Understanding organ dysfunction in hemophagocytic lymphohistiocytosis

Intensive Care Medicine

Volumn 34, Issue 7, 2008, Pages 1177-1187

  Créput, Caroline ^a   Galicier, Lionel ^a   Buyse, Sophie ^a   Azoulay, Elie ^a  

^a SAINT LOUIS HOSPITAL   (France)

Author keywords

Autoimmune disease; Cytopenia; Hemophagocytosis; Histiocytosis; Langerhans cells; Th1 Cytokines activation

Indexed keywords

ANTIBIOTIC AGENT; ANTIFUNGAL AGENT; ANTIVIRUS AGENT; CORTICOSTEROID; CYCLOSPORIN; ETANERCEPT; ETOPOSIDE; IMMUNOGLOBULIN; INFLIXIMAB; STEROID; VASOACTIVE AGENT;

BACTERIAL INFECTION; BONE MARROW; CONNECTIVE TISSUE DISEASE; CORRELATION ANALYSIS; CYTOPATHOLOGY; DISEASE SEVERITY; EARLY DIAGNOSIS; EARLY INTERVENTION; ERYTHROPHAGOCYTOSIS; HEART; HEMOPHAGOCYTIC LYMPHOHISTIOCYTOSIS; HISTOPATHOLOGY; HUMAN; IMMUNE DEFICIENCY; INTENSIVE CARE; KIDNEY; LABORATORY TEST; LIVER; LUNG; LUPUS VULGARIS; LYMPH NODE; LYMPHOPROLIFERATIVE DISEASE; MORTALITY; MULTIPLE ORGAN FAILURE; MYCOSIS; NATURAL KILLER CELL; PARASITOSIS; PATHOPHYSIOLOGY; PRACTICE GUIDELINE; PROGNOSIS; REVIEW; SEPSIS; SKIN; SPLEEN; SURVIVAL RATE; TREATMENT PLANNING; VIRUS INFECTION;

HISTIOCYTES; HUMANS; INFECTION; LYMPHOHISTIOCYTOSIS, HEMOPHAGOCYTIC; PROGNOSIS; TH1 CELLS;

EID: 46149083954     PISSN: 03424642     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00134-008-1111-y     Document Type: Review

References (95)

