Cardiac Involvement and Absence of Asthma – What is Phenotype Specificity of EGPA: A Case Report

  • Clinical Medicine & Research
  • September 2022,
  • 20
  • (3)
  • 170-
  • 176;
  • DOI: https://doi.org/10.3121/cmr.2022.1683
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Abstract

Eosinophilic granulomatosis with polyangiitis (EGPA) typically is characterized by asthma, blood eosinophilia, and extrapulmonary manifestations. Asthma is a major EGPA symptom affecting almost all patients, but cardiac involvement is one of the most serious manifestations, responsible for 31% of deaths. Two recently defined phenotypes of EGPA, according to the patient’s antineutrophil cytoplasmic antibody (ANCA) status, differ significantly in clinical features and prognosis. We share a case of EGPA characterized by atypical manifestation without any evidence of asthma, in whom extensive cardiac involvement was the dominant manifestation of vasculitis. This case demonstrates the difficulties associated with phenotyping EGPA and highlights the importance of cardiac magnetic resonance imaging (CMRI) in definitive diagnosis.

Keywords:

Eosinophilic granulomatosis with polyangiitis (EGPA), formerly known as Churg-Strauss syndrome, is now recognized as a form of antineutrophil cytoplasmic antibody (ANCA)–associated vasculitis (AAV) characterized by eosinophil–rich granulomatous inflammation and small to medium–sized vessel vasculitis.1,2 Classic EGPA is associated with asthma, blood eosinophilia, and extrapulmonary manifestations.3 Asthma is a major manifestation of EGPA, affecting almost all patients, and often occurs before the onset of systemic vasculitis (mean interval, 9.3 ±10.8 years).4 It usually manifests in the age range of 30-40 years-of-age but can also manifest during childhood. The commonly involved systems include the peripheral nervous system and lungs, followed by the skin.5,6 However, EGPA can affect any organ system, and cardiac involvement is one of the most serious manifestations, responsible for 31% deaths due to EGPA.7 Recently, two phenotypes of EGPA according to the patient’s ANCA status, which differ significantly in clinical features and prognosis, were defined.8,9 We present a rare case of EGPA, without any evidence of asthma, admitted due to symptoms of eosinophilic pneumonia, and in whom cardiac involvement was the dominant manifestation of vasculitis. The case demonstrates the difficulties associated with phenotyping of EGPA and highlights the importance of cardiac magnetic resonance imaging (CMRI) in definitive diagnosis.

