Cryptococcosis diagnosis and treatment: What do we know now

Fungal Genetics and Biology

Volumn 78, Issue , 2015, Pages 49-54

  Perfect, John R ^a   Bicanic, Tihana ^b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Management; Medical mycology; Meningitis; Pathophysiology

Indexed keywords

AMPHOTERICIN B; AMPHOTERICIN B DEOXYCHOLATE; AMPHOTERICIN B LIPID COMPLEX; DEXAMETHASONE; FLUCONAZOLE; FLUCYTOSINE; ANTIFUNGAL AGENT;

ANTIGEN DETECTION; ARTICLE; CEREBROSPINAL FLUID CULTURE; CONTROLLED CLINICAL TRIAL (TOPIC); CRYPTOCOCCAL MENINGITIS; CRYPTOCOCCOSIS; CRYPTOCOCCUS GATTII; CRYPTOCOCCUS NEOFORMANS; DRUG EFFICACY; DRUG SAFETY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDEMIC; FUNGAL GENOME; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS IDENTIFICATION; GENE LOCUS; GENOME ANALYSIS; GENOTYPE; GEOGRAPHIC DISTRIBUTION; GLASGOW COMA SCALE; HISTOPATHOLOGY; HUMAN; INCIDENCE; INTRACRANIAL PRESSURE; MOLECULAR PATHOLOGY; NONHUMAN; OUTCOME ASSESSMENT; PATHOGEN CLEARANCE; POINT OF CARE TESTING; PREVALENCE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); STRAIN IDENTIFICATION; TREATMENT DURATION; CLASSIFICATION; DIAGNOSTIC TEST; FILOBASIDIELLA; IMMUNOAFFINITY CHROMATOGRAPHY; ISOLATION AND PURIFICATION; MENINGITIS, CRYPTOCOCCAL; MICROBIOLOGICAL EXAMINATION; POINT OF CARE SYSTEM; PROCEDURES;

ANTIFUNGAL AGENTS; CRYPTOCOCCUS; DIAGNOSTIC TESTS, ROUTINE; HUMANS; IMMUNOCHROMATOGRAPHY; MENINGITIS, CRYPTOCOCCAL; MICROBIOLOGICAL TECHNIQUES; POINT-OF-CARE SYSTEMS;

EID: 84931384740     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2014.10.003     Document Type: Article

References (64)

1. Anonymous Rapid Advice. Diagnosis, Prevention and Management of Cryptococcal Disease in HIV-infected Adults, Adolescents and Children 2011, WHO Press, Geneva, Switzerland.
2. Bennett J.E., Dismukes W.E., Duma R.J., et al. A comparison of amphotericin B alone and combined with flucytosine in the treatment of cryptococcal meningitis. N. Engl. J. Med. 1979, 301:123-131.
3. Bicanic T., Meintjes G., Wood R., Hayes M., Rebe K., Bekker L.G., Harrison T. Fungal burden, early fungicidal activity, and outcome in cryptococcal meningitis in antiretroviral-naive or antiretroviral-experienced patients treated with amphotericin B or fluconazole. Clin. Infect. Dis. 2007, 45:76-80.
4. Bicanic T., Brouwer A.E., Meintjes G., Rebe K., Limmathrotsakul D., Chierakul W., Teparrukkul P., Loyse A. Relationship of cerebrospinal fluid pressure, fungal burden and outcome in patients with cryptococcal meningitis undergoing serial lumbar punctures. AIDS 2009, 23:701-706.
5. Billmyre R.B., Croll D., Li W., Mieczkowski P., Carter D.A., Cuomo C.A., Kronstad J.W., Heitman J. Highly recombinant VGII Cryptococcus gattii population develops clonal outbreak clusters through both sexual macroevolution and asexual microevolution. mBio 2014, 5:e01494.
6. Boulware D.R., Bonham S.C., Meya D.B., Wiesner D.L., Park G.S., Kambugu A., Janoff E.N., Bohjanen P.R. Paucity of initial cerebrospinal fluid inflammation in cryptococcal meningitis is associated with subsequent immune reconstitution inflammatory syndrome. J. Infect. Dis. 2010, 202:962-970.