1. Scott R, Robb-Smith A (1939) Histiocytic medullary reticulosis. Lancet 2:194-198
2. Risdall RJ, McKenna RW, Nesbit ME, Krivit W, Balfour HH Jr, Simmons RL, Brunning RD (1979) Virus-associated hemophagocytic syndrome: a benign histiocytic proliferation distinct from malignant histiocytosis. Cancer 44:993-1002
3. Cohen RA, Hutter JJ Jr, Boxer MA, Goldman DS (1980) Histiocytic medullary reticulosis associated with acute Epstein-Barr (EB) virus infection. Am J Pediatr Hematol Oncol 2:245-248
4. McKenna RW, Risdall RJ, Brunning RD (1981) Virus associated hemophagocytic syndrome. Hum Pathol 12:395-398
5. Wilson ER, Malluh A, Stagno S, Crist WM (1981) Fatal Epstein-Barr virus-associated hemophagocytic syndrome. J Pediatr 98:260-262
6. Ezdinli EZ, Kucuk O, Chedid A, Sinclair TF, Thomas K, Singh S, Sarpel S, Jovanovic L (1986) Hypogammaglobulinemia and hemophagocytic syndrome associated with lymphoproliferative disorders. Cancer 57:1024-1037
7. Liang DC, Chu ML, Shih CC (1986) Reactive histiocytosis in acute lymphoblastic leukemia and non-Hodgkin's lymphoma. Cancer 58:1289-1284
8. March LM, Webb J, Eckstein RP (1986) Cytophagic panniculitis. Aust N Z J Med 16:397-401
9. Gauvin F, Toledano B, Champagne J, Lacroix J (2000) Reactive hemophagocytic syndrome presenting as a component of multiple organ dysfunction syndrome. Crit Care Med 28:3341-3345
10. Strauss R, Neureiter D, Westenburger B, Wehler M, Kirchner T, Hahn EG (2004) Multifactorial risk analysis of bone marrow histiocytic hyperplasia with hemophagocytosis in critically ill medical patients: a postmortem clinicopathologic analysis. Crit Care Med 32:1316-1321
11. Nahum E, Ben-Ari J, Stain J, Schonfeld T (2000) Hemophagocytic lymphohistiocytic syndrome: unrecognized cause of multiple organ failure. Pediatr Crit Care Med 1:51-54
12. Stephan F, Thioliere B, Verdy E, Tulliez M (1997) Role of hemophagocytic histiocytosis in the etiology of thrombocytopenia in patients with sepsis syndrome or septic shock. Clin Infect Dis 25:1159-1164
13. Grom AA (2003) Macrophage activation syndrome and reactive hemophagocytic lymphohistiocytosis: The same entities? Curr Opin Rheumatol 15:587-590
14. Dinarello CA, Wolff SM (1993) The role of interleukin-1 in disease. N Engl J Med 328:106-113
15. Dinarello CA, Cannon JG (1993) Cytokine measurements in septic shock. Ann Intern Med 119:853-854
16. Reiner AP, Spivak JL (1988) Hematophagic histiocytosis. A report of 23 new patients and a review of the literature. Medicine (Baltimore) 67:369-388
17. Shirono K, Tsuda H (1995) Virus-associated haemophagocytic syndrome in previously healthy adults. Eur J Haematol 55:240-244
18. Ohta H, Yumara-Yagi K, Sakata N, Inoue M, Kawa-Ha K (1994) Capillary leak syndrome in patients with hemophagocytic lymphohistiocytosis. Acta Paediatr 83:1113-1114
19. Honig LS, Snipes GJ, Vogel H, Horoupian DS (1991) Sensorimotor neuropathy in hemophagocytosis syndrome. Acta Neurol Scand 84:316-320
20. Hanada T, Ono I, Iinuma S, Nagai Y (1989) Pure red cell aplasia in association with virus associated haemophagocytic syndrome (VAHS). Br J Haematol 73:570-571
21. Koduri PR, Carandang G, DeMarais P, Patel AR (1995) Hyperferritinemia in reactive hemophagocytic syndrome report of four adult cases. Am J Hematol 49:247-249
22. Esumi N, Ikushima S, Todo S, Imashuku S (1987) Hyperferritinemia in malignant histiocytosis and virus-associated hemophagocytic syndrome. N Engl J Med 316:346-347
23. Esumi N, Ikushima S, Hibi S, Todo S, Imashuku S (1988) High serum ferritin level as a marker of malignant histiocytosis and virus-associated hemophagocytic syndrome. Cancer 61:2071-2076
