Candida albicans the main opportunistic pathogenic fungus in humans

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(A) Arrow: formation of penetration pore in hypha of R. solani. (B) Arrows: Th2RI99 penetration tubes around the apical hypha of R. solani." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Eliana Melignani, Mara E. Martin, Vanesa Y. Mema, Catalina B. Taibo, Julia V. Sabio y García, Viviana A. Barrera" "autores" => array:6 [ 0 => array:2 [ "nombre" => "Eliana" "apellidos" => "Melignani" ] 1 => array:2 [ "nombre" => "Mara E." "apellidos" => "Martin" ] 2 => array:2 [ "nombre" => "Vanesa Y." "apellidos" => "Mema" ] 3 => array:2 [ "nombre" => "Catalina B." "apellidos" => "Taibo" ] 4 => array:2 [ "nombre" => "Julia V." "apellidos" => "Sabio y García" ] 5 => array:2 [ "nombre" => "Viviana A." "apellidos" => "Barrera" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754122001067?idApp=UINPBA00004N" "url" => "/03257541/0000005500000002/v1_202306160952/S0325754122001067/v1_202306160952/en/main.assets" ] "itemAnterior" => array:18 [ "pii" => "S0325754122001055" "issn" => "03257541" "doi" => "10.1016/j.ram.2022.11.003" "estado" => "S300" "fechaPublicacion" => "2023-04-01" "aid" => "525" "copyright" => "Asociación Argentina de Microbiología" "documento" => "article" "crossmark" => 1 "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2023;55:181-8" "abierto" => array:3 [ "ES" => false "ES2" => false "LATM" => false ] "gratuito" => false "lecturas" => array:1 [ "total" => 0 ] "en" => array:13 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "Comprehensive evaluation of abattoirs with no Hazard Analysis Critical Control Point plan in Tucumán, Argentina" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => array:3 [ 0 => "en" 1 => "en" 2 => "es" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "181" "paginaFinal" => "188" ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Evaluación integral de frigoríficos sin un plan de análisis de peligros y puntos críticos de control en Tucumán, Argentina" ] ] "contieneResumen" => array:2 [ "en" => true "es" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Gabriela Pérez Terrazzino, Magdalena Costa, Alejandro López Campo, Carolina Saade, María Paula Moreno Mochi, Marcelo Signorini, Ariel Roge, Claudia Van Der Ploeg, Gerardo Leotta, María Ángela Jure" "autores" => array:10 [ 0 => array:2 [ "nombre" => "Gabriela" "apellidos" => "Pérez Terrazzino" ] 1 => array:2 [ "nombre" => "Magdalena" "apellidos" => "Costa" ] 2 => array:2 [ "nombre" => "Alejandro" "apellidos" => "López Campo" ] 3 => array:2 [ "nombre" => "Carolina" "apellidos" => "Saade" ] 4 => array:2 [ "nombre" => "María Paula" "apellidos" => "Moreno Mochi" ] 5 => array:2 [ "nombre" => "Marcelo" "apellidos" => "Signorini" ] 6 => array:2 [ "nombre" => "Ariel" "apellidos" => "Roge" ] 7 => array:2 [ "nombre" => "Claudia" "apellidos" => "Van Der Ploeg" ] 8 => array:2 [ "nombre" => "Gerardo" "apellidos" => "Leotta" ] 9 => array:2 [ "nombre" => "María Ángela" "apellidos" => "Jure" ] ] ] ] "resumen" => array:1 [ 0 => array:3 [ "titulo" => "Highlights" "clase" => "author-highlights" "resumen" => "<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">•Study focused on two abattoirs without HACCP plan from Tucumán, Argentina.</li><li class="elsevierStyleListItem" id="lsti0010">•Risk estimation showed a marked predominance of high risk in both abattoirs.</li><li class="elsevierStyleListItem" id="lsti0015">•Differences of indicator microorganisms between abattoirs were not significant.</li><li class="elsevierStyleListItem" id="lsti0020">•Salmonella spp. and STEC were isolated from carcass and environmental samples.</li><li class="elsevierStyleListItem" id="lsti0025">•The need to work with authority in search of a standard remains unaddressed.</li></ul>" ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754122001055?idApp=UINPBA00004N" "url" => "/03257541/0000005500000002/v1_202306160952/S0325754122001055/v1_202306160952/en/main.assets" ] "en" => array:21 [ "idiomaDefecto" => true "cabecera" => "Special article" "titulo" => "Candida albicans the main opportunistic pathogenic fungus in humans" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "189" "paginaFinal" => "198" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Ignacio Uriel Macias-Paz, Salvador Pérez-Hernández, Alejandra Tavera-Tapia, Juan Pedro Luna-Arias, José Eugenio Guerra-Cárdenas, Elizabeth Reyna-Beltrán" "autores" => array:6 [ 0 => array:3 [ "nombre" => "Ignacio Uriel" "apellidos" => "Macias-Paz" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 1 => array:3 [ "nombre" => "Salvador" "apellidos" => "Pérez-Hernández" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 2 => array:3 [ "nombre" => "Alejandra" "apellidos" => "Tavera-Tapia" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 3 => array:3 [ "nombre" => "Juan Pedro" "apellidos" => "Luna-Arias" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 4 => array:3 [ "nombre" => "José Eugenio" "apellidos" => "Guerra-Cárdenas" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 5 => array:4 [ "nombre" => "Elizabeth" "apellidos" => "Reyna-Beltrán" "email" => array:1 [ 0 => "ereyna@docentes.uat.edu.mx" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Faculty of Medicine “Dr. Alberto Romo Caballero”, Autonomous University of Tamaulipas, Tampico (Tamaulipas), Mexico" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Department of Cell Biology, Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav-IPN), Mexico" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Candida albicans el principal hongo patógeno oportunista en humanos" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1181 "Ancho" => 2540 "Tamanyo" => 533911 ] ] "descripcion" => array:1 [ "en" => "Candida albicans cells analyzed by scanning electron microscopy. In (A), yeasts are in the process of budding, the arrows indicate the site of cell division between the mother cell and the daughter cell. In (B), mycelia of C. albicans, involved in tissue invasion during the infectious process." ] ] ] "textoCompleto" => "IntroductionFungal infections cause about 1.7 million deaths worldwide per year mainly in immunocompromised individuals with two or more pathological conditions<a class="elsevierStyleCrossRefs" href="#bib0520">6,42</a>. The incidence of infections caused by the genus Candida has steadily increased since the 1970s perhaps due to an increased risk of opportunistic infections, the improvement in clinical procedures that identify fungi causing nosocomial infections, as well as the development of antifungal resistance due to prolonged exposure to treatment<a class="elsevierStyleCrossRef" href="#bib0545">11</a>.There are currently more than 150 species of Candida, and approximately 20 are known to cause infections in humans. Candida albicans is the main causative agent of candidiasis and the primary fungal infection in adults and pediatric patients<a class="elsevierStyleCrossRefs" href="#bib0530">8,66,82</a>. In the USA, it was reported that sepsis caused by C. albicans has a mortality rate of approximately 40%, which is higher than any other sepsis caused by bacteria or fungi<a class="elsevierStyleCrossRef" href="#bib0935">89</a>. Infections caused by the genus Candida are the main cause of nosocomial fungal infections especially in tertiary care hospitals<a class="elsevierStyleCrossRef" href="#bib0575">17</a>.In recent decades, other non-albicans species such as C. glabrata, C. parapsilosis, C. tropicalis, C. krusei (Pichia kudriavzevii), C. dubliniensis, C. kefyr, C. famata, C. auris and others have become highly relevant at the clinical level due to their increasing prevalence as etiologic agents of candidiasis<a class="elsevierStyleCrossRefs" href="#bib0590">20,49,73,79,82</a>. In particular, C. auris is considered an emerging serious global health threat by the Centers for Disease and Control Prevention (CDC) because of its multidrug resistance. However, C. albicans stands as the major fungal pathogen of humans<a class="elsevierStyleCrossRefs" href="#bib0530">8,82</a>.Candida albicansC. albicans has various yeast-like morphologies (white, opaque, gray, and intestinal), two forms of hyphae (linear and sinusoidal), a pseudohyphae, and chlamydospores (<a class="elsevierStyleCrossRefs" href="#fig0005">Figs. 1 and 2</a>). Pseudohyphae remain attached after cytokinesis and generate mycelia after multiple rounds of cell division similar to hyphal cells. In addition to this great diversity of forms, C. albicans can grow in single-cell cultures, biofilms, and microcolonies<a class="elsevierStyleCrossRef" href="#bib0565">15</a>.<elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia>As a commensal fungus, C. albicans asymptomatically colonizes the oral mucosa, skin, vagina, and gastrointestinal tract of healthy individuals, and represents over 80% of vaginal and oral yeast strains isolated from asymptomatic humans. Therefore, it has various characteristics, both commensal and virulent, which allows it to be part of the natural microbiome in humans and, to invade tissues and organs<a class="elsevierStyleCrossRefs" href="#bib0565">15,85,89</a> in the case of a weakened immune system.C. albicans has a complex interaction with the host through the cell wall, which is the main structure in contact with the host. It is essential for fungal cellular integrity. The fungal cell wall protects the cells from environmental stress, including drastic changes in temperature, osmotic changes, dehydration, and immune response<a class="elsevierStyleCrossRef" href="#bib0535">9</a>.Among the most critical components of the C. albicans cell wall are chitin, glucan, and mannoproteins<a class="elsevierStyleCrossRef" href="#bib0535">9</a>. The latter are vital in morphogenesis and pathogenesis because they function as environmental sensors, structural elements, cross-linking enzymes, and adhesins; these components could be the point of interest in generating new antifungal drugs. Most of the proteins are characterized by their high heterogeneity, low abundance, low solubility, and hydrophobicity<a class="elsevierStyleCrossRef" href="#bib0850">72</a>. The recent analysis of the proteome of the C. albicans cell wall by mass spectrometry demonstrated the presence of proteins S7A, S13, and S16A of the 40S ribosome as well as the 60S ribosome protein L30, the glycolytic enzymes enolase 1 (Eno1), glyceraldehyde-3 phosphate dehydrogenases 1 and 2, pyruvate kinase, fructose bisphosphate aldolase, phosphoglycerate kinase 1 (Pgk1), phosphoglycerate mutase, and pyruvate decarboxylase, heat shock proteins SSA1 and SSB1, mitochondrial outer membrane protein porin 1 and ADP/ATP transporter protein, the plasma membrane ATPase PMA1 and the galactose transporter-related protein Hgt7, the elongation factor 1-α 1, cell wall agglutinin-like sequence protein 1 (Als1) and 2 (Als2), and the proteins 1,3-β-glucanosyltransferase PGA4 and chitinase 2<a class="elsevierStyleCrossRef" href="#bib0860">74</a>. Of these proteins, Eno1, Pgk1, and Als1 showed favorable immunogenicity<a class="elsevierStyleCrossRefs" href="#bib0595">21,77</a>. Experimental evidence indicates that Eno1 has transglutaminase activity in the cell wall of C. albicans, which is of crucial importance in osmotic protection and transition from yeast to mycelium<a class="elsevierStyleCrossRef" href="#bib0865">75</a>. Eno1 is the main antigen in patients with candidiasis<a class="elsevierStyleCrossRef" href="#bib0685">39</a>. Leu et al.<a class="elsevierStyleCrossRef" href="#bib0725">47</a> demonstrated that previous immunization with anti-Eno1 (CaS1) antibodies prolonged the survival of mice and zebrafish that developed candidiasis. CaS1-treated mice had significantly reduced levels of inflammatory cytokines and lower fungal load in the kidney and spleen. The authors also indicated that anti-Eno1 (CaS1) antibodies could be a potential immunotherapeutic treatment against C. albicans infections<a class="elsevierStyleCrossRef" href="#bib0725">47</a>.When in contact with the host, epithelial cells are the first line of defense: They induce the expression of antimicrobial peptides such as defensins, cathelicidins, and histatins, which favor the control of C. albicans growth in the commensal phase and during infection<a class="elsevierStyleCrossRef" href="#bib0670">36</a>.In addition, the tight junctions seal the space between the host cell surface and the mucosal lamina propia, thus preventing interepithelial invasion by C. albicans<a class="elsevierStyleCrossRef" href="#bib0975">97</a>. In the case of intestinal or vaginal epithelial cells, the mucus layer composed of mucins promotes protection and prevents direct contact with the epithelium. In the oral cavity, saliva contains various antimicrobial agents such as lactoferrin, lysozyme, histatins, cathelicidin (LL-37), calprotectin, and defensins, forming a chemical barrier that prevents the growth of C. albicans<a class="elsevierStyleCrossRefs" href="#bib0670">36,97</a>. However, patients in intensive care surgical units receive prolonged treatment with antibiotics, chemotherapy, or immunosuppressive drugs that favor the conversion of the yeast C. albicans into pathogenic cells (hyphae and pseudohyphae), thus leading to candidiasis<a class="elsevierStyleCrossRefs" href="#bib0530">8,82</a>. Therefore, C. albicans changes into an opportunistic fungus when there is an imbalance between the host's immunity and the commensal microenvironment, thus causing superficial or disseminated infection<a class="elsevierStyleCrossRefs" href="#bib0580">18,32</a>.Virulence factors contributing to the pathogenesis of C. albicansCandida albicans has various virulence factors such as the morphological transition from yeast cell to hyphae (both forms seem to be involved in pathogenesis), the expression of adhesins and invasins on the cell surface, the ability to damage host cells, biofilm formation, and secretion of hydrolytic enzymes<a class="elsevierStyleCrossRef" href="#bib0935">89</a>.When in contact with host cells, the cell wall of C. albicans has a role in adhesion to host cells through adhesins as well as intercellular communication, i.e., the “glycan code.” This interaction results in the development of a pathogenic state or the production of a resistance reaction by the host<a class="elsevierStyleCrossRef" href="#bib0840">70</a>. The central regulator of fungal adherence is the transcription factor Bcr1 whose target genes are ALS3, ALS1, ECE1, and HWP1 that also favor biofilm formation<a class="elsevierStyleCrossRef" href="#bib0800">62</a>. Among the most studied adhesins are agglutinin-like sequence proteins (ALS). Of the ALS family proteins (Als1-9), Als 5-7 and 9 are found on the surface of yeast cells. Als3 is expressed exclusively in the hyphae and binds E-cadherins on epithelial cells and N-cadherins on endothelial cells. Als3 and Als1 are involved in C. albicans biofilm formation. Hosseini et al.