7. Boulware D.R., Meya D.B., Muzoora C., Rolfes M.A., Huppler Hullsiek K., Musubire A., Taseera K., Nabeta H.W., Schutz C., Williams D.A., Rajasingham R., Rhein J., Thienemann F., Lo M.W., Nielsen K., Bergemann T.L., Kambugu A., Manabe Y.C., Janoff E.N., Bohjanen P.R., Meintjes G., Team C.T. Timing of antiretroviral therapy after diagnosis of cryptococcal meningitis. N. Engl. J. Med. 2014, 370:2487-2498.
8. Bratton E.W., El Husseini N., Chastain C.A., Lee M.S., Poole C., Sturmer T., Juliano J.J., Weber D.J., Perfect J.R. Comparison and temporal trends of three groups with cryptococcosis: HIV-infected, solid organ transplant, and HIV-negative/non-transplant. PLoS One 2012, 7:e43582.
9. Bratton E.W., El Husseini N., Chastain C.A., Lee M.S., Poole C., Stürmer T., Weber D.J., Juliano J.J., Perfect J.R. Approaches to antifungal therapies and their effectiveness among patients with cryptococcosis. Antimicrob. Agents Chemother. 2013, 57:2485-2495.
10. Brizendine K.D., Baddley J.W., Pappas P.G. Predictors of mortality and differences in clinical features among patients with cryptococcosis according to immune status. PLoS One 2013, 8:e60431.
11. Brouwer A.E., Rajanuwong A., Chierakul W., Griffin G.E., Larsen R.A., White N.J., Harrison T.S. Combination antifungal therapies for HIV-associated cryptococcal meningitis: feasibility and power of quantitative CSF cultures to determine fungicidal activity. Lancet 2004, 363:1764-1767.
12. Chen S.C., Korman T.M., Slavin M.A., Marriott D., Byth K., Bak N., Currie B.J., Hajkowicz K., Heath C.H., Kidd S., McBride W.J., Meyer W., Murray R., Playford E.G., Sorrell T.C., Australia, New Zealand Mycoses Interest Group Cryptococcus Antifungal therapy and management of complications of cryptococcosis due to Cryptococcus gattii. Clin. Infect. Dis. 2013, 57:543-551.
13. Chen Y., Toffaletti D.L., Tenor J.L., Litvintseva A.P., Fang C., Mitchell T.G., McDonald T.R., Nielsen K., Boulware D.R., Bicanic T., Perfect J.R. The Cryptococcus neoformans transcriptome at the site of human meningitis. mBio 2014, 5. e01087-13.
14. Day J.N., Chau T.T., Wolbers M. Combination antifungal therapy for cryptococcal meningitis. N. Engl. J. Med. 2013, 368:1291-1302.
15. Engelthaler D.M., Hicks N.D., Gillece J.D., Roe C.C., Schupp J.M., Driebe E.M., Gilgado F., Carriconde F., Trilles L., Firacative C., Ngamskulrungroj P., Castañeda E., dos Santos Lazera M., Melhem M.S.C., Pérez-Bercoff Å., Huttley G., Sorrell T.C., Voelz K., May R.C., Fisher M.C., Thompson G.R., Lockhart S.R., Keim P., Meyer W. Cryptococcus gattii in North American Pacific Northwest: whole-population genome analysis provides insights into species evolution and dispersal. mBio 2014, 5:e01464.
16. Graybill J.R., Sobel J., Saag M., van der Horst C., Powderly W., Cloud G., Riser L., Hamil R.J., Dismukes W. Diagnosis and management of increased intracranial pressure in patients with AIDS and cryptococcal meningitis. Clin. Infect. Dis. 2000, 30:47-54.
17. Gupta A.O., Singh N. Immune reconstitution syndrome and fungal infections. Curr. Opin. Infect. Dis. 2011, 24:527-533.
18. Hagen F., Ceresini P.C., Polacheck I., Ma H., van Nieuwerburgh F., Gabaldón T., Kagan S., Pursall E.R., Hoogveld H.L., van Iersel L.J.J., Klau G.W., Kelk S.M., Stougie L., Bartlett K.H., Voelz K., Pryszcz L.P., Castañeda E., Lazera M., Meyer W., Deforce D., Meis J.F., May R.C., Klaassen C.H.W., Boekhout T. Ancient dispersal of the human fungal pathogen Cryptococcus gattii from the Amazon rainforest. PLoS One 2013, 8:e71148.