24. Dinarello CA, Gelfand JA, Wolff SM (1993) Anticytokine strategies in the treatment of the systemic inflammatory response syndrome. J Am Med Assoc 269:1829-1835
25. Henter JI, Carlson LA, Soder O, Nilsson-Ehle P, Elinder G (1991) Lipoprotein alterations and plasma lipoprotein lipase reduction in familial hemophagocytic lymphohistiocytosis. Acta Paediatr Scand 80:675-681
26. Ooe K (1992) Pathogenesis and clinical significance of hemophagocytic syndrome: hypothesis. Pediatr Pathol 12:309-312
27. McClure PD, Strachan P, Saunders EF (1974) Hypofibrinogenemia and thrombocytopenia in familial hemophagocytic reticulosis. J Pediatr 85:67-70
28. de Kerguenec C, Hillaire S, Molinie V, Gardin C, Degott C, Erlinger S, Valla D (2001) Hepatic manifestations of hemophagocytic syndrome: a study of 30 cases. Am J Gastroenterol 96:852-857
29. Billiau AD, Roskams T, Van Damme-Lombaerts R, Matthys P, Wouters C (2005) Macrophage activation syndrome: characteristic findings on liver biopsy illustrating the key role of activated, IFN-gamma-producing lymphocytes and IL-6- and TNF-alpha-producing macrophages. Blood 105:1648-1651
30. Whiting JF, Green RM, Rosenbluth AB, Gollan JL (1995) Tumor necrosis factor-alpha decreases hepatocyte bile salt uptake and mediates endotoxin-induced cholestasis. Hepatology 22:1273-1278
31. Iso ON, Hashimoto N, Tanaka A, Sunaga S, Oka T, Kurokawa K, Watanabe T (1998) Cytokine-induced hypoalbuminemia in a patient with hemophagocytic syndrome: direct in vitro evidence for the role of tumor necrosis factor-alpha. Dig Dis Sci 43:67-73
32. Weber J, Yang JC, Topalian SL, Parkinson DR, Schwartzentruber DS, Ettinghausen SE, Gunn H, Mixon A, Kim H, Cole D et al. (1993) Phase I trial of subcutaneous interleukin-6 in patients with advanced malignancies. J Clin Oncol 11:499-506
33. Braun MC, Cohn RA, Kletzel M (1996) Nephrotic syndrome accompanying familial hemophagocytic syndrome. J Pediatr Hematol Oncol 18:195-197
34. Thaunat O, Delahousse M, Fakhouri F, Martinez F, Stephan JL, Noel LH, Karras A (2006) Nephrotic syndrome associated with hemophagocytic syndrome. Kidney Int 69:1892-1898
35. Chubachi A, Miura I, Hatano Y, Ohshima A, Nishinari T, Miura AB (1995) Syndrome of inappropriate secretion of antidiuretic hormone in patients with lymphoma-associated hemophagocytic syndrome. Ann Hematol 70:53-55
36. Favara BE (1996) Histopathology of the liver in histiocytosis syndromes. Pediatr Pathol Lab Med 16:413-433
37. Janka GE (2007) Hemophagocytic syndromes. Blood Rev 21:245-253
38. Danish EH, Dahms BB, Kumar ML (1985) Cytomegalovirus-associated hemophagocytic syndrome. Pediatrics 75:280-283
39. Lasserre M, Huguet C, Terno O (1993) Acute severe herpes simplex hepatitis with virus-associated hemophagocytic syndrome in an immunocompetent adult. J Hepatol 18:256-257
40. Boruchoff SE, Woda BA, Pihan GA, Durbin WA, Burstein D, Blacklow NR (1990) Parvovirus B19-associated hemophagocytic syndrome. Arch Intern Med 150:897-899
41. Morimoto A, Teramura T, Asazuma Y, Mukoyama A, Imashuku S (2003) Hemophagocytic syndrome associated with severe adenoviral pneumonia: usefulness of real-time polymerase chain reaction for diagnosis. Int J Hematol 77:295-298
42. Kyoda K, Nakamura S, Machi T, Kitagawa S, Ohtake S, Matsuda T (1998) Acute hepatitis A virus infection-associated hemophagocytic syndrome. Am J Gastroenterol 93:1187-1188
43. Guerin C, Pozzetto B, Berthoux F (1989) Hemophagocytic syndrome associated with coxsackie virus A 9 infection in a non-immunosuppressed adult. Intensive Care Med 15:547-548
