Importance of Candida-bacterial polymicrobial biofilms in disease.

Candida albicans is the most prevalent human fungal pathogen, with an ability to inhabit diverse host niches and cause disease in both immunocompetent and immunocompromised individuals. C. albicans also readily forms biofilms on indwelling medical devices and mucosal tissues, which serve as an infectious reservoir that is difficult to eradicate, and can lead to lethal systemic infections. Biofilm formation occurs within a complex milieu of host factors and other members of the human microbiota. Polymicrobial interactions will probably dictate the cellular and biochemical composition of the biofilm, as well as influence clinically relevant outcomes, such as drug and host resistance and virulence. In this manuscript, we review C. albicans infections in the context of in vivo polymicrobial biofilms and implications for pathogenesis.

[1]  D. Hogan,et al.  Fungal--bacterial interactions: a mixed bag of mingling microbes. , 2006, Current opinion in microbiology.

[2]  S. Gaffen,et al.  Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis , 2009, The Journal of experimental medicine.

[3]  E. Carlson Enhancement by Candida albicans of Staphylococcus aureus, Serratia marcescens, and Streptococcus faecalis in the establishment of infection in mice , 1983, Infection and immunity.

[4]  R. Darouiche,et al.  Candida Infections of Medical Devices , 2004, Clinical Microbiology Reviews.

[5]  R. Kolter,et al.  Pseudomonas-Candida Interactions: An Ecological Role for Virulence Factors , 2002, Science.

[6]  N. R. de Melo,et al.  Efficacy and safety of a contraceptive vaginal ring (NuvaRing) compared with a combined oral contraceptive: a 1-year randomized trial. , 2005, Contraception.

[7]  Gerald R. Fink,et al.  Dynamic, Morphotype-Specific Candida albicans β-Glucan Exposure during Infection and Drug Treatment , 2008, PLoS pathogens.

[8]  O. Unal,et al.  Diagnosis of vulvovaginitis: comparison of clinical and microbiological diagnosis , 2010, Archives of Gynecology and Obstetrics.

[9]  H. Lochs,et al.  An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole. , 2008, American journal of obstetrics and gynecology.

[10]  M. Harriott,et al.  Ability of Candida albicans Mutants To Induce Staphylococcus aureus Vancomycin Resistance during Polymicrobial Biofilm Formation , 2010, Antimicrobial Agents and Chemotherapy.

[11]  J. Sobel Pathogenesis and treatment of recurrent vulvovaginal candidiasis. , 1992, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[12]  D. Heyland,et al.  The relationship between Candida species cultured from the respiratory tract and systemic inflammation in critically ill patients with ventilator-associated pneumonia , 2011, Canadian journal of anaesthesia = Journal canadien d'anesthesie.

[13]  D. Dunn,et al.  Candida albicans and Escherichia coli are synergistic pathogens during experimental microbial peritonitis. , 1997, The Journal of surgical research.

[14]  D. Hogan,et al.  Mixed bacterial-fungal infections in the CF respiratory tract. , 2010, Medical mycology.

[15]  D. Grimes,et al.  Intrauterine devices and pelvic inflammatory disease: recent developments. , 1987, Contraception.

[16]  N. Gow,et al.  Cell wall glycans and soluble factors determine the interactions between the hyphae of Candida albicans and Pseudomonas aeruginosa , 2008, FEMS microbiology letters.

[17]  Gordon Ramage,et al.  The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. , 2002, FEMS microbiology letters.

[18]  B. Wickes,et al.  Characteristics of biofilm formation by Candida albicans. , 2001, Revista iberoamericana de micologia.

[19]  C. Allen,et al.  Differences in mucosal reaction related to Candida albicans isolates. , 1987, Journal of oral pathology.

[20]  D. Soll,et al.  Frequency, intensity, species, and strains of oral Candida vary as a function of host age , 1996, Journal of clinical microbiology.

[21]  E. Urbán,et al.  Biofilm formation on intrauterine devices in relation to duration of use. , 2005, Journal of medical microbiology.

[22]  Gordon Ramage,et al.  Candida biofilms on implanted biomaterials: a clinically significant problem. , 2006, FEMS yeast research.

[23]  Claire Collins,et al.  Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. , 2006, The Journal of clinical investigation.

[24]  P. Stewart,et al.  Biofilms in chronic wounds , 2008, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[25]  A. Mitchell,et al.  How to build a biofilm: a fungal perspective. , 2006, Current opinion in microbiology.

[26]  L. C. Dutton,et al.  Streptococcus gordonii Modulates Candida albicans Biofilm Formation through Intergeneric Communication , 2009, Infection and Immunity.

[27]  A. McKenzie,et al.  Development of Allergic Airway Disease in Mice following Antibiotic Therapy and Fungal Microbiota Increase: Role of Host Genetics, Antigen, and Interleukin-13 , 2005, Infection and Immunity.

[28]  Saul Tzipori,et al.  Self-Regulation of Candida albicans Population Size during GI Colonization , 2007, PLoS pathogens.

[29]  Trees Jansen,et al.  Human dectin-1 deficiency and mucocutaneous fungal infections. , 2009, The New England journal of medicine.