19. Hamill R.J., Sobel J.D., El-Sadr W., Johnson P.C., Graybill J.R., Javaly K., Barker D.E. Comparison of 2 doses of liposomal amphotericin B and conventional amphotericin B deoxycholate for treatment of AIDS-associated acute cryptococcal meningitis: a randomized, double-blind clinical trial of efficacy and safety. Clin. Infect. Dis. 2010, 51:225-232.
20. Hansen J., Slechta E.S., Gates-Hollingsworth M.A., Neary B., Barker A.P., Bauman S., Kozel T.R., Hanson K.E. Large-scale evaluation of the immuno-mycologics lateral flow and enzyme-linked immunoassays for detection of cryptococcal antigen in serum and cerebrospinal fluid. Clin. Vaccine Immunol. 2013, 20:52-55.
21. Harris J.R., Lockhart S.R., Sondermeyer G., Vugia D.J., Crist M.B., D'Angelo M.T., Sellers B., Franco-Paredes C., Makvandi M., Smelser C., Greene J., Stanek D., Signs K., Nett R.J., Chiller T., Park B.J. Cryptococcus gattii infections in multiple states outside the US Pacific Northwest. Emerg. Infect. Dis. 2013, 19:1620-1626.
22. Heitman J., Kozel T.R., Kwon-Chung K.J., Perfect J.R., Casadevall A. Cryptococcus: From Human Pathogen to Model Yeast 2011, ASM Press, Washington, DC, USA.
23. Hu G., Wang J., Choi J., Jung W.H., Liu I., Litvintseva A.P., Bicanic T., Aurora R., Mitchell T.G., Perfect J.R., Kronstad J.W. Variation in chromosome copy number influences the virulence of Cryptococcus neoformans and occurs in isolates from AIDS patients. BMC Genom. 2011, 12:526.
24. Jackson A.T., Nussbaum J.C., Phulusa J., Namarika D., Chikasema M., Kanyemba C., Jarvis J.N., Jaffar S., Hosseinipour M.C., van der Horst C., Harrison T.S. A phase II randomized controlled trial adding oral flucytosine to high-dose fluconazole, with short-course amphotericin B, for cryptococcal meningitis. AIDS 2012, 26:1363-1370.
25. Janbon G., Ormerod K.L., Paulet D., Byrnes E.J., Yadav V., Chatterjee G., Mullapudi N., Hon C.-C., Billmyre R.B., Brunel F., Bahn Y.-S., Chen W., Chen Y., Chow E.W.L., Coppée J.-Y., Floyd-Averette A., Gaillardin C., Gerik K.J., Goldberg J., Gonzalez-Hilarion S., Gujja S., Hamlin J.L., Hsueh Y.-P., Ianiri G., Jones S., Kodira C.D., Kozubowski L., Lam W., Marra M., Mesner L.D., Mieczkowski P.A., Moyrand F., Nielsen K., Proux C., Rossignol T., Schein J.E., Sun S., Wollschlaeger C., Wood I.A., Zeng Q., Neuvéglise C., Newlon C.S., Perfect J.R., Lodge J.K., Idnurm A., Stajich J.E., Kronstad J.W., Sanyal K., Heitman J., Fraser J.A., Cuomo C.A., Dietrich F.S. Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet. 2014, 10:e1004261.
26. Jarvis J.N., Lawn S.D., Vogt M., Bangani N., Wood R., Harrison T.S. Screening for cryptococcal antigenemia in patients accessing an antiretroviral treatment program in South Africa. Clin. Infect. Dis. 2009, 48:856-862.
27. Jarvis J.N., Meintjes G., Rebe K., Williams G.N., Bicanic T., Williams A., Schutz C., Bekker L.G., Wood R., Harrison T.S. Adjunctive interferon-γ immunotherapy for the treatment of HIV-associated cryptococcal meningitis: a randomized controlled trial. AIDS 2012, 26:1105-1113.
