Eosinophilic cardiomyopathy

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]

Overview

Eosinophillic Cardiomyopathy also known as Loeffler's Syndrome is a type of restrictive cardiomyopathy caused by eosinophillic infiltration of the endomyocardium. It is a feature of hypereosinophilic syndrome and occurs in 40-50% of all cases. Eosinophills enter the tissue and undergo degranulation; release cytotoxic proteins; increase production of reactive oxygen species, enzymes, growth factor, and cytokines. This process leads to tissue damage and dysfunction, eventually leading to fibrosis and restrictive cardiomyopathy. There are 3 stages of the eosinophilic cardiomyopathy: Stage 1 that is acute necrotic stage, stage 2 that is mural thrombus formation, and stage 3 that is ibrotic stage. There are many causes of hypereosinophilic syndrome (HES) with eosinophilic cardiomyopathy, these can be classified as reactive, conal myeloid disorder, and idiopathic hypereosinophillic syndrome.

Historical Perspective

  • Eosinophillic Cardiomypoathy was first discovered by Wilhem Loeffler, a Swiss Physician, in 1936.[1] [2]

Classification

  • Eosinophilic Cardiomyopathy may be classified according to cause into three subtypes/groups:[3][4]

Pathophysiology

  • The pathogenesis of eosinophilic cadiomyopathy is characterized by hypereosinophilia [11], thrombi formation [12], restrictive cardiomyopathy[13] [14], and heart failure [15].[16]
  • The FLP1L1-PDGFRA fusion gene has been associated with the development chronic eosinophilic leukemia [17]and hypereosiniophilic syndrome.[18] [19]
  • The PDGFRa, PDGFRb, and PDGFR1 genes have been associated with the development of clonal myeloid disorders leading to hypereosiniophilic syndrome.[20] [21]
  • On gross pathology, cardiac hypertrophy and fibrosis are characteristic findings of Eosinophilic Cardiomyopathy.[22]
  • On microscopic histopathological analysis, hypereosinophilia, myocardial and myofibrillar disarray, and endoperimysial interstitial fibrosis are characteristic findings of Eosinophilic Cardiomyopathy.[23]

Clinical Features

Differentiating [disease name] from other Diseases

Epidemiology and Demographics

Age

  • Patients of all age groups may develop ecosinophilic cardiomyopathy.[34]
  • Eosinopilic cardiomyopathy is more commonly observed among patients aged 20-50 years old.[35]

Gender

  • Men are more commonly affected with eosinophilic cadiomyopathy than Females.[36]
  • The male to female ratio is approximately 1.47. [37]

Race

  • There is no racial predilection for eosinophilic cardiomyopathy.

Risk Factors

Natural History, Complications and Prognosis

  • Prognosis is generally good, and depends on its etiology.[42]

Diagnosis

Diagnostic Criteria

  • An elevated eosinophil count (>1500/mm3) on 2 separate tests (≥1 mo).
  • Tissue hypereosinophilia based on >20% eosinophils in a bone marrow section.
  • Marked disposition of eosinophilic granule proteins in tissue plus organ damage directly due to hypereosinophilia.

Symptoms

Physical Examination

Laboratory Findings

Imaging Findings

  • Cardiac MRI is the imaging diagnostic study of choice for eosinophilic cardiomyopathy.[53]
  • On cardiac MRI, eosinophilic cardiomyopathy is characterized by hyper-enhancement and thrombus formation.[54]
  • Echocardiography may demonstrate:[55]
    • Endomyocardial thickening
    • Ventricular thrombus formation
    • Mitral valve involvement

Other Diagnostic Studies

Treatment

Medical Therapy

Surgery

  • Valve replacement may be performed for patients with valvular damage in eosinophilic cardiomyopathy.[63]
  • Cardiac transplant may be performed for patients with irreversible damage in eosinophilic cardiomyopathy.[64]

Prevention

  • There are no primary preventive measures available for eosinophilic cardiomyopathy.