[30]  A. Kucharska,et al.  The in vitro activity of vaginal Lactobacillus with probiotic properties against Candida. , 2005, Infectious diseases in obstetrics and gynecology.

[31]  K. Stoltze,et al.  Oral candidiasis and immune status of HIV-infected patients. , 1994, Journal of oral pathology & medicine : official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology.

[32]  A. Mitchell,et al.  Critical Role of Bcr1-Dependent Adhesins in C. albicans Biofilm Formation In Vitro and In Vivo , 2006, PLoS pathogens.

[33]  G. Huffnagle,et al.  Regulation of Candida albicans Morphogenesis by Fatty Acid Metabolites , 2004, Infection and Immunity.

[34]  J. Sobel Pathogenesis and Epidemiology of Vulvovaginal Candidiasis , 1988, Annals of the New York Academy of Sciences.

[35]  A. Nobbs,et al.  Heterologous Expression of Candida albicans Cell Wall-Associated Adhesins in Saccharomyces cerevisiae Reveals Differential Specificities in Adherence and Biofilm Formation and in Binding Oral Streptococcus gordonii , 2010, Eukaryotic Cell.

[36]  J. Timsit,et al.  Candida colonization of the respiratory tract and subsequent pseudomonas ventilator-associated pneumonia. , 2006, Chest.

[37]  M. Shirtliff,et al.  Effect of farnesol on Candida dubliniensis biofilm formation and fluconazole resistance. , 2006, FEMS yeast research.

[38]  J. Lopez-Ribot,et al.  The Transcriptional Regulator Nrg1p Controls Candida albicans Biofilm Formation and Dispersion , 2010, Eukaryotic Cell.

[39]  A. Nobbs,et al.  Interaction of Candida albicans Cell Wall Als3 Protein with Streptococcus gordonii SspB Adhesin Promotes Development of Mixed-Species Communities , 2010, Infection and Immunity.

[40]  E. Carlson,et al.  Synergistic effect of Candida albicans and Staphylococcus aureus on mouse mortality , 1982, Infection and immunity.

[41]  C. Barr,et al.  Oral mucosal lesions and HIV viral load in the Women's Interagency HIV Study (WIHS). , 2000, Journal of acquired immune deficiency syndromes.

[42]  B. Wickes,et al.  Inhibition of Candida albicans Biofilm Formation by Farnesol, a Quorum-Sensing Molecule , 2002, Applied and Environmental Microbiology.

[43]  E. Carlson,et al.  Protection by Candida albicans of Staphylococcus aureus in the establishment of dual infection in mice , 1985, Infection and immunity.

[44]  C. Kauffman,et al.  Epidemiology of oral candidiasis in HIV-infected patients: colonization, infection, treatment, and emergence of fluconazole resistance. , 1994, The American journal of medicine.

[45]  P. Lipke,et al.  Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature. , 2007, Diagnostic microbiology and infectious disease.

[46]  Jeffrey N. Weiser,et al.  Colonization of mucosal surfaces. , 2005 .

[47]  A. Telenti,et al.  Polymicrobial fungemia: microbiology, clinical features, and significance. , 1989, Reviews of infectious diseases.

[48]  E. Carlson,et al.  Synergism of Candida albicans and delta toxin producing Staphylococcus aureus on mouse mortality and morbidity: protection by indomethacin. , 1988, Zentralblatt fur Bakteriologie, Mikrobiologie, und Hygiene. Series A, Medical microbiology, infectious diseases, virology, parasitology.

[49]  S. Dowd,et al.  Identification of yeast in chronic wounds using new pathogen-detection technologies. , 2009, Journal of wound care.

[50]  G. Taylor,et al.  Pseudomonas aeruginosa pyocyanin and 1-hydroxyphenazine inhibit fungal growth. , 1999, Journal of clinical pathology.

[51]  A. Mitchell,et al.  Function of Candida albicans Adhesin Hwp1 in Biofilm Formation , 2006, Eukaryotic Cell.

[52]  B. Peters,et al.  Cross-kingdom interactions: Candida albicans and bacteria. , 2009, FEMS microbiology letters.

[53]  H Lee,et al.  Fabrication of a multi-applicable removable intraoral denture system for rodent research. , 2011, Journal of oral rehabilitation.

[54]  D. Fry,et al.  Candida sepsis. Implications of polymicrobial blood-borne infection. , 1985, Archives of surgery.

[55]  M. Harriott,et al.  Candida albicans forms biofilms on the vaginal mucosa , 2010, Microbiology.

[56]  E. Carlson,et al.  Effect of strain of Staphylococcus aureus on synergism with Candida albicans resulting in mouse mortality and morbidity , 1983, Infection and immunity.

[57]  A. Mitchell,et al.  Complementary Adhesin Function in C. albicans Biofilm Formation , 2008, Current Biology.

[58]  E. Anaissie,et al.  Fungal Infections in Patients with Cancer , 1990, Pharmacotherapy.

[59]  Martin Schmidt,et al.  Antifungal mechanisms supporting boric acid therapy of Candida vaginitis. , 2008, The Journal of antimicrobial chemotherapy.