28. Jarvis J.N., Casazza J.P., Stone H.H., Meintjes G., Lawn S.D., Levitz S.M., Harrison T.S., Koup R.A. The phenotype of the Cryptococcus-specific CD4+ memory T-cell response is associated with disease severity and outcome in HIV-associated cryptococcal meningitis. J. Infect. Dis. 2013, 207:1817-1828.
29. Jarvis J.N., Bicanic T., Loyse A., Namarika D., Jackson A., Nussbaum J.C., Longley N., Muzoora C., Phulusa J., Taseera K., Kanyembe C., Wilson D., Hosseinipour M.C., Brouwer A.E., Limmathurotsakul D., White N., van der Horst C., Wood R., Meintjes G., Bradley J., Jaffar S., Harrison T. Determinants of mortality in a combined cohort of 501 patients with HIV-associated Cryptococcal meningitis: implications for improving outcomes. Clin. Infect. Dis. 2014, 58:736-745.
30. Larsen R.A., Leal M.A.E., Chan L.S. Fluconazole compared with amphotericin B plus flucytosine for cryptococcal meningitis in AIDS. Ann. Intern. Med. 1990, 113:183-187.
31. Lee A., Toffaletti D.L., Tenor J., Soderblom E.J., Thompson J.W., Moseley M.A., Price M., Perfect J.R. Survival defects of Cryptococcus neoformans mutants exposed to human cerebrospinal fluid result in attenuated virulence in an experimental model of meningitis. Infect. Immun. 2012, 78:4213-4225.
32. Lightowler J.V., Cooke G.S., Mutevedzi P., Lessells R.J., Newell M.L., Dedicoat M. Treatment of cryptococcal meningitis in KwaZulu-Natal, South Africa. PLoS One 2010, 5:e8630.
33. Livermore J., Howard S.J., Sharp A.D., Goodwin J., Gregson L., Felton T., Schwartz J.A., Walker C., Moser B., Muller W., Harrison T.S., Perfect J.R., Hope W.W. Efficacy of an abbreviated induction regimen of amphotericin B deoxycholate for cryptococcal meningoencephalitis: 3days of therapy is equivalent to 14days. mBio 2013, 5. e00725-13.
34. Longley N., Muzoora C., Taseera K., Mwesigye J., Rwebembera J., Chakera A., Wall E., Andia I., Jaffar S., Harrison T.S. Dose-response effect of high-dose fluconazole for HIV-associated cryptococcal meningitis in southwestern Uganda. Clin. Infect. Dis. 2008, 47:1556-1561.
35. Longley N., Harrison T.S., Jarvis J.N. Cryptococcal immune reconstitution inflammatory syndrome. Curr. Opin. Infect. Dis. 2013, 26:26-34.
36. Loyse A., Thangaraj H., Easterbrook P., Ford N., Roy M., Chiller T., Govender N., Harrison T.S., Bicanic T. Cryptococcal meningitis: improving access to essential antifungal medicines in resource-poor countries. Lancet Infect. Dis. 2013, 13:629-637.
37. Mayanja-Kizza H., Oishi K., Mitarai S., Yamashita H., Nalongo K., Watanabe K., Izumi T., Jungala O., Augustine K., Mugerwa R., Nagatake T., Matsumoto K. Combination therapy with fluconazole and flucytosine for cryptococcal meningitis in Ugandan patients with AIDS. Clin. Infect. Dis. 1998, 26:1362-1366.
38. McKenney J., Smith R.M., Chiller T.M., Detels R., French A., Margolick J., Klausner J.D. Prevalence and correlates of cryptococcal antigen positivity among AIDS patients - United States, 1986-2012. Morb. Mortal. Wkly Rep. 2014, 63:585-587.
39. Meya D.B., Manabe Y.C., Castelnuovo B., Cook B.A., Elbireer A.M., Kambugu A., Kamya M.R., Bohjanen P.R., Boulware D.R. Cost-effectiveness of serum cryptococcal antigen screening to prevent deaths among HIV-infected persons with a CD4+ cell count ≤100cells/μL who start HIV therapy in resource-limited settings. Clin. Infect. Dis. 2010, 51:448-455.