44. Henter JI, Chow CB, Leung CW, Lau YL (2006) Cytotoxic therapy for severe avian influenza A (H5N1) infection. Lancet 367:870-873
45. Chen TL, Wong WW, Chiou TJ (2003) Hemophagocytic syndrome: an unusual manifestation of acute human immunodeficiency virus infection. Int J Hematol 78:450-452
46. Baraldes MA, Domingo P, Gonzalez MJ, Aventin A, Coll P (1998) Tuberculosis-associated hemophagocytic syndrome in patients with acquired immunodeficiency syndrome. Arch Intern Med 158:194-195
47. Yang WK, Fu LS, Lan JL, Shen GH, Chou G, Tseng CF, Chi CS (2003) Mycobacterium avium complex-associated hemophagocytic syndrome in systemic lupus erythematosus patient: report of one case. Lupus 12:312-316
48. Masri K, Mahon N, Rosario A, Mirza I, Keys TF, Ratliff NB, Starling RC (2003) Reactive hemophagocytic syndrome associated with disseminated histoplasmosis in a heart transplant recipient. J Heart Lung Transplant 22:487-491
49. Kumar N, Jain S, Singh ZN (2000) Disseminated histoplasmosis with reactive hemophagocytosis: aspiration cytology findings in two cases. Diagn Cytopathol 23:422-424
50. Kontopoulou T, Tsaousis G, Vaidakis E, Fanourgiakis P, Michalakeas E, Trigoni E, Samarkos M (2002) Hemophagocytic syndrome in association with visceral leishmaniasis. Am J Med 113:439-440
51. Tapisiz A, Belet N, Ciftci E, Ince E, Dogru U (2007) Hemophagocytic lymphohistiocytosis associated with visceral leishmaniasis. J Trop Pediatr 11:11
52. Taillan B, Ferrari E, Heudier P, Fuzibet JG, Dujardin P (1991) Hemophagocytic syndrome in pneumocystosis. Presse Med 20:1456-1457 [in French]
53. Garcia Escudero A, Benitez Moya JM, Lag Asturiano E (2000) Hemophagocytic syndrome and invasive aspergillosis in a patient with Churg-Strauss vasculitis. Med Clin (Barc) 115:598 [in Spanish]
54. Bhatia S, Bauer F, Bilgrami SA (2003) Candidiasis-associated hemophagocytic lymphohistiocytosis in a patient infected with human immunodeficiency virus. Clin Infect Dis 37:e161-e166
55. Jaffe ES, Costa J, Fauci AS, Cossman J, Tsokos M (1983) Malignant lymphoma and erythrophagocytosis simulating malignant histiocytosis. Am J Med 75:741-749
56. Chuang HC, Lay JD, Hsieh WC, Su IJ (2007) Pathogenesis and mechanism of disease progression from hemophagocytic lymphohistiocytosis to Epstein-Barr virus-associated T-cell lymphoma: nuclear factor-kappa B pathway as a potential therapeutic target. Cancer Sci 98:1281-1287
57. Janka G, Imashuku S, Elinder G, Schneider M, Henter JI (1998) Infection- and malignancy-associated hemophagocytic syndromes. Secondary hemophagocytic lymphohistiocytosis. Hematol Oncol Clin North Am 12:435-444
58. Kojima H, Takei N, Mukai Y, Hasegawa Y, Suzukawa K, Nagata M, Noguchi M, Mori N, Nagasawa T (2003) Hemophagocytic syndrome as the primary clinical symptom of Hodgkin's disease. Ann Hematol 82:53-56
59. Aouba A, Lambotte O, Vasiliu V, Divine M, Valensi F, Varet B, Bazarbachi A, Hermine O (2004) Hemophagocytic syndrome as a presenting sign of transformation of smoldering to acute adult T-cell leukemia/lymphoma: efficacy of anti-retroviral and interferon therapy. Am J Hematol 76:187-189
60. Srichaikul T, Punyagupta S, Mongkolsritrakul W, Jidpugdeebodin S (2004) EBV and hemophagocytic syndrome: analysis of 3 cases, with speculation on clinical features, therapy and role of EBV. J Med Assoc Thai 87:974-983
61. Fardet L, Blum L, Kerob D, Agbalika F, Galicier L, Dupuy A, Lafaurie M, Meignin V, Morel P, Lebbe C (2003) Human herpesvirus 8-associated hemophagocytic lymphohistiocytosis in human immunodeficiency virus-infected patients. Clin Infect Dis 37:285-291