Case Report

A woman, age 34 years, was admitted to our institute due to recurrent symptoms of dyspnea, cough, fever, and pulmonary infiltrations for 6 months. She did not report any history of asthma or allergy including allergic rhinitis or nasal polyps. Her children suffered from food allergy, but none of the family members had asthma. Previously, no evidence of marked peripheral eosinophilia was observed (<1,5000 cells/μl). Results of pulmonary function tests (spirometry) were normal, and the symptoms subsided after antibiotic therapy. One month before the current hospitalization, in March 2017, dyspnea and cough worsened, with additional hemoptysis. Based on the findings of a computed tomography (CT), the possibility of pulmonary embolism was excluded, and bilateral pneumonia was diagnosed. The patient was again administered antibiotics, but 2 weeks later symptoms recurred, and moderate eosinophilia was evident (2,000 cells/μl) without any extrapulmonary symptoms. The results of echocardiography (ECHO) and levels of basic cardiac markers (brain natriuretic peptide [BNP] and troponin T) were normal. No obstruction was evident on spirometry. Eosinophilic pneumonia was suspected, and after 2 weeks, in April 2017, she was referred to our institute. On admission, her general condition was not bad, but physical examination revealed blood pressure of 90/60 mmHg, pulse rate as 130 bpm, and body temperature of 38°C. No clinical signs of bronchospasm were observed, and crackles were auscultated in the lower right lobe of the lung. On the dorsal surface of the hands, subcutaneous red nodules were observed, while small petechiae (the so-called “splinters”) were found underneath the nails. There was no evidence of swelling in the lower limbs. Results of complete blood count showed leukocytosis (25,000 cells/μl) with high eosinophilia (17,000 cells/μl). Serum biochemistry revealed elevated levels of troponin T at 2.1 ng/ml (normal, <0.014 ng/ml), BNP at 9,453 pg/ml (normal, <125 pg/ml), C-reactive protein at 350 mg/ml (normal, <5.0 mg/ml), and IgE at 1,001 IU/ml (normal, <100 IU/ml). The plasma creatinine level was normal, but hematuria and proteinuria manifested. Serum was negative for anti-myeloperoxidase (MPO)- and anti-proteinase 3 (PR3)-ANCA. Spirometry revealed correct parameters (forced expiratory volume in the first second (FEV1)=3.43 L (109% pred), and forced vital capacity (FVC)=4.14 L (110% pred), without airway obstruction (FEV1/FVC=0.82). Chest CT demonstrated the presence of bilateral peripheral pulmonary infiltrations and cardiomegaly with pericardial effusion (Figure 1). Electrocardiogram (ECG) showed sinus tachycardia with non-specific ST-T segment elevation in all leads. ECHO revealed hypokinesis of apical segments and features suggestive of interstitial cardiac edema with moderate pericardial effusion. CMRI demonstrated extensive acute inflammation of all three layers of the heart with reduced left-ventricular function (ejection fraction [EF], 40%), wall thrombi at the apex of the left ventricle, thrombus on papillary muscles, and small areas of microinfarctions resulting from coronary vasculitis (Figure 2). Although the serum was negative for ANCA, and the patient did not report any history of asthma and/or allergy, EGPA was diagnosed based on peripheral marked eosinophilia and extrapulmonary symptoms with extensive cardiac disease visualized in CMRI. According to the revised five-factors score (FFS), the severity of the disease established two points.10 According to the recommended protocol,11 corticosteroid treatment (1 mg/kg) in combination with oral cyclophosphamide (2 mg/kg) was initiated, and immediate improvements in symptoms and laboratory findings were evident. During hospitalization, dyspnea improved, heart ratio was restored to normal, and fever disappeared. Laboratory findings showed improvements in complete blood count (9,000 cells/μl), eosinophil count (350 cells/μl), and urine parameters. Troponin T levels were restored, and BNP levels decreased (1260 pg/ml). On ECG, ST-T-segment elevation resolved. Follow-up CMRI performed after 3 months of immunosuppression showed substantial regression of lesions with improvement in EF (increase to 52%), while chest CT demonstrated complete resolution of pulmonary infiltration and restoration of heart size (Figure 3).

Chest CT axial images, lung window (A, B), mediastinal window (C) shows predominant peripheral bilateral ill-defined areas of airspace opacities (black arrow) with or without air-bronchogram (A, B) and ground-glass opacities (black asterisk) with interlobular septal thickening (white arrow) (B). The pericardial effusion was also present (white asterisk) (C).
Figure 1.

Chest CT axial images, lung window (A, B), mediastinal window (C) shows predominant peripheral bilateral ill-defined areas of airspace opacities (black arrow) with or without air-bronchogram (A, B) and ground-glass opacities (black asterisk) with interlobular septal thickening (white arrow) (B). The pericardial effusion was also present (white asterisk) (C).

Magnetic resonance images: black blood T2-weighted STIR images in long axis (A) and short axis (B); white arrows-subendocardial and transmural oedema. (C) Late Gadolinium Enhanced (LGE) images with fat saturation in long axis (C), and transverse (D) views. White arrows: infarct-like LGE pattern within subendocardial layer. Yellow arrows: extensive LGE with microvascular obstruction (MVO) in interventricular septum and anterior apical segment of the LV. Black arrows - pericardium enhancement. (E) Early Gadolinium Enhancement (TI 600 [ms]) in short axis; black arrows - thrombus on papillary muscles; yellow arrow – MVO area within the interventricular septum. (F) Steady-state free precession (SSFP) sequence end systolic image in short axis. Pericardial fluid surrounded LV and RV.
Figure 2.