40. Muzoora C.K., Kabanda T., Ortu G., Ssentamu J., Hearn P., Mwesigye J., Longley N., Jarvis J.N., Jaffar S., Harrison T.S. Short course amphotericin B with high dose fluconazole for HIV-associated cryptococcal meningitis. J. Infect. 2012, 64:76-81.
41. Ngamskulrungroj P., Himmelreich U., Breger J.A., Wilson C., Chayakulkeeree M., Krockenberger M.B., Malik R., Daniel H.M., Toffaletti D., Djordjevic J.T., Mylonakis E., Meyer W., Perfect J.R. The trehalose synthesis pathway is an integral part of the virulence composite for Cryptococcus gattii. Infect. Immun. 2009, 77:4584-4596.
42. Ngamskulrungroj P., Chang Y., Sionov E., Kwon-Chung K.J. The primary target organ of Cryptococcus gattii is different from that of Cryptococcus neoformans in a murine model. mBio 2012, 3. e00103-12.
43. Nussbaum J.C., Jackson A., Namarika D., Phulusa J., Kenala J., Kanyemba C., Jarvis J.N., Jaffar S., Hostetler J., Hosseinipour M.C., Kamwendo D., van der Horst C.M., Harrison T.S. Combination flucytosine and high-dose fluconazole compared with fluconazole monotherapy for the treatment of cryptococcal meningitis: a randomized trial in Malawi. Clin. Infect. Dis. 2010, 50:338-344.
44. Park B.J., Wannemuehler K.A., Marston B.J., Govender N., Pappas P.G., Chiller T.M. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 2009, 23:525-530.
45. Perfect J.R. Fungal diagnosis: how do we do it and can we do better?. Curr. Med. Res. Opin. 2013, 29(Suppl. 4):3-11.
46. Perfect J.R., Dismukes W.E., Pappas P.G., Singh N., Harrison T.E., Lortholary O., Dromer F., Sobel J.D., Sorrell T.C., Goldman D.L., Nuygen M.H., Hammil R.D., Larsen R.A., Powderly W.G., Graybill J.R. Clinical practice guidelines for the management of cryptococcal disease: 2010 Update by the Infectious Diseases Society of America. Clin. Infect. Dis. 2010, 50:291-322.
47. Posteraro B., Vella A., Cogliati M., De Carolis E., Florio A.R., Posteraro P., Sanguinetti M., Tortorano A.M. Matrix-assisted laser desorption ionization-time of flight mass spectrometry-based method for discrimination between molecular types of Cryptococcus neoformans and Cryptococcus gattii. J. Clin. Microbiol. 2012, 50:2472-2476.
48. Pyrgos V., Seitz A.E., Steiner C.A., Prevots D.R., Williamson P.R. Epidemiology of cryptococcal meningitis in the US: 1997-2009. PLoS One 2013, 8:e56269.
49. Robertson E.J., Najjuka G., Rolfes M.A., Akampurira A., Jain N., Anantharanjit J., von Hohenberg M., Tassieri M., Carlsson A., Meya D.B., Harrison T.S., Fries B.C., Boulware D.R., Bicanic T. Cryptococcus neoformans ex vivo capsule size is associated with intracranial pressure and host immune response in HIV-associated cryptococcal meningitis. J. Infect. Dis. 2014, 209:74-82.
50. Rohatgi S., Gohil S., Kuniholm M.H., Schultz H., Dufaud C., Armour K.L., Badri S., Mailliard R.B., Pirofski L.-a. Fc gamma receptor 3A polymorphism and risk for HIV-associated cryptococcal disease. mBio 2013, 4. e00573-13.
51. Rolfes M.A., Hullsiek K.H., Rhein J., Nabeta H.W., Taseera K., Schutz C., Musubire A., Rajasingham R., Williams D.A., Thienemann F., Muzoora C., Meintjes G., Meya D.B., Boulware D.R. The effect of therapeutic lumbar punctures on acute mortality from cryptococcal meningitis. Clin. Infect. Dis. 2014, 59. (in press).