<a class="elsevierStyleCrossRef" href="#bib0675">37</a> reported clinical isolates of C. albicans expressing Als1 and Als3 that were resistant to fluconazole; adherence was more substantial than in the controls (cells that do not express Als1 and Als3).Another protein capable of binding epithelial E-cadherins is Ssa1 (Hsp70-like heat shock protein). Als3 and Ssa1 induce endocytosis of C. albicans in host cells. However, the active penetration generated by hyphae is the primary mechanism implemented by C. albicans to invade tissue<a class="elsevierStyleCrossRefs" href="#bib0775">57,59</a>.Another crucial virulence protein is hyphal wall protein 1 (Hwp1): The N-terminal region of Hwp1 serves as a substrate for epithelial cell transglutaminase, thus resulting in covalent binding of C. albicans to epithelial cell proteins, which appears to be essential in the development of oropharyngeal candidiasis but not for disseminated candidiasis. The adhesion of Candida cells by the action of the mentioned adhesins can induce endocytosis and active penetration into the host cells to later spread in the tissues, bloodstream, and organs<a class="elsevierStyleCrossRef" href="#bib0750">52</a>.Pleomorphic transitionThe morphological change from unicellular yeast to filamentous hyphae form is crucial in the virulence of C. albicans. The virulence capacity of hyphae is not produced by their morphology per se but by the expression of specific genes. For example, the Csa2 protein participates in the utilization of iron from hemoglobin and favors the growth of hyphae<a class="elsevierStyleCrossRef" href="#bib0680">38</a>. Another protein involved in the regulation of morphogenesis and biofilm formation is Hgc, which is related to cyclin G1 and the deletion of the gene encoding HGC1 attenuates the virulence of C. albicans in systemic infections in mice<a class="elsevierStyleCrossRef" href="#bib0980">98</a>.Various studies indicate that in an infectious process, the C. albicans yeast cells spread to other regions of the organism via a phagocyte-dependent mechanism, where neutrophils and macrophages can be vehicles for dissemination, while the hypha invades and damages host tissue by directing growth in response to contact with a solid surface, a process called thigmotropism<a class="elsevierStyleCrossRefs" href="#bib0630">28,36</a>.Macrophages phagocytize fungal cells in animal models of C. albicans infection. Hypha formation within the macrophages is related to damage to the phagosome. This process induces metabolic starvation and the evasion of the acidic environment by changing the pH value to neutral due to the production of neutralizing metabolites<a class="elsevierStyleCrossRef" href="#bib0710">44</a>. Hyphal formation and β-glucan masking inhibit phagosome acidification of macrophages, thus leading to intracellular hyphal formation and causing macrophage cell death due to physical forces<a class="elsevierStyleCrossRef" href="#bib0505">3</a>. The binding of Staphylococcus aureus cells to the hyphae of C. albicans facilitates the dissemination of bacteria through mucosal barriers. These are often isolated simultaneously in cases of infections associated with biofilms<a class="elsevierStyleCrossRef" href="#bib0680">38</a>.Candida albicans biofilmsMicrobial biofilms are communities of cells that adhere to solid surfaces or are present at liquid–air interfaces. They are the most common growth stage of growth for many microbial species and are often more resistant to drugs and physical insults<a class="elsevierStyleCrossRef" href="#bib0745">51</a>. The cellular composition of C. albicans biofilms includes two main types of cells: yeast (small, oval cells) and long, tubular hyphal cells<a class="elsevierStyleCrossRef" href="#bib0625">27</a>.As the structure of C. albicans biofilm matures, its outer layers release yeast cells, which are thought to disperse and mediate the spread of C. albicans to other tissues; therefore, they are an essential part of the infection process<a class="elsevierStyleCrossRef" href="#bib0965">95</a>. Various studies show that the Candida biofilm matrix comprises carbohydrates, proteins, nucleic acids, hexosamine, phosphorus, and uronic acid<a class="elsevierStyleCrossRef" href="#bib0500">2</a>. This matrix controls cell dispersion, protects against the immune system, and participates in developing resistance to azoles, polyenes, and pyrimidine analogs by not allowing the passage of these antimycotics<a class="elsevierStyleCrossRef" href="#bib0895">81</a>. One of the main components of the extracellular biofilm matrix is β-1,3 glucan. Different genes (BGL2, PHR1, and XOG1) are involved in crosslinking during planktonic cell growth, remodeling, and elongation of glucan chains<a class="elsevierStyleCrossRef" href="#bib0930">88</a>. The extracellular polysaccharide matrix of Candida biofilms facilitates adhesion to surfaces and other biopolymers, thus generating biofilms with structural integrity<a class="elsevierStyleCrossRef" href="#bib0655">33</a>. C. albicans has two transcriptional regulators of extracellular matrix generation in biofilms: Rlm1 and Zap1. Experimental evidence indicates that deletion of Rlm1 decreases matrix levels. Conversely, Zap1 deletion leads to the accumulation of excess extracellular matrix<a class="elsevierStyleCrossRef" href="#bib0805">63</a>.The life cycle of C. albicans biofilms begins when planktonic yeast cells adhere to the substrate, i.e., either hard (such as biomaterials that are part of a prosthetic device or the surface of a denture) or soft (such as a layer of mucosal epithelium in the oral or vaginal cavity) to then proliferate and mature into a structured biofilm composed of layers of yeast, pseudohyphae, and hyphae. The cells that make up the biofilm then disperse or their disintegration occurs at the end of the cycle<a class="elsevierStyleCrossRefs" href="#bib0645">31,92</a>.One of the main problems in hospital environments is the formation of biofilms on the surface of medical devices implemented in patients’ treatment. For example, the formation of biofilms on catheters, heart valves and dentures have a high capacity to promote infections that progressively spread to the bloodstream and generate systemic infections<a class="elsevierStyleCrossRefs" href="#bib0740">50,63</a>. Current estimates of the biofilm development risk on catheters is 30%; however, this depends on the location of the device<a class="elsevierStyleCrossRef" href="#bib0755">53</a>.Biofilms are characterized by drug resistance, and thus, removing the device that exhibits biofilm formation ends up being the most viable and effective option to reduce the risk of systemic infection. However, it is problematic if the patients are in a severe state of the disease or need a surgical procedure for their removal<a class="elsevierStyleCrossRef" href="#bib0740">50</a>.Secreted hydrolytic enzymesVarious hydrolytic enzymes (proteases, phospholipases, lipases, and hemolysins) secreted by C. albicans contribute to the host invasion process. Secreted aspartic proteases (Saps) encoded by a family of genes (SAP1 to SAP10) are factors associated with the virulence of C. albicans. They degrade human proteins such as hemoglobin, albumin, keratin, collagen, laminin, fibronectin, mucin, and almost all immunoglobulins. Sap9 and Sap10 remain bound to the cell surface and are strongly involved in biofilm formation by C. albicans unlike other members of the family<a class="elsevierStyleCrossRef" href="#bib0695">41</a>. However, experimental evidence suggests that Sap1 to Sap6 do not play a significant role in the virulence of C. albicans in a murine model of disseminated candidiasis<a class="elsevierStyleCrossRef" href="#bib0555">13</a>.Phospholipases (PLs) play an essential role in tissue invasion by Candida. PLs are enzymes that hydrolyze one or more ester bonds in glycerophospholipids. Studies have evaluated the importance of phospholipase B (PLB) in pathogenicity via the disruption of the host membranes; they allow the tip of the hypha to enter the cytoplasm, thus indicating that the null mutant of the same (PLB−/−) exhibited attenuated virulence in animal models<a class="elsevierStyleCrossRef" href="#bib0815">65</a>. Other PLs including PLC1, PLC2, and PLC3 subtypes are involved in the virulence of C. albicans because the heterozygous plc1/PLC1 mutant and the mutants lacking PLC2 and PLC3 were deficient in hyphae formation<a class="elsevierStyleCrossRef" href="#bib0830">68</a>.Lipases are another class of lipolytic enzymes that contribute to the virulence of C. albicans. These enzymes catalyze the hydrolysis of the ester bonds of triglycerides, thus releasing fatty acids. Paraje et al.