62. Seliem RM, Griffith RC, Harris NL, Beheshti J, Schiffman FJ, Longtine J, Kutok J, Ferry JA (2007) HHV-8+, EBV+ multicentric plasmablastic microlymphoma in an HIV+ Man: the spectrum of HHV-8+ lymphoproliferative disorders expands. Am J Surg Pathol 31:1439-1445
63. Li CF, Ye H, Liu H, Du MQ, Chuang SS (2006) Fatal HHV-8-associated hemophagocytic syndrome in an HIV-negative immunocompetent patient with plasmablastic variant of multicentric Castleman disease (plasmablastic microlymphoma). Am J Surg Pathol 30:123-127
64. Okuda T, Sakamoto S, Deguchi T, Misawa S, Kashima K, Yoshihara T, Ikushima S, Hibi S, Imashuku S (1991) Hemophagocytic syndrome associated with aggressive natural killer cell leukemia. Am J Hematol 38:321-323
65. Ma L, Bandarchi B, Glusac EJ (2005) Fatal subcutaneous panniculitis-like T-cell lymphoma with interface change and dermal mucin, a dead ringer for lupus erythematosus. J Cutan Pathol 32:360-365
66. Palazzi DL, McClain KL, Kaplan SL (2003) Hemophagocytic syndrome after Kawasaki disease. Pediatr Infect Dis J 22:663-666
67. al-Eid W, al-Jefri A, Bahabri S, al-Mayouf S (2000) Hemophagocytosis complicating Kawasaki disease. Pediatr Hematol Oncol 17:323-329
68. Okada M, Suzuki K, Hidaka T, Shinohara T, Kataharada K, Matsumoto M, Takada K, Ohsuzu F (2001) Hemophagocytic syndrome in systemic lupus erythematosus. Intern Med 40:1263-1264
69. Sekigawa I, Suzuki J, Nawata M, Ikeda K, Koike M, Iida N, Hashimoto H, Oshimi K (2001) Hemophagocytosis in autoimmune disease. Clin Exp Rheumatol 19:333-338
70. Dhote R, Simon J, Papo T, Detournay B, Sailler L, Andre MH, Dupond JL, Larroche C, Piette AM, Mechenstock D, Ziza JM, Arlaud J, Labussiere AS, Desvaux A, Baty V, Blanche P, Schaeffer A, Piette JC, Guillevin L, Boissonnas A, Christoforov B (2003) Reactive hemophagocytic syndrome in adult systemic disease: report of twenty-six cases and literature review. Arthritis Rheum 49:633-639
71. Menasche G, Feldmann J, Fischer A, Basile Gde S (2005) Primary hemophagocytic syndromes point to a direct link between lymphocyte cytotoxicity and homeostasis. Immunol Rev 203:165-179
72. Egeler RM, Shapiro R, Loechelt B, Filipovich A (1996) Characteristic immune abnormalities in hemophagocytic lymphohistiocytosis. J Pediatr Hematol Oncol 18:340-345
73. Osugi Y, Hara J, Tagawa S, Takai K, Hosoi G, Matsuda Y, Ohta H, Fujisaki H, Kobayashi M, Sakata N, Kawa-Ha K, Okada S, Tawa A (1997) Cytokine production regulating Th1 and Th2 cytokines in hemophagocytic lymphohistiocytosis. Blood 89:4100-4103
74. Akashi K, Hayashi S, Gondo H, Mizuno S, Harada M, Tamura K, Yamasaki K, Shibuya T, Uike N, Okamura T et al. (1994) Involvement of interferon-gamma and macrophage colony-stimulating factor in pathogenesis of haemophagocytic lymphohistiocytosis in adults. Br J Haematol 87:243-250
75. Hasegawa D, Kojima S, Tatsumi E, Hayakawa A, Kosaka Y, Nakamura H, Sako M, Osugi Y, Nagata S, Sano K (1998) Elevation of the serum Fas ligand in patients with hemophagocytic syndrome and Diamond-Blackfan anemia. Blood 91:2793-2799
76. Imashuku S, Hibi S, Sako M, Ishida Y, Mugishima H, Chen J, Tsunematsu Y (1995) Soluble interleukin-2 receptor: a useful prognostic factor for patients with hemophagocytic lymphohistiocytosis. Blood 86:4706-4707
77. Imashuku S, Hibi S (1991) Cytokines in hemophagocytic syndrome. Br J Haematol 77:438-440
78. Henter JI, Elinder G, Soder O, Hansson M, Andersson B, Andersson U (1991) Hypercytokinemia in familial hemophagocytic lymphohistiocytosis. Blood 78:2918-2922
79. Fujiwara F, Hibi S, Imashuku S (1993) Hypercytokinemia in hemophagocytic syndrome. Am J Pediatr Hematol Oncol 15:92-98