52. Rosen L.B., Freeman A.F., Yang L.M., Jutivorakool K., Olivier K.N., Angkasekwinai N., Suputtamongkol Y., Bennett J.E., Pyrgos V., Williamson P.R., Ding L., Holland S.M., Browne S.K. Anti-GM-CSF autoantibodies in patients with cryptococcal meningitis. J. Immunol. 2013, 190:3959-3966.
53. Rugemalila J., Maro V.P., Kapanda G., Ndaro A.J., Jarvis J.N. Cryptococcal antigen prevalence in HIV-infected Tanzanians: a cross-sectional study and evaluation of a point-of-care lateral flow assay. Trop. Med. Int. Health 2013, 18:1075-1079.
54. Saijo T., Chen J., Chen S.C., Rosen L.B., Yi J., Sorrell T.C., Bennett J.E., Holland S.M., Browne S.K., Kwon-Chung K.J. Anti-granulocyte-macrophage colony-stimulating factor autoantibodies are a risk factor for central nervous system infection by Cryptococcus gattii in otherwise immunocompetent patients. mBio 2014, 5. e00912-14.
55. Seaton R.A., Verma N., Naraqi S., Wembri J.P., Warrell D.A. The effect of corticosteroids on visual loss in Cryptococcus neoformans var. gattii meningitis. Trans. R. Soc. Trop. Med. Hyg. 1997, 91:50-52.
56. Siddiqi O.K., Ghebremichael M., Dang X., Atadzhanov M., Kaonga P., Khoury M.N., Koralnik I.J. Molecular diagnosis of central nervous system opportunistic infections in HIV-infected Zambian adults. Clin. Infect. Dis. 2014, 58:1771-1777.
57. Siddiqui A.A., Brouwer A.E., Wuthiekanun V., Jaffar S., Shattock R., Irving D., Sheldon J., Chierakul W., Peacock S., Day N., White N.J., Harrison T.S. IFN-gamma at the site of infection determines rate of clearance of infection in cryptococcal meningitis. J. Immunol. 2005, 174:1746-1750.
58. Sionov E., Lee H., Chang Y.C., Kwon-Chung K.J. Cryptococcus neoformans overcomes stress of azole drugs by formation of disomy in specific multiple chromosomes. PLoS Pathog. 2010, 6:e1000848.
59. Sionov E., Chang Y.C., Kwon-Chung K.J. Azole heteroresistance in Cryptococcus neoformans: emergence of resistant clones with chromosomal disomy in the mouse brain during fluconazole treatment. Antimicrob. Agent Chemother. 2013, 57:5127-5130.
60. Smith R.M., Mba-Jonas A., Tourdjman M., Schimek T., DeBess E., Marsden-Haug N., Harris J.R. Treatment and outcomes among patients with Cryptococcus gattii infections in the United States Pacific Northwest. PLoS One 2014, 9:e88875.
61. van der Horst C.M., Saag M.S., Cloud G.A., Hamill R.J., Graybill J.R., Sobel J.D., Johnson P.C., Tuazon C.U., Kerkering T., Moskovitz B.L., Powderly W.G., Dismukes W.E. Treatment of cryptococcal meningitis associated with the acquired immunodeficiency syndrome. National Institute of Allergy and Infectious Diseases Mycoses Study Group and AIDS Clinical Trials Group. N. Engl. J. Med. 1997, 337:15-21.
62. Van Wyk M., Govender N.P., Mitchell T.G., Litvintseva A.P. Multilocus sequence typing of serially collected isolates of Cryptococcus from HIV-infected patients in South Africa. J. Clin. Microbiol. 2014, 52:1921-1931. GERMS-SA.
63. Wiesner D.L., Moskalenko O., Corcoran J.M., McDonald T., Rolfes M.A., Meya D.B., Kajumbula H.A.K., Bohjanen P.R., Knight J.F., Boulware D.R.K.N. Cryptococcal genotype influences immunologic response and human clinical outcome after meningitis. mBio 2012, 3. e00196-12.
64. Zhu L.P., Wu J.Q., Xu B., Ou X.T., Zhang Q.Q., Weng X.H. Cryptococcal meningitis in non-HIV-infected patients in a Chinese tertiary care hospital, 1997-2007. Med. Mycol. 2010, 48:570-579.