References

  1. Christopher C. Cheung, Maggie Constantine, Amir Ahmadi, Carolyn Shiau & Luke Y. C. Chen (2017). "Eosinophilic Myocarditis". The American journal of the medical sciences. 354 (5): 486–492. doi:10.1016/j.amjms.2017.04.002. PMID 29173361. Unknown parameter |month= ignored (help)
  2. Amit Alam, Shankar Thampi, Shahryar G. Saba & Rita Jermyn (2017). "Loeffler Endocarditis: A Unique Presentation of Right-Sided Heart Failure Due to Eosinophil-Induced Endomyocardial Fibrosis". Clinical medicine insights. Case reports. 10: 1179547617723643. doi:10.1177/1179547617723643. PMID 28890659.
  3. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  4. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  5. Christopher C. Cheung, Maggie Constantine, Amir Ahmadi, Carolyn Shiau & Luke Y. C. Chen (2017). "Eosinophilic Myocarditis". The American journal of the medical sciences. 354 (5): 486–492. doi:10.1016/j.amjms.2017.04.002. PMID 29173361. Unknown parameter |month= ignored (help)
  6. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  7. Christopher C. Cheung, Maggie Constantine, Amir Ahmadi, Carolyn Shiau & Luke Y. C. Chen (2017). "Eosinophilic Myocarditis". The American journal of the medical sciences. 354 (5): 486–492. doi:10.1016/j.amjms.2017.04.002. PMID 29173361. Unknown parameter |month= ignored (help)
  8. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  9. Christopher C. Cheung, Maggie Constantine, Amir Ahmadi, Carolyn Shiau & Luke Y. C. Chen (2017). "Eosinophilic Myocarditis". The American journal of the medical sciences. 354 (5): 486–492. doi:10.1016/j.amjms.2017.04.002. PMID 29173361. Unknown parameter |month= ignored (help)
  10. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  11. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  12. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  13. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  14. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  15. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  16. M. Arima & T. Kanoh (1999). "Eosinophilic myocarditis associated with dense deposits of eosinophil cationic protein (ECP) in endomyocardium with high serum ECP". Heart (British Cardiac Society). 81 (6): 669–671. PMID 10336931. Unknown parameter |month= ignored (help)
  17. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  18. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  19. Jason Gotlib (2015). "World Health Organization-defined eosinophilic disorders: 2015 update on diagnosis, risk stratification, and management". American journal of hematology. 90 (11): 1077–1089. doi:10.1002/ajh.24196. PMID 26486351. Unknown parameter |month= ignored (help)
  20. Christopher C. Cheung, Maggie Constantine, Amir Ahmadi, Carolyn Shiau & Luke Y. C. Chen (2017). "Eosinophilic Myocarditis". The American journal of the medical sciences. 354 (5): 486–492. doi:10.1016/j.amjms.2017.04.002. PMID 29173361. Unknown parameter |month= ignored (help)
  21. Jason Gotlib (2015). "World Health Organization-defined eosinophilic disorders: 2015 update on diagnosis, risk stratification, and management". American journal of hematology. 90 (11): 1077–1089. doi:10.1002/ajh.24196. PMID 26486351. Unknown parameter |month= ignored (help)
  22. Gustav Mattsson & Peter Magnusson (2017). "Eosinophilic granulomatosis with polyangiitis: myocardial thickening reversed by corticosteroids". BMC cardiovascular disorders. 17 (1): 299. doi:10.1186/s12872-017-0734-8. PMID 29262787. Unknown parameter |month= ignored (help)
  23. A. Angelini, V. Calzolari, G. Thiene, G. M. Boffa, M. Valente, L. Daliento, C. Basso, F. Calabrese, R. Razzolini, U. Livi & R. Chioin (1997). "Morphologic spectrum of primary restrictive cardiomyopathy". The American journal of cardiology. 80 (8): 1046–1050. PMID 9352976. Unknown parameter |month= ignored (help)