<a class="elsevierStyleCrossRef" href="#bib0825">67</a> demonstrated in vitro that the lipase released from C. albicans induces cytotoxicity and favors the accumulation of lipid droplets in the cytoplasm of macrophages and hepatocytes<a class="elsevierStyleCrossRef" href="#bib0825">67</a>. During systemic infection, C. albicans produces hemolysins that lyse erythrocytes to obtain iron—an essential element for the growth and metabolism of this fungus. A comparative analysis of the ability of C. albicans and non-albicans Candida isolates from the oral cavity of human immunodeficiency virus (HIV)-positive patients showed that 92% of the species produce hemolysins with 58% of the strains exhibiting intense hemolytic activity<a class="elsevierStyleCrossRef" href="#bib0880">78</a>.Another virulence factor of C. albicans is the cytolytic exotoxin “candidalysin” that is only produced by the hyphae. It is essential during mucosal and systemic infection<a class="elsevierStyleCrossRefs" href="#bib0780">58,61</a>. Candidalysin is an amphipathic molecule that takes on an α-helical structure and facilitates the permeability of host cell membranes, thus resulting in the efflux of lactate dehydrogenase protein and destabilizing the host cell membranes<a class="elsevierStyleCrossRef" href="#bib0920">86</a>. The host may recognize C. albicans as a potentially pathogenic agent and initiate an immune response at this stage. Candidalysin is an immunostimulatory molecule and favors the influx of cytokines into the epithelium when C. albicans infection occurs<a class="elsevierStyleCrossRef" href="#bib0665">35</a>.In the oral infection, epithelial cells respond directly to the presence of candidalysin due to the activation of the epidermal growth factor receptor (EGFR), which is essential in the infection process<a class="elsevierStyleCrossRef" href="#bib0665">35</a>. This activation triggers the mitogen-activated protein kinase (MAPK) signaling pathway, which comprises ERK1/2 (extracellular signal-regulated kinase 1/2), JNK (c-Jun N-terminal kinase), and p38<a class="elsevierStyleCrossRef" href="#bib0795">61</a>. This leads to the production of interleukins 1 and 36 (IL-1 and IL-36) to promote the proliferation of innate TCR+ T cells as well as the expression of IL-17A, which is essential for antifungal defense in the oral mucosa<a class="elsevierStyleCrossRef" href="#bib0960">94</a>. Candidalysin can also induce the production of IL-1β, IL-36, and the NLRP3 inflammasome proinflammatory substances that help IL-17-mediated diseases<a class="elsevierStyleCrossRef" href="#bib0660">34</a>.Immune responseThe first step in the host defense against C. albicans is the innate immune system—particularly neutrophils, dendritic cells, and macrophages<a class="elsevierStyleCrossRef" href="#bib0770">56</a>. These phagocytes detect pathogen-associated molecular patterns (PMAPs) through pattern recognition receptors (PRRs), thus resulting in signal-mediated transcription and subsequent secretion of inflammatory mediators such as chemokines and cytokines that recruit other immune cells to eliminate the pathogen at the site of infection and activate the adaptive immune response<a class="elsevierStyleCrossRef" href="#bib0790">60</a>.C. albicans PMAPs responsible for the inflammatory response reside in the outer and inner layers of the cell wall<a class="elsevierStyleCrossRef" href="#bib0605">23</a>. The main PAMPs that trigger cytokine production and phagocytosis are mannoses and glucan, which are recognized by a variety of receptors<a class="elsevierStyleCrossRef" href="#bib0790">60</a>. The main PRR groups that recognize C. albicans are C-type lectin receptors, RIG I-type receptors, NOD-type receptors, and “Toll”-type receptors<a class="elsevierStyleCrossRef" href="#bib0515">5</a>. In the case of candidalysin, an activation of EGFR signaling is induced in a PAMP-independent manner promoting the secretion of neutrophil-targeted chemokines<a class="elsevierStyleCrossRef" href="#bib0665">35</a>.As a consequence of the hostile action of C. albicans, the epithelium in which the infection is found will tend to induce an innate immune response through the release of alarmins (also called damage-associated molecular patterns, DAMP), adenosine monophosphate (AMP), and chemokines of immune cells. The alarmins may be recognized by the receptors of the innate immune cells with subsequent activation<a class="elsevierStyleCrossRefs" href="#bib0570">16,34</a>.In the case of secondary infection by C. albicans, a synergy occurs between the activation of phagocytic cells through dectin-1/CARF9 or Toll 2 receptor-like pathways with T-helper 17 (Th17) lymphocytes that recognize Candida<a class="elsevierStyleCrossRef" href="#bib0730">48</a>. Individuals with mutations in genes that disrupt the T-helper 17 cells (Th17) or interleukin-17 receptor (IL-17R) signaling pathway are highly capable of becoming infected and developing chronic mucocutaneous candidiasis<a class="elsevierStyleCrossRef" href="#bib0955">93</a>.High-risk people currently receive antifungal prophylaxis. Although it effectively prevents Candida infections, its prolonged use can lead to the development of strains resistant to available antifungals<a class="elsevierStyleCrossRef" href="#bib0600">22</a>.Clinical aspectsC. albicans is believed to enter the gastrointestinal tract and colonize human skin as it passes through the birth canal during childbirth<a class="elsevierStyleCrossRef" href="#bib0970">96</a>. In healthy people, the presence of this microorganism is benign; however, immunosuppressed patients can frequently suffer from infections of the oral cavity called “oral candidiasis” (OC). Immunosuppressive infections such as HIV are a significant risk factor for developing OC in addition to the use of dentures and being very young or very old<a class="elsevierStyleCrossRef" href="#bib0760">54</a>. Pseudomembranous candidiasis is the classic presentation of OC. It manifests as white plaques that can be found on the tongue, buccal mucosa, oral pharynx and soft and hard palates. These lesions are caused by yeast overgrowth on the oral mucosa with desquamation of epithelial cells and accumulation of fungal hyphae, keratin, fibrin, and necrotic tissue<a class="elsevierStyleCrossRef" href="#bib0765">55</a>.Another type of candidiasis that affects millions of women each year is vulvovaginal candidiasis (VVC). It is estimated that approximately 75% of all women suffer from VVC at least once in their lives<a class="elsevierStyleCrossRef" href="#bib0915">85</a>. Predisposing factors for