[60]  C. Seneviratne,et al.  Community lifestyle of Candida in mixed biofilms: a mini review , 2009, Mycoses.

[61]  Intrauterine devices and pelvic inflammatory disease: an international perspective , 1992, The Lancet.

[62]  G. Baillie,et al.  Mixed species biofilms of Candida albicans and Staphylococcus epidermidis. , 2002, Journal of medical microbiology.

[63]  L. J. Douglas,et al.  Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. , 2006, Journal of medical microbiology.

[64]  G. Baillie,et al.  Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. , 2000, The Journal of antimicrobial chemotherapy.

[65]  D. Andes,et al.  Development and Validation of an In Vivo Candida albicans Biofilm Denture Model , 2010, Infection and Immunity.

[66]  S. Dowd,et al.  Survey of fungi and yeast in polymicrobial infections in chronic wounds. , 2011, Journal of wound care.

[67]  H. Kent,et al.  Epidemiology of vaginitis. , 1991, American journal of obstetrics and gynecology.

[68]  E. Denamur,et al.  Candida albicans impairs macrophage function and facilitates Pseudomonas aeruginosa pneumonia in rat* , 2009, Critical care medicine.

[69]  L. Bahamondes,et al.  Follow-up of users of intrauterine device with and without bacterial vaginosis and other cervicovaginal infections. , 2003, Contraception.

[70]  Duccio Cavalieri,et al.  The dectin-1/inflammasome pathway is responsible for the induction of protective T-helper 17 responses that discriminate between yeasts and hyphae of Candida albicans , 2011, Journal of leukocyte biology.

[71]  G. Toews,et al.  Role of Antibiotics and Fungal Microbiota in Driving Pulmonary Allergic Responses , 2004, Infection and Immunity.

[72]  J. Sobel,et al.  Oral lesions among women living with or at risk for HIV infection. HIV Epidemiology Research Study (HERS) Group. , 1998, The American journal of medicine.

[73]  J. Crump,et al.  Intravascular Catheter-Associated Infections , 2000, European Journal of Clinical Microbiology and Infectious Diseases.

[74]  S. Boris,et al.  Role played by lactobacilli in controlling the population of vaginal pathogens. , 2000, Microbes and infection.

[75]  A. Gikas,et al.  Prospective study of the impact of broad-spectrum antibiotics on the yeast flora of the human gut , 1994, European Journal of Clinical Microbiology and Infectious Diseases.

[76]  B. Peters,et al.  Microbial interactions and differential protein expression in Staphylococcus aureus –Candida albicans dual-species biofilms , 2010, FEMS immunology and medical microbiology.

[77]  Mahmoud A. Ghannoum,et al.  Biofilm Formation by the Fungal PathogenCandida albicans: Development, Architecture, and Drug Resistance , 2001, Journal of bacteriology.

[78]  D. M. Walker,et al.  Denture stomatitis: a review. , 1987, Journal of oral rehabilitation.

[79]  D. Andes,et al.  Beta -1,3 glucan as a test for central venous catheter biofilm infection. , 2007, The Journal of infectious diseases.

[80]  M. Gigante,et al.  Sexually transmitted diseases and reproductive tract infections among contraceptive users , 1998, International journal of gynaecology and obstetrics: the official organ of the International Federation of Gynaecology and Obstetrics.

[81]  C. Smyth,et al.  Electron microscopy of adhesive interactions between Gardnerella vaginalis and vaginal epithelial cells, McCoy cells and human red blood cells. , 1989, Journal of general microbiology.

[82]  B. Larsen,et al.  Candida albicans morphogenesis is influenced by estrogen , 1997, Cellular and Molecular Life Sciences CMLS.

[83]  D. Wray,et al.  Denture stomatitis in the elderly. , 1990, Oral microbiology and immunology.

[84]  S. Baliga,et al.  Candida biofilms in medical devices: evolving trends. , 2007, Kathmandu University medical journal.

[85]  M. Falagas,et al.  Probiotics for prevention of recurrent vulvovaginal candidiasis: a review. , 2006, The Journal of antimicrobial chemotherapy.

[86]  P. Diaz,et al.  Characterization of Mucosal Candida albicans Biofilms , 2009, PloS one.

[87]  M. Harriott,et al.  Candida albicans and Staphylococcus aureus Form Polymicrobial Biofilms: Effects on Antimicrobial Resistance , 2009, Antimicrobial Agents and Chemotherapy.

[88]  D. Soll,et al.  Genetic dissimilarity of commensal strains of Candida spp. carried in different anatomical locations of the same healthy women , 1991, Journal of clinical microbiology.

[89]  Nicholas J. Jacobs,et al.  Antifungal mechanisms by which a novel Pseudomonas aeruginosa phenazine toxin kills Candida albicans in biofilms , 2010, Molecular microbiology.

[90]  T. Farley,et al.  Intrauterine devices and pelvic inflammatory disease: an international perspective , 1992, The Lancet.

[91]  L. J. Douglas,et al.  Penetration of Candida Biofilms by Antifungal Agents , 2004, Antimicrobial Agents and Chemotherapy.