT. In three of four patients with lung carcinoma, the paracardiac area was the only site of associated nodal disease. All six patients with colon carcinoma and paracardiac adenopathy underwent contrast-enhanced CT of the liver with 1 -cm contiguous slices. Although liver metas-
6 34 SUSSMAN ET AL. AJR:149, July 1987 Fig. 10.-Partial volume of ziphold tip mlmlcklog paracardiac adenopathy. A, Rounded soft-tissue density (arrowhead) is seen In midline at base of heart B, Next slice cephalad shows that soft-tissue density Is immediately contiguous with bony xlphold tip (arrowhead) above. tases were seen in three patients, three showed adenopathy despite the lack ofliver metastases detected by CT. Detecting the presence of paracardiac adenopathy may alter clinical treatment plans. A decision not to place an intrahepatic chemotherapy pump in the patient with a hepatoma was made on the basis of the presence of extrahepatic disease as evidenced by the paracardiac adenopathy. Castellino et al. [1 3] recently reported that the CT finding of cardiophrenicangle nodes in patients with Hodgkin s disease had modified treatment in 1 8%. Such changes might include an increase in the radiotherapy dosage to the cardiophrenic angle or enlargement of treatment ports to encompass this previously unrecognized disease site [13]. In this study, only 1 1 of the 45 patients had biopsy proof directly from the paracardiac node. Of the other 34 patients, biopsy was not obtained from the paracardiac region, but from the primary tumor or infected site. Therefore, we cannot be sure that in these 34 patients the adenopathy was from underlying disease rather than from another unknown disease process, although the latter is unlikely. Another concern in those patients with enlarged paracardiac lymph nodes with biopsy proof only from other sites is that the lymph-node enlargement was from benign reactive hyperplasia rather than from neoplastic disease. Therefore, if an important therapeutic decision hinges on the cause of the nodal enlargement, one may need biopsy proof from the node itself. Pitfalls in the diagnosis of paracardiac masses seen by us include lung parenchymal masses abutting the pericardium, loculated pericardial effusions, atelectatic lung abutting the pericardium, focal postoperative blood collections, partial volume of the xiphoid tip (Fig. 10), and a liver mass protruding up through the diaphragm, presumably through a foramen of Morgagni hernia. A 1-cm upper limit of normal for lymph-node size in the paracardiac region may be used, although smaller nodes, if numerous, must be viewed with suspicion. In conclusion, paracardiac adenopathy may be caused by a wide variety of nonlymphomatous malignant and occasionally benign diseases. ACKNOWLEDGMENT We thank Janice Waters for secretarial assistance in preparing this manuscript. REFERENCES 1 Cho CS, Blank N, Castellino RA. CT evaluation of cardiophrenic angle lymph nodes in patients with malignant lymphoma. AiR 1984;i43: Jochelson MS, Balikian JP, Mauch P, Liebman H. Pen- and paracardial involvement in lymphoma: a radiographic study in 11 cases. AJA 1983;i40: MCLOUd TC, Meyer JE. Mediastinal metastases. Radio! Clin North Am : Glazer GM, Gross BH, Quint LE, Francis lr, Bookstein FL, Omnger MB. Normal modiastinal lymph nodes: number and size according to American Thoracic Society mapping. AiR 1985;144:26i Meyer JE, MCLOUd TC. Undfors KK. CT demonstration of cardiophrenic angle tymphadenopathy in Hodgkin disease. J Comput Assist Tomogr 1985;9: Rouviere H. Anatomy of the human lymphatic system (a compendium translated from the original by Tobias MJ). Ann Arbor, Ml: Edward Grothers, 1938: Weinberg JA. The intrathoracic IymphaticS. In: Haggensen CD, Feind CR, Hector FP, Slanetz CA, Weinberg JA, ads. The lymphatics in cancer. Philadelphia: Saunders, 1972: Castellino RA, Blank N. Adenopathy of the cardiophrenic angle (diaphragmatic) lymph nodes. AiR 1972;114: Glazer HS, Aronberg DJ, Sagel 88, Friedman PJ. CT demonstration of calcified mediastinal lymph nodes: a guide to the new ATS classification. AiR 1986;147: Lein HH, Lund G. COmputed tomography of mediastinal lymph nodes. Acta Radiol (Diagnj (Stockh) 1985;26:64i vock P, Houler J. Cardiophrenic angle adenopathy: update of causes and significance. Radiology 1986;159: Bledin A, Bemardino ME, Ubshitz HI. Cardiophrenic angle nodes: an unusual CT finding of advanced metastatic disease. J Comput Tomogr 1980;4: 193-i Castellino RA, Blank N, Hoppe RT, Cho C. Hodgkin disease: contributions of chest CT in the initial staging evaluation. Radiology 1986;160: Anglelini GD, Butchart EG. Lymphoma mimicking cardiomegaly. Thorax 1984;39: Crowe JE. Cardiophrenic adenopathy in Hodgkin s disease. Am J Dis Child 1975;129:1i6-1i7
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