Magnetic resonance images: black blood T2-weighted STIR images in long axis (A) and short axis (B); white arrows-subendocardial and transmural oedema. (C) Late Gadolinium Enhanced (LGE) images with fat saturation in long axis (C), and transverse (D) views. White arrows: infarct-like LGE pattern within subendocardial layer. Yellow arrows: extensive LGE with microvascular obstruction (MVO) in interventricular septum and anterior apical segment of the LV. Black arrows - pericardium enhancement. (E) Early Gadolinium Enhancement (TI 600 [ms]) in short axis; black arrows - thrombus on papillary muscles; yellow arrow – MVO area within the interventricular septum. (F) Steady-state free precession (SSFP) sequence end systolic image in short axis. Pericardial fluid surrounded LV and RV.

Chest CT axial images, lung window (A, B), mediastinal window (C) shows regression of lung airspace and ground -glass opacities (A, B). Some linear scars in the left lower lobe were observed (B). No pericardial effusion was present (C).
Figure 3.

Chest CT axial images, lung window (A, B), mediastinal window (C) shows regression of lung airspace and ground -glass opacities (A, B). Some linear scars in the left lower lobe were observed (B). No pericardial effusion was present (C).

Discussion

The presented case highlights four important and unusual characteristics EGPA: (1) atypical clinical manifestation without evidence of asthma, (2) extensive cardiac involvement as the dominant involved system, but diagnosed after specialized procedure, (3) contribution of CMRI in accurate diagnosis, and 4) difficulties in phenotype specificity.

EGPA characteristically develops in the following three consecutive phases: allergic, eosinophilic, and vasculitic phases.12 The first, allergic phase, is the prodromal phase characterized by asthma, allergic rhinitis, and sinusitis. The second, eosinophilic phase, manifests as peripheral eosinophilia and eosinophilic tissue infiltration. Lastly, the third, systemic vasculitic phase, shows peripheral neuropathy, skin symptoms, and/or glomerulonephritis or other symptoms of vasculitis. Asthma is a characteristic feature associated with EGPA, observed in almost all patients.13,14 Its presence is required for diagnosing the disease according to the Lanham’s criteria,12 and it is next to sinusitis in the diagnosis of EGPA, according to the American College of Rheumatology classification criteria.1 Asthma in EGPA is usually of late-onset, affecting between the age of 30 and 40 years, and mostly precedes the symptoms of systemic vasculitis.4 Furthermore, it is usually severe, antedates systemic manifestations by a mean duration of 12 years, and progresses to long-term persistent airflow obstruction despite initiation of corticosteroids in considerable number of patients, which affects long-term management and morbidity.13 According to the results of a recent study, severe rhinosinusitis, pulmonary infiltration, obesity, and severe asthma at vasculitis diagnosis, independently predicted severe asthma at the 3-year follow-up.15 Our patient deviates from this classical pattern. She did not show evident symptoms of asthma both in a physical examination as well as in pulmonary function tests. Admittedly, she did report a few months’ history of recurrent cough and dyspnea, but these symptoms subsided after antibiotic therapy alone. Hence, we speculate that not all patients with presumed EGPA have characteristic succession of disease stages, and the absence of the prodromal phase, especially of asthma, does not exclude the diagnosis of EGPA, but render the diagnosis more difficult. In our patient, severe and rapidly progressive eosinophilia required immediate cytoreduction and did not permit histological evaluation (for example, of the skin lesions). High levels of troponin T and BNP were strongly suggestive of cardiac damage by eosinophils, and further investigations such as ECHO and CMRI, helped in the diagnosis of EGPA.