80. Castilletti C, Preziosi R, Bernardini G, Caterini A, Gomes V, Calcaterra S, Carletti F, Capobianchi MR, Armignacco O (2004) Hemophagocytic syndrome in a patient with acute human immunodeficiency virus infection. Clin Infect Dis 38:1792-1793
81. Lambotte O, Khellaf M, Harmouche H, Bader-Meunier B, Manceron V, Goujard C, Amoura Z, Godeau B, Piette JC, Delfraissy JF (2006) Characteristics and long-term outcome of 15 episodes of systemic lupus erythematosus-associated hemophagocytic syndrome. Medicine (Baltimore) 85:169-182
82. Karras A, Thervet E, Legendre C (2004) Hemophagocytic syndrome in renal transplant recipients: report of 17 cases and review of literature. Transplantation 77:238-243
83. Lin MT, Chang HM, Huang CJ, Chen WL, Lin CY, Lin CY, Chuang SS (2007) Massive expansion of EBV+ monoclonal T cells with CD5 down regulation in EBV-associated haemophagocytic lymphohistiocytosis. J Clin Pathol 60:101-103
84. Chuang HC, Lay JD, Chuang SE, Hsieh WC, Chang Y, Su IJ (2007) Epstein-Barr virus (EBV) latent membrane protein-1 down-regulates tumor necrosis factor-alpha (TNF-alpha) receptor-1 and confers resistance to TNF-alpha-induced apoptosis in T cells: implication for the progression to T-cell lymphoma in EBV-associated hemophagocytic syndrome. Am J Pathol 170:1607-1617
85. Kaito K, Kobayashi M, Katayama T, Otsubo H, Ogasawara Y, Sekita T, Saeki A, Sakamoto M, Nishiwaki K, Masuoka H, Shimada T, Yoshida M, Hosoya T (1997) Prognostic factors of hemophagocytic syndrome in adults: analysis of 34 cases. Eur J Haematol 59:247-253
86. Imashuku S (2000) Advances in the management of hemophagocytic lymphohistiocytosis. Int J Hematol 72:1-11
87. Imashuku S, Hibi S, Tabata Y, Todo S (1999) Hemophagocytic syndrome in five patients with Epstein-Barr virus negative B-cell lymphoma. Cancer 85:2298-2300
88. Imashuku S, Kuriyama K, Sakai R, Nakao Y, Masuda S, Yasuda N, Kawano F, Yakushijin K, Miyagawa A, Nakao T, Teramura T, Tabata Y, Morimoto A, Hibi S (2003) Treatment of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis (EBV-HLH) in young adults: a report from the HLH study center. Med Pediatr Oncol 41:103-109
89. Hardikar W, Pang K, Al-Hebbi H, Curtis N, Couper R (2006) Successful treatment of cytomegalovirus-associated haemophagocytic syndrome following paediatric orthotopic liver transplantation. J Paediatr Child Health 42:389-391
90. Ramasamy K, Lim ZY, Savvas M, Salisbury JR, Dokal I, Mufti GJ, Pagliuca A (2006) Disseminated herpes virus (HSV-2) infection with rhabdomyolysis and hemophagocytic lymphohistiocytosis in a patient with bone marrow failure syndrome. Ann Hematol 85:629-630
91. Imashuku S, Hibi S, Ohara T, Iwai A, Sako M, Kato M, Arakawa H, Sotomatsu M, Kataoka S, Asami K, Hasegawa D, Kosaka Y, Sano K, Igarashi N, Maruhashi K, Ichimi R, Kawasaki H, Maeda N, Tanizawa A, Arai K, Abe T, Hisakawa H, Miyashita H, Henter JI (1999) Effective control of Epstein-Barr virus-related hemophagocytic lymphohistiocytosis with immunochemotherapy. Histiocyte Society. Blood 93:1869-1874
92. Papo T, Andre MH, Amoura Z, Lortholary O, Tribout B, Guillevin L, Piette JC (1999) The spectrum of reactive hemophagocytic syndrome in systemic lupus erythematosus. J Rheumatol 26:927-930
93. Ravelli A, Viola S, Benedetti F de, Magni-Manzoni S, Tzialla C, Martini A (2001) Dramatic efficacy of cyclosporine A in macrophage activation syndrome. Clin Exp Rheumatol 19:108
94. Ravelli A (2002) Macrophage activation syndrome. Curr Opin Rheumatol 14:548-552
95. Henzan T, Nagafuji K, Tsukamoto H, Miyamoto T, Gondo H, Imashuku S, Harada M (2006) Success with infliximab in treating refractory hemophagocytic lymphohistiocytosis. Am J Hematol 81:59-61