developing VVC are less well-defined than for OC and include uncontrolled diabetes mellitus, use of antibiotics, oral contraception, pregnancy, hormonal therapy, immunosuppression, corticosteroids, and genetic predisposition<a class="elsevierStyleCrossRef" href="#bib0635">29</a>. The main symptoms of VVC include itching, burning, and pain in the vaginal and vulvar tissue; these are commonly accompanied by odorless vaginal discharge<a class="elsevierStyleCrossRef" href="#bib0915">85</a>. Recent evidence shows that VVC is an immunopathology in which the immune response specifically involving the patient's neutrophils and related cytokines exacerbates the symptoms of the disease without adequately controlling the growth of Candida<a class="elsevierStyleCrossRef" href="#bib0870">76</a>.A complication caused by C. albicans is systemic candidiasis; its dissemination begins with the invasion of mucosal surfaces and subsequent entry into the bloodstream<a class="elsevierStyleCrossRef" href="#bib0925">87</a>. This infection is difficult to diagnose because the symptoms are similar to systemic bacterial infections. Systemic candidiasis is associated with a high mortality rate, neutropenia, and damage to the gastrointestinal mucosa<a class="elsevierStyleCrossRef" href="#bib0760">54</a>. Other factors that promote the development of disseminated candidiasis include central venous catheters that allow direct access of the fungus to the bloodstream, the application of broad-spectrum antibiotics (that favor antifungal resistance), and disrupted mucosal barriers including gastrointestinal barriers during trauma or surgery<a class="elsevierStyleCrossRef" href="#bib0760">54</a>. During systemic candidiasis, C. albicans has to break through the endothelial lining of blood vessels at the site of infection. Likewise, once disseminated, it must go back through the endothelium of the blood vessels to leave the circulation<a class="elsevierStyleCrossRef" href="#bib0640">30</a>. When C. albicans leaves the circulatory system, it spreads to virtually any organ including the brain, kidney, liver, and lung often leading to death<a class="elsevierStyleCrossRef" href="#bib0705">43</a>.Infection by SARS-CoV-2 (a type of respiratory coronavirus) causes COVID-19. This is mainly transmitted by respiratory droplets through close contact between people<a class="elsevierStyleCrossRef" href="#bib0550">12</a>. Between 5 and 30% of patients with COVID-19 develop a critical illness and require admission to the ICU where they may undergo mechanical ventilation, parenteral nutrition, broad-spectrum antibacterial therapy, indwelling central venous catheters, and administration of corticosteroids (due to their immunosuppressive capacity). These conditions favor the development of secondary infections<a class="elsevierStyleCrossRef" href="#bib0835">69</a>. COVID-19 is not a cause of—nor does it imply a direct association with—infection caused by C. albicans. This is because the immune system cells, which are the most important in the defense against C. albicans are not committed, e.g., monocytes, macrophages, and neutrophils. However, the use of indwelling central venous catheters (because of their propensity to form biofilms) and the administration of corticosteroids in patients with COVID-19 present a risk of producing a nosocomial infection caused by C. albicans. In fact, it has become a major concern because the transition from superficial to invasive candidiasis produces a lethality rate of 70% in patients with COVID-19 in critical condition<a class="elsevierStyleCrossRefs" href="#bib0585">19,24</a>. In a recent report of 989 Italian individuals with COVID-19, 21 candidemia cases were detected, indicating a marked prevalence among these patients versus a historical cohort<a class="elsevierStyleCrossRef" href="#bib0810">64</a>.Drugs used to treat infections caused by C. albicansFungal resistance to currently used drugs is a growing problem, and although C. albicans is the most common species of Candida that causes severe infections, other species such as C. auris, C. glabrata and C. parapsilosis<a class="elsevierStyleCrossRef" href="#bib0530">8</a> have developed vast antifungal resistance. The antifungals mainly used to treat infections caused by Candida species are the azoles, echinocandins, and polyenes; however, these drugs tend to not be successful when the infection involves the C. albicans biofilm<a class="elsevierStyleCrossRefs" href="#bib0560">14,26</a>. Unfortunately, these treatment options have become unsatisfactory due to the increased development of resistance, selective pressure, the unavailability of conventional antifungals for systemic administration, and adverse effects at higher drug concentrations<a class="elsevierStyleCrossRef" href="#bib0690">40</a>.Resistance to antifungal drugs can be divided into two forms: clinical and mycological resistance. Clinical resistance is the incomplete eradication of the fungus in a patient who was administered a drug with antifungal activity in vitro against the fungus in question. Mycological resistance allows the fungus to grow and reproduce despite the presence of the drug with antifungal activity demonstrated in vitro<a class="elsevierStyleCrossRef" href="#bib0845">71</a>. Antifungals currently used to treat candidiasis have certain deficiencies, for example, polyenes that cause nephrotoxicity, echinocandins with an exclusive intravenous route, and some thiazoles that have toxicity and difficulties in their absorption<a class="elsevierStyleCrossRef" href="#bib0715">45</a>.AzolesAzoles are responsible for inhibiting the growth and replication of fungi by inhibiting the enzyme lanosterol 14-α-demethylase (Erg11p). This enzyme is responsible for the conversion of lanosterol into ergosterol—a limiting step in the biosynthesis of ergosterol, which is the most abundant fungal cell membrane<a class="elsevierStyleCrossRef" href="#bib0525">7</a>. Fluconazole, itraconazole, and voriconazole are azole drugs that are used to treat C. albicans infections due to their high bioavailability<a class="elsevierStyleCrossRef" href="#bib0615">25</a>. Fluconazole is the most widely used antifungal drug; however, the current antifungal resistance exhibited by many fungal species has caused a limitation in its use<a class="elsevierStyleCrossRef" href="#bib0940">90</a>.EchinocandinsEchinocandins are the drugs of choice for most cases of candidemia and invasive candidiasis<a class="elsevierStyleCrossRef" href="#bib0890">80</a>. The mechanism of action of echinocandins is the non-competitive inhibition of (1,3)-β-d-glucan synthase—this molecule synthesizes the polysaccharide 1,3-β-d-glucan, which is part of the cell wall. It causes osmotic deregulation of the fungus and subsequent lysis. There are currently three molecules that work under this concept: caspofungin, micafungin, and anidulafungin<a class="elsevierStyleCrossRefs" href="#bib0720">46,91</a>. Resistance to these drugs is developed thanks to mutations in the FKS gene that encodes the enzyme glucan synthase<a class="elsevierStyleCrossRef" href="#bib0510">4</a>.PolyenesFungicidal polyenes are amphipathic drugs. The main mechanism of action of these chemicals is their binding to the fungal cell membrane ergosterol to form transmembrane channels, thus acting as an exit gate for the cell contents (including K+ and Na+ ions) until the cell lyses<a class="elsevierStyleCrossRefs" href="#bib0905">83,84</a>. However, due to the similarity between ergosterol and cholesterol and the low solubility of polyenes, the