Cardiac involvement is a serious systemic manifestation associated with poor prognosis, accounting for one-third of the deaths in EGPA patients.7 It is reported even in 60% of cases,16 and the most frequent manifestations are cardiomyopathy, pericarditis, and valvular disease;8,9 a considerably rarer symptom is coronary vasculitis,which could lead to myocardial infarction17 and death. The severity of clinical cardiac symptoms varies from mild to clinically overt life-threatening conditions, while some patients may be asymptomatic. Dennert et al,18 during a detailed cardiac evaluation of 32 ambulatory EGPA patients assumed to be in remission, revealed that 62% showed cardiac involvement. Among them, 66% showed ECG abnormalities (13% showed major changes), 50% showed abnormal findings on ECHO, and 62% revealed CMRI abnormalities. However, only 25% of these patients were symptomatic. In another study, clinical symptoms were reported in 42% EGPA cases, and the most common symptom was exertion dyspnoea,19 which was also observed in our patient.

The degree of cardiac involvement associated with eosinophilic infiltration could be related to the stimulus attracting the eosinophils, duration of eosinophilia, and degree of eosinophil activation. Deleterious effects on the heart are more common in cases of profound eosinophilia (≥5,000 cells/μl),20 which is consistent with the findings associated with our patient, in whom blood eosinophil count increased to 17,000 cells/μl. Three characteristic and successive stages of endomyocardial injury caused by eosinophils have been described.21 The first stage is a result of eosinophilic infiltration in the tissues, which leads to cell necrosis after the release of granular proteins. The second stage is represented by thrombosis formation, and the third stage corresponds to fibrotic scarring, which is an irreversible damage. The only potentially reversible phase of cardiac injury is the first stage, but most patients do not show any cardiac symptoms or may present only with non-specific signs. Early diagnosis is essential in such cases, because reduction in the eosinophil count due to early institution of treatment is crucial to limit myocardial necrosis. We hypothesized that clinical evaluation alone is not sufficient to exclude cardiac involvement, and two important points must be considered: rapid progression of cardiac injury in the course of eosinophilia, and the need to repeat basic cardiac examinations in patients diagnosed with eosinophilia, even if preliminary results are negative. Previously, our patient showed moderate eosinophilia (2,000 cells/μl), and the results of basic cardiac tests (ECHO and levels of cardiac serological markers) were normal, while 2 weeks later, the eosinophil count rose significantly (17,000 cells/μl), and features of severe cardiac damage were evident. Despite extensive cardiac disease, the clinical symptoms of cardiac involvement were almost non-existent and did not suggest the presence of any cardiac condition. Abnormalities in repeated routine tests led to the diagnosis of cardiac involvement and were the basis of further specialized definitive examination.

The only imaging modality to clearly depict cardiac involvement in EGPA is CMRI,22-26 which was evident in our patient. CMRI has optimal spatial and temporal resolutions without any need of radiation and clearly shows the cardiac complications characteristic of the disease. It can assess myocardial ischemia, coronary microvascular disease, myocardial fibrosis, pericardial inflammation, myocarditis, valvular lesions, and/or intraventricular thrombosis.27 The most important information provided by CMRI is the assessment of disease acuity. CMRI, using the combination of T2-weight, and early and late gadolinium enhancement, can distinguish acute from chronic inflammation.22 A CMRI study targeted to detect cardiac lesions and to monitor the treatment efficacy in EGPA patients with cardiac involvement revealed the presence of myocardial edema in 87.8% patients, perfusion defects in 54.5%, and late gadolinium enhancement indicative of replacement fibrosis, in all patients.19 In our case, CMRI lesions were typical of EGPA and similar to other described cases,28-30 but they are extensive and simultaneously affected all layers of the heart. The lesions included the myocardium, endocardium, and pericardium, the formation of wall thrombi at the apex of the left ventricle, and reduced the left-ventricular EF. Diffuse T2-weight signal elevation revealed the presence of myocardial edema, yielding the diagnosis of acute myocarditis, while late-gadolinium enhancement images showed diffuse contrast enhancement without the presence of any focal lesion. Areas of microinfarctions (the so-called “no -reflow” areas) resulting from vasculitis of small coronary vessels, as observed in our patient, are rare condition.22 The contribution of CMRI was invaluable in the diagnosis of EGPA.