  24. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  25. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  26. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  27. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  28. Nooreen Hussain, Preeti Patel, Jonathan Yin, Rachael Davis & Ossama Ikladios (2019). "A case of Loeffler's endocarditis after initiation of adalimumab". Journal of community hospital internal medicine perspectives. 9 (1): 29–32. doi:10.1080/20009666.2018.1562852. PMID 30788072.
  29. Petar M. Seferovic, Marija Polovina, Johann Bauersachs, Michael Arad, Tuvia Ben Gal, Lars H. Lund, Stephan B. Felix, Eloisa Arbustini, Alida L. P. Caforio, Dimitrios Farmakis, Gerasimos S. Filippatos, Elias Gialafos, Vladimir Kanjuh, Gordana Krljanac, Giuseppe Limongelli, Ales Linhart, Alexander R. Lyon, Ruzica Maksimovic, Davor Milicic, Ivan Milinkovic, Michel Noutsias, Ali Oto, Oztekin Oto, Sinisa U. Pavlovic, Massimo F. Piepoli, Arsen D. Ristic, Giuseppe M. C. Rosano, Hubert Seggewiss, Milika Asanin, Jelena P. Seferovic, Frank Ruschitzka, Jelena Celutkiene, Tiny Jaarsma, Christian Mueller, Brenda Moura, Loreena Hill, Maurizio Volterrani, Yuri Lopatin, Marco Metra, Johannes Backs, Wilfried Mullens, Ovidiu Chioncel, Rudolf de Boer, Stefan Anker, Claudio Rapezzi, Andrew J. S. Coats & Carsten Tschope (2019). "Heart failure in cardiomyopathies: a position paper from the Heart Failure Association of the European Society of Cardiology". European journal of heart failure. doi:10.1002/ejhf.1461. PMID 30989768. Unknown parameter |month= ignored (help)
  30. Adeyemi Adedamola Taiwo, Lavanya Alapati & Assad Movahed (2019). "Cardiac amyloidosis: A case report and review of literature". World journal of clinical cases. 7 (6): 742–752. doi:10.12998/wjcc.v7.i6.742. PMID 30968039. Unknown parameter |month= ignored (help)
  31. Jian Liang Tan & Sandeep K. Sharma (2018). "Cardiac sarcoidosis presenting with syncope and rapidly progressive atrioventricular block: a case report". European heart journal. Case reports. 2 (4): yty103. doi:10.1093/ehjcr/yty103. PMID 31020179. Unknown parameter |month= ignored (help)
  32. Kristen N.. Brown & Rene R.. Diaz (2019). "Restrictive (Infiltrative) Cardiomyopathy". PMID 30725919. Unknown parameter |month= ignored (help)
  33. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  34. Jason Gotlib (2015). "World Health Organization-defined eosinophilic disorders: 2015 update on diagnosis, risk stratification, and management". American journal of hematology. 90 (11): 1077–1089. doi:10.1002/ajh.24196. PMID 26486351. Unknown parameter |month= ignored (help)
  35. Jason Gotlib (2015). "World Health Organization-defined eosinophilic disorders: 2015 update on diagnosis, risk stratification, and management". American journal of hematology. 90 (11): 1077–1089. doi:10.1002/ajh.24196. PMID 26486351. Unknown parameter |month= ignored (help)
  36. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  37. Jason Gotlib (2015). "World Health Organization-defined eosinophilic disorders: 2015 update on diagnosis, risk stratification, and management". American journal of hematology. 90 (11): 1077–1089. doi:10.1002/ajh.24196. PMID 26486351. Unknown parameter |month= ignored (help)
  38. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  39. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  40. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  41. Paulo Dinis, Rogerio Teixeira, Luis Puga, Carolina Lourenco, Maria Carmo Cachulo & Lino Goncalves (2018). "Eosinophilic Myocarditis: Clinical Case and Literature Review". Arquivos brasileiros de cardiologia. 110 (6): 597–599. doi:10.5935/abc.20180089. PMID 30226920. Unknown parameter |month= ignored (help)
  42. Paulo Dinis, Rogerio Teixeira, Luis Puga, Carolina Lourenco, Maria Carmo Cachulo & Lino Goncalves (2018). "Eosinophilic Myocarditis: Clinical Case and Literature Review". Arquivos brasileiros de cardiologia. 110 (6): 597–599. doi:10.5935/abc.20180089. PMID 30226920. Unknown parameter |month= ignored (help)