latter compounds tend to have substantial adverse effects in patients, leading to further limiting their use. Some examples of polyenes are amphotericin B and nystatin<a class="elsevierStyleCrossRef" href="#bib0540">10</a>.Resistance to polyenes is due to changes in ergosterol molecules or plasma membrane content as well as the exchange between ergosterol, cholesterol, or stigmasterol (components of the cell membrane) for 3-hydroxy or 3-oxo sterols, which have less affinity for polyenes<a class="elsevierStyleCrossRef" href="#bib0495">1</a>.ConclusionsThere has been a significant increase in potentially fatal infections caused by Candida. As the main pathogenic fungus of humans, C. albicans is characterized by a complex interaction with host cells, the bacterial microbiome, and the immune system. The increase in people facing predisposing conditions such as cancer chemotherapy, organ transplants, or HIV infections is becoming a greater risk for developing yeast infections. These infections could be managed more effectively if more rapid and specific diagnostic and therapeutic alternatives were available as well as the development of new therapeutic alternatives for the timely identification of fungal species and species with multi-drug resistance in patients undergoing long-term therapies. Therefore, understanding how the interactions of virulence factors, the microbiome, and the host response contribute to a Candida infection is of clinical relevance. There is also a need for laboratories to perform routine in vitro susceptibility testing in isolates from immunocompromised patients.Conflict of interestsThe authors declare no conflict of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:21 [ 0 => array:3 [ "identificador" => "xres1914223" "titulo" => "Highlights" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:3 [ "identificador" => "xres1914225" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 2 => array:2 [ "identificador" => "xpalclavsec1652802" "titulo" => "Keywords" ] 3 => array:3 [ "identificador" => "xres1914224" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0015" ] ] ] 4 => array:2 [ "identificador" => "xpalclavsec1652801" "titulo" => "Palabras clave" ] 5 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 6 => array:2 [ "identificador" => "sec0010" "titulo" => "Candida albicans" ] 7 => array:2 [ "identificador" => "sec0015" "titulo" => "Virulence factors contributing to the pathogenesis of C. albicans" ] 8 => array:2 [ "identificador" => "sec0020" "titulo" => "Pleomorphic transition" ] 9 => array:2 [ "identificador" => "sec0025" "titulo" => "Candida albicans biofilms" ] 10 => array:2 [ "identificador" => "sec0030" "titulo" => "Secreted hydrolytic enzymes" ] 11 => array:2 [ "identificador" => "sec0035" "titulo" => "Immune response" ] 12 => array:2 [ "identificador" => "sec0040" "titulo" => "Clinical aspects" ] 13 => array:2 [ "identificador" => "sec0045" "titulo" => "Drugs used to treat infections caused by C. albicans" ] 14 => array:2 [ "identificador" => "sec0050" "titulo" => "Azoles" ] 15 => array:2 [ "identificador" => "sec0055" "titulo" => "Echinocandins" ] 16 => array:2 [ "identificador" => "sec0060" "titulo" => "Polyenes" ] 17 => array:2 [ "identificador" => "sec0065" "titulo" => "Conclusions" ] 18 => array:2 [ "identificador" => "sec0070" "titulo" => "Conflict of interests" ] 19 => array:2 [ "identificador" => "xack671500" "titulo" => "Acknowledgments" ] 20 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2022-03-18" "fechaAceptado" => "2022-08-23" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1652802" "palabras" => array:3 [ 0 => "Candida albicans" 1 => "Candidiasis" 2 => "Virulence factors" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1652801" "palabras" => array:3 [ 0 => "Candida albicans" 1 => "Candidiasis" 2 => "Factores de virulencia" ] ] ] ] "tieneResumen" => true "highlights" => array:2 [ "titulo" => "Highlights" "resumen" => "<ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005">•Candida albicans is the main opportunistic fungus of humans.</li><li class="elsevierStyleListItem" id="lsti0010">•Eno1, Pgk1 and Als1 of C. albicans have significant immunogenicity.</li><li class="elsevierStyleListItem" id="lsti0015">•Virulence factors involved in the pathogenesis of C. albicans.</li></ul>" ] "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Candida albicans is a commensal of the mammalian microbiome and the primary pathogenic fungus of humans. It becomes a severe health problem in immunocompromised patients and can cause a wide variety of mucosal and systemic infections. The interaction between C. albicans and host cells is characterized by the expression of virulence factors such as adhesins and invasins, the secretion of hydrolytic enzymes, a transition from yeast to filamentous hyphae form, and the ability to form biofilms; these features collectively result in cell adhesion, invasion, and damage. This review describes complex commensal interactions of C. albicans with host cells and the cellular events that it triggers in a pathogenic environment. We also review the host immune response induced by C. albicans antigens and the mechanisms developed by this fungus to avoid the action of antifungal agents." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "Candida albicans es un comensal del microbioma de mamíferos y el principal hongo patógeno de humanos. En pacientes inmunocomprometidos se convierte en un grave problema de salud por causar una amplia variedad de infecciones en mucosas y sistémicas. La interacción entre C. albicans y las células del huésped lleva a la expresión de factores de virulencia, como adhesinas e invasinas, a la secreción de enzimas hidrolíticas y a la transición de levadura a hifa filamentosa, capaz de para formar biopelículas, lo que genera adherencia, invasión y daño celular. En esta revisión describimos la compleja interacción comensal de C. albicans con la célula huésped y los eventos celulares que ejecuta en un ambiente patogénico. También se revisa la respuesta inmunitaria del huésped inducida por antígenos de C. albicans y los mecanismos desarrollados por este hongo para evitar la acción de agentes antifúngicos." ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1181 "Ancho" => 2540 "Tamanyo" => 533911 ] ] "descripcion" => array:1 [ "en" => "Candida albicans cells analyzed by scanning electron microscopy. In (A), yeasts are in the process of budding, the arrows indicate the site of cell division between the mother cell and the daughter cell. In (B), mycelia of C. albicans, involved in tissue invasion during the infectious process." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 967 "Ancho" => 2474 "Tamanyo" => 331127 ] ] "descripcion" => array:1 [ "en" => "C. albicans cells in cell transition analyzed by light microscopy. In (A), a combination of chlamydospores (arrowheads) and hyphae (arrows) are found. In (B), pseudohyphae (asterisk), chlamydospores (arrowhead), and multicellular hyphae (arrows) are seen. 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Conacyt for the doctoral scholarship granted with the number 346900 with which the experiments were carried out." 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Candida albicans el principal hongo patógeno oportunista en humanos

Ignacio Uriel Macias-Paza, Salvador Pérez-Hernándeza, Alejandra Tavera-Tapiaa, Juan Pedro Luna-Ariasb, José Eugenio Guerra-Cárdenasa, Elizabeth Reyna-Beltrána,

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ereyna@docentes.uat.edu.mx

Corresponding author.