EGPA, although classified as AAV, is a disease occupying a crossroad between ANCA vasculitis and eosinophilic inflammation, what was shown in our case. This dual pathology resulted in two phenotypes of the disease that could be distinguished by differing organ involvements between ANCA-positive and ANCA-negative patients. Two large-scale studies8,9 demonstrated that ANCA was positive in 38% EGPA patients. ANCA-positive patients showed the features of peripheral neuropathy, glomerulonephritis, and skin symptoms (the so-called “vasculitic” phenotype) more frequently, whereas endo-myocardial involvement and lung infiltration prevailed in the ANCA-negative subset (the so-called “tissular” phenotype). Further studies confirmed the differences in phenotypes based on ANCA status,31,32 and additionally revealed that EGPA comprised two genetically and clinically distinct subsets: ANCA-positive disease is an MHC (major histocompatibility complex) association with microscopic polyangiitis (MPA), while ANCA-negative–disease is genetically more similar to asthma.31 The new diagnostic criteria for EGPA proposed in 2013, which included the ANCA status,33 recommended that patients with asthma and blood eosinophil count <1,500 cells/μl without ANCA, vasculitis, or surrogates of vasculitis should be termed as hypereosinophilic asthma with systemic manifestations, non-vasculitis. Our patient cannot be assigned to a specific phenotype. She shared the features of both vasculitis and eosinophilic inflammation. She is a typical example of EGPA with overlapping features of hypereosinophilic syndrome (HES) and polyangiitis overlap syndrome (POS). On one hand, she showed skin and kidney symptoms, but on the other hand, eosinophilic cardiac inflammation dominated (although with intermediate features of inflammation in the small coronary vessels by CMRI). ANCA (both MPO- and PR3-) were not detected, which is more typical for the “tissular” phenotype (HES), and not for the “vasculitic” (POS) phenotype and hence, the patient did not show any symptom of asthma (Table 1). Some studies have confirmed that ANCA is an insufficient element to categorize EGPA patients with features of vasculitis, which was confirmed by the findings of our case. In a retrospective analysis of 157 patients, 47% patients with systemic vasculitis were ANCA negative, while 29% with MPO-ANCA did not show any features of vasculitis.34 Thus, in MPA and granulomatosis with polyangiitis (GPA), the pathogenic role of ANCA has been established,35,36 while in EGPA, the role of ANCA is still unclear, especially the association between ANCA and eosinophilic inflammation.

View this table:
Table 1.

Clinical features of our patient on the background of clinically subgroups of EGPA (based on the Furuta et al35)

Conclusion

We presented an atypical case of EGPA with no evidence of asthma, extensive cardiac involvement, and overlapping features of HES and POS. First, we observed that not all patients with presumed EGPA have characteristic succession of disease stages and the absence of the prodromal phase (especially of asthma), does not exclude the diagnosis of EGPA. Second, only clinical evaluation is not sufficient to exclude cardiac involvement in patients diagnosed with eosinophilia, and in every case, basic cardiac tests should be performed and repeated, even if preliminary results are negative. Third, the essential role of CMRI in diagnosing EGPA was highlighted, and finally, the heterogeneity of the disease obstructing the designation of specific disease phenotype was underscored.

Footnotes

  • Disclosure: The authors have declared no financial support or conflicts of interest relevant to this work. Written informed consent was obtained from the patient for the publication of this case report.

  • Received April 20, 2021.
  • Revision received February 12, 2022.
  • Accepted March 22, 2022.

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Clinical Medicine & Research

Vol. 20, Issue 3

1 Sep 2022

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Keywords

Asthma, Cardiac magnetic resonance imaging, Eosinophilic granulomatosis with polyangiitis, Phenotypes