  43. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  44. Peter Valent, Amy D. Klion, Hans-Peter Horny, Florence Roufosse, Jason Gotlib, Peter F. Weller, Andrzej Hellmann, Georgia Metzgeroth, Kristin M. Leiferman, Michel Arock, Joseph H. Butterfield, Wolfgang R. Sperr, Karl Sotlar, Peter Vandenberghe, Torsten Haferlach, Hans-Uwe Simon, Andreas Reiter & Gerald J. Gleich (2012). "Contemporary consensus proposal on criteria and classification of eosinophilic disorders and related syndromes". The Journal of allergy and clinical immunology. 130 (3): 607–612. doi:10.1016/j.jaci.2012.02.019. PMID 22460074. Unknown parameter |month= ignored (help)
  45. Ming Gao, Weihua Zhang, Waiou Zhao, Ling Qin, Fei Pei & Yang Zheng (2018). "Loeffler endocarditis as a rare cause of heart failure with preserved ejection fraction: A case report and review of literature". Medicine. 97 (11): e0079. doi:10.1097/MD.0000000000010079. PMID 29538200. Unknown parameter |month= ignored (help)
  46. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  47. Petar M. Seferovic, Marija Polovina, Johann Bauersachs, Michael Arad, Tuvia Ben Gal, Lars H. Lund, Stephan B. Felix, Eloisa Arbustini, Alida L. P. Caforio, Dimitrios Farmakis, Gerasimos S. Filippatos, Elias Gialafos, Vladimir Kanjuh, Gordana Krljanac, Giuseppe Limongelli, Ales Linhart, Alexander R. Lyon, Ruzica Maksimovic, Davor Milicic, Ivan Milinkovic, Michel Noutsias, Ali Oto, Oztekin Oto, Sinisa U. Pavlovic, Massimo F. Piepoli, Arsen D. Ristic, Giuseppe M. C. Rosano, Hubert Seggewiss, Milika Asanin, Jelena P. Seferovic, Frank Ruschitzka, Jelena Celutkiene, Tiny Jaarsma, Christian Mueller, Brenda Moura, Loreena Hill, Maurizio Volterrani, Yuri Lopatin, Marco Metra, Johannes Backs, Wilfried Mullens, Ovidiu Chioncel, Rudolf de Boer, Stefan Anker, Claudio Rapezzi, Andrew J. S. Coats & Carsten Tschope (2019). "Heart failure in cardiomyopathies: a position paper from the Heart Failure Association of the European Society of Cardiology". European journal of heart failure. doi:10.1002/ejhf.1461. PMID 30989768. Unknown parameter |month= ignored (help)
  48. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  49. Petar M. Seferovic, Marija Polovina, Johann Bauersachs, Michael Arad, Tuvia Ben Gal, Lars H. Lund, Stephan B. Felix, Eloisa Arbustini, Alida L. P. Caforio, Dimitrios Farmakis, Gerasimos S. Filippatos, Elias Gialafos, Vladimir Kanjuh, Gordana Krljanac, Giuseppe Limongelli, Ales Linhart, Alexander R. Lyon, Ruzica Maksimovic, Davor Milicic, Ivan Milinkovic, Michel Noutsias, Ali Oto, Oztekin Oto, Sinisa U. Pavlovic, Massimo F. Piepoli, Arsen D. Ristic, Giuseppe M. C. Rosano, Hubert Seggewiss, Milika Asanin, Jelena P. Seferovic, Frank Ruschitzka, Jelena Celutkiene, Tiny Jaarsma, Christian Mueller, Brenda Moura, Loreena Hill, Maurizio Volterrani, Yuri Lopatin, Marco Metra, Johannes Backs, Wilfried Mullens, Ovidiu Chioncel, Rudolf de Boer, Stefan Anker, Claudio Rapezzi, Andrew J. S. Coats & Carsten Tschope (2019). "Heart failure in cardiomyopathies: a position paper from the Heart Failure Association of the European Society of Cardiology". European journal of heart failure. doi:10.1002/ejhf.1461. PMID 30989768. Unknown parameter |month= ignored (help)
  50. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  51. Jason Gotlib (2015). "World Health Organization-defined eosinophilic disorders: 2015 update on diagnosis, risk stratification, and management". American journal of hematology. 90 (11): 1077–1089. doi:10.1002/ajh.24196. PMID 26486351. Unknown parameter |month= ignored (help)
  52. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  53. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  54. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  55. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  56. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  57. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  58. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
  59. Princess U. Ogbogu, Douglas R. Rosing & McDonald K. 3rd Horne (2007). "Cardiovascular manifestations of hypereosinophilic syndromes". Immunology and allergy clinics of North America. 27 (3): 457–475. doi:10.1016/j.iac.2007.07.001. PMID 17868859. Unknown parameter |month= ignored (help)
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