a Faculty of Medicine “Dr. Alberto Romo Caballero”, Autonomous University of Tamaulipas, Tampico (Tamaulipas), Mexico

b Department of Cell Biology, Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav-IPN), Mexico

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      "titulo" => "Comprehensive evaluation of abattoirs with no Hazard Analysis Critical Control Point plan in Tucum&#225;n&#44; Argentina"
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          "autoresLista" => "Gabriela P&#233;rez Terrazzino, Magdalena Costa, Alejandro L&#243;pez Campo, Carolina Saade, Mar&#237;a Paula Moreno Mochi, Marcelo Signorini, Ariel Roge, Claudia Van Der Ploeg, Gerardo Leotta, Mar&#237;a &#193;ngela Jure"
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          "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8226;</span><p id="par0005" class="elsevierStylePara elsevierViewall">Study focused on two abattoirs without HACCP plan from Tucum&#225;n&#44; Argentina&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8226;</span><p id="par0010" class="elsevierStylePara elsevierViewall">Risk estimation showed a marked predominance of high risk in both abattoirs&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8226;</span><p id="par0015" class="elsevierStylePara elsevierViewall">Differences of indicator microorganisms between abattoirs were not significant&#46;</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">&#8226;</span><p id="par0020" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Salmonella</span> spp&#46; and STEC were isolated from carcass and environmental samples&#46;</p></li><li class="elsevierStyleListItem" id="lsti0025"><span class="elsevierStyleLabel">&#8226;</span><p id="par0025" class="elsevierStylePara elsevierViewall">The need to work with authority in search of a standard remains unaddressed&#46;</p></li></ul></p></span>"
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    "cabecera" => "<span class="elsevierStyleTextfn">Special article</span>"
    "titulo" => "<span class="elsevierStyleItalic">Candida albicans</span> the main opportunistic pathogenic fungus in humans"
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        "autoresLista" => "Ignacio Uriel Macias-Paz, Salvador P&#233;rez-Hern&#225;ndez, Alejandra Tavera-Tapia, Juan Pedro Luna-Arias, Jos&#233; Eugenio Guerra-C&#225;rdenas, Elizabeth Reyna-Beltr&#225;n"
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            "entidad" => "Faculty of Medicine &#8220;Dr&#46; Alberto Romo Caballero&#8221;&#44; Autonomous University of Tamaulipas&#44; Tampico &#40;Tamaulipas&#41;&#44; Mexico"
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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Candida albicans</span> cells analyzed by scanning electron microscopy&#46; In &#40;A&#41;&#44; yeasts are in the process of budding&#44; the arrows indicate the site of cell division between the mother cell and the daughter cell&#46; In &#40;B&#41;&#44; mycelia of <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; involved in tissue invasion during the infectious process&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Introduction</span><p id="par0020" class="elsevierStylePara elsevierViewall">Fungal infections cause about 1&#46;7 million deaths worldwide per year mainly in immunocompromised individuals with two or more pathological conditions<a class="elsevierStyleCrossRefs" href="#bib0520"><span class="elsevierStyleSup">6&#44;42</span></a>&#46; The incidence of infections caused by the genus <span class="elsevierStyleItalic">Candida</span> has steadily increased since the 1970s perhaps due to an increased risk of opportunistic infections&#44; the improvement in clinical procedures that identify fungi causing nosocomial infections&#44; as well as the development of antifungal resistance due to prolonged exposure to treatment<a class="elsevierStyleCrossRef" href="#bib0545"><span class="elsevierStyleSup">11</span></a>&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">There are currently more than 150 species of <span class="elsevierStyleItalic">Candida</span>&#44; and approximately 20 are known to cause infections in humans&#46; <span class="elsevierStyleItalic">Candida albicans</span> is the main causative agent of candidiasis and the primary fungal infection in adults and pediatric patients<a class="elsevierStyleCrossRefs" href="#bib0530"><span class="elsevierStyleSup">8&#44;66&#44;82</span></a>&#46; In the USA&#44; it was reported that sepsis caused by <span class="elsevierStyleItalic">C&#46; albicans</span> has a mortality rate of approximately 40&#37;&#44; which is higher than any other sepsis caused by bacteria or fungi<a class="elsevierStyleCrossRef" href="#bib0935"><span class="elsevierStyleSup">89</span></a>&#46; Infections caused by the genus <span class="elsevierStyleItalic">Candida</span> are the main cause of nosocomial fungal infections especially in tertiary care hospitals<a class="elsevierStyleCrossRef" href="#bib0575"><span class="elsevierStyleSup">17</span></a>&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">In recent decades&#44; other non-albicans species such as <span class="elsevierStyleItalic">C&#46; glabrata</span>&#44; <span class="elsevierStyleItalic">C&#46; parapsilosis</span>&#44; <span class="elsevierStyleItalic">C&#46; tropicalis</span>&#44; <span class="elsevierStyleItalic">C&#46; krusei</span> &#40;<span class="elsevierStyleItalic">Pichia kudriavzevii</span>&#41;<span class="elsevierStyleItalic">&#44; C&#46; dubliniensis</span>&#44; <span class="elsevierStyleItalic">C&#46; kefyr</span>&#44; <span class="elsevierStyleItalic">C&#46; famata</span>&#44; <span class="elsevierStyleItalic">C&#46; auris</span> and others have become highly relevant at the clinical level due to their increasing prevalence as etiologic agents of candidiasis<a class="elsevierStyleCrossRefs" href="#bib0590"><span class="elsevierStyleSup">20&#44;49&#44;73&#44;79&#44;82</span></a>&#46; In particular&#44; <span class="elsevierStyleItalic">C&#46; auris</span> is considered an emerging serious global health threat by the Centers for Disease and Control Prevention &#40;CDC&#41; because of its multidrug resistance&#46; However&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> stands as the major fungal pathogen of humans<a class="elsevierStyleCrossRefs" href="#bib0530"><span class="elsevierStyleSup">8&#44;82</span></a>&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Candida albicans</span><p id="par0035" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">C&#46; albicans</span> has various yeast-like morphologies &#40;white&#44; opaque&#44; gray&#44; and intestinal&#41;&#44; two forms of hyphae &#40;linear and sinusoidal&#41;&#44; a pseudohyphae&#44; and chlamydospores &#40;<a class="elsevierStyleCrossRefs" href="#fig0005">Figs&#46; 1 and 2</a>&#41;&#46; Pseudohyphae remain attached after cytokinesis and generate mycelia after multiple rounds of cell division similar to hyphal cells&#46; In addition to this great diversity of forms&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> can grow in single-cell cultures&#44; biofilms&#44; and microcolonies<a class="elsevierStyleCrossRef" href="#bib0565"><span class="elsevierStyleSup">15</span></a>&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall">As a commensal fungus&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> asymptomatically colonizes the oral mucosa&#44; skin&#44; vagina&#44; and gastrointestinal tract of healthy individuals&#44; and represents over 80&#37; of vaginal and oral yeast strains isolated from asymptomatic humans&#46; Therefore&#44; it has various characteristics&#44; both commensal and virulent&#44; which allows it to be part of the natural microbiome in humans and&#44; to invade tissues and organs<a class="elsevierStyleCrossRefs" href="#bib0565"><span class="elsevierStyleSup">15&#44;85&#44;89</span></a> in the case of a weakened immune system&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">C&#46; albicans</span> has a complex interaction with the host through the cell wall&#44; which is the main structure in contact with the host&#46; It is essential for fungal cellular integrity&#46; The fungal cell wall protects the cells from environmental stress&#44; including drastic changes in temperature&#44; osmotic changes&#44; dehydration&#44; and immune response<a class="elsevierStyleCrossRef" href="#bib0535"><span class="elsevierStyleSup">9</span></a>&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Among the most critical components of the <span class="elsevierStyleItalic">C&#46; albicans</span> cell wall are chitin&#44; glucan&#44; and mannoproteins<a class="elsevierStyleCrossRef" href="#bib0535"><span class="elsevierStyleSup">9</span></a>&#46; The latter are vital in morphogenesis and pathogenesis because they function as environmental sensors&#44; structural elements&#44; cross-linking enzymes&#44; and adhesins&#59; these components could be the point of interest in generating new antifungal drugs&#46; Most of the proteins are characterized by their high heterogeneity&#44; low abundance&#44; low solubility&#44; and hydrophobicity<a class="elsevierStyleCrossRef" href="#bib0850"><span class="elsevierStyleSup">72</span></a>&#46; The recent analysis of the proteome of the <span class="elsevierStyleItalic">C&#46; albicans</span> cell wall by mass spectrometry demonstrated the presence of proteins S7A&#44; S13&#44; and S16A of the 40S ribosome as well as the 60S ribosome protein L30&#44; the glycolytic enzymes enolase 1 &#40;Eno1&#41;&#44; glyceraldehyde-3 phosphate dehydrogenases 1 and 2&#44; pyruvate kinase&#44; fructose bisphosphate aldolase&#44; phosphoglycerate kinase 1 &#40;Pgk1&#41;&#44; phosphoglycerate mutase&#44; and pyruvate decarboxylase&#44; heat shock proteins SSA1 and SSB1&#44; mitochondrial outer membrane protein porin 1 and ADP&#47;ATP transporter protein&#44; the plasma membrane ATPase PMA1 and the galactose transporter-related protein Hgt7&#44; the elongation factor 1-&#945; 1&#44; cell wall agglutinin-like sequence protein 1 &#40;Als1&#41; and 2 &#40;Als2&#41;&#44; and the proteins 1&#44;3-&#946;-glucanosyltransferase PGA4 and chitinase 2<a class="elsevierStyleCrossRef" href="#bib0860"><span class="elsevierStyleSup">74</span></a>&#46; Of these proteins&#44; Eno1&#44; Pgk1&#44; and Als1 showed favorable immunogenicity<a class="elsevierStyleCrossRefs" href="#bib0595"><span class="elsevierStyleSup">21&#44;77</span></a>&#46; Experimental evidence indicates that Eno1 has transglutaminase activity in the cell wall of <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; which is of crucial importance in osmotic protection and transition from yeast to mycelium<a class="elsevierStyleCrossRef" href="#bib0865"><span class="elsevierStyleSup">75</span></a>&#46; Eno1 is the main antigen in patients with candidiasis<a class="elsevierStyleCrossRef" href="#bib0685"><span class="elsevierStyleSup">39</span></a>&#46; Leu et al&#46;<a class="elsevierStyleCrossRef" href="#bib0725"><span class="elsevierStyleSup">47</span></a> demonstrated that previous immunization with anti-Eno1 &#40;CaS1&#41; antibodies prolonged the survival of mice and zebrafish that developed candidiasis&#46; CaS1-treated mice had significantly reduced levels of inflammatory cytokines and lower fungal load in the kidney and spleen&#46; The authors also indicated that anti-Eno1 &#40;CaS1&#41; antibodies could be a potential immunotherapeutic treatment against <span class="elsevierStyleItalic">C&#46; albicans</span> infections<a class="elsevierStyleCrossRef" href="#bib0725"><span class="elsevierStyleSup">47</span></a>&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">When in contact with the host&#44; epithelial cells are the first line of defense&#58; They induce the expression of antimicrobial peptides such as defensins&#44; cathelicidins&#44; and histatins&#44; which favor the control of <span class="elsevierStyleItalic">C&#46; albicans</span> growth in the commensal phase and during infection<a class="elsevierStyleCrossRef" href="#bib0670"><span class="elsevierStyleSup">36</span></a>&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">In addition&#44; the tight junctions seal the space between the host cell surface and the mucosal lamina propia&#44; thus preventing interepithelial invasion by <span class="elsevierStyleItalic">C&#46; albicans</span><a class="elsevierStyleCrossRef" href="#bib0975"><span class="elsevierStyleSup">97</span></a>&#46; In the case of intestinal or vaginal epithelial cells&#44; the mucus layer composed of mucins promotes protection and prevents direct contact with the epithelium&#46; In the oral cavity&#44; saliva contains various antimicrobial agents such as lactoferrin&#44; lysozyme&#44; histatins&#44; cathelicidin &#40;LL-37&#41;&#44; calprotectin&#44; and defensins&#44; forming a chemical barrier that prevents the growth of <span class="elsevierStyleItalic">C&#46; albicans</span><a class="elsevierStyleCrossRefs" href="#bib0670"><span class="elsevierStyleSup">36&#44;97</span></a>&#46; However&#44; patients in intensive care surgical units receive prolonged treatment with antibiotics&#44; chemotherapy&#44; or immunosuppressive drugs that favor the conversion of the yeast <span class="elsevierStyleItalic">C&#46; albicans</span> into pathogenic cells &#40;hyphae and pseudohyphae&#41;&#44; thus leading to candidiasis<a class="elsevierStyleCrossRefs" href="#bib0530"><span class="elsevierStyleSup">8&#44;82</span></a>&#46; Therefore&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> changes into an opportunistic fungus when there is an imbalance between the host&#39;s immunity and the commensal microenvironment&#44; thus causing superficial or disseminated infection<a class="elsevierStyleCrossRefs" href="#bib0580"><span class="elsevierStyleSup">18&#44;32</span></a>&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Virulence factors contributing to the pathogenesis of <span class="elsevierStyleItalic">C&#46; albicans</span></span><p id="par0065" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Candida albicans</span> has various virulence factors such as the morphological transition from yeast cell to hyphae &#40;both forms seem to be involved in pathogenesis&#41;&#44; the expression of adhesins and invasins on the cell surface&#44; the ability to damage host cells&#44; biofilm formation&#44; and secretion of hydrolytic enzymes<a class="elsevierStyleCrossRef" href="#bib0935"><span class="elsevierStyleSup">89</span></a>&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">When in contact with host cells&#44; the cell wall of <span class="elsevierStyleItalic">C&#46; albicans</span> has a role in adhesion to host cells through adhesins as well as intercellular communication&#44; i&#46;e&#46;&#44; the &#8220;glycan code&#46;&#8221; This interaction results in the development of a pathogenic state or the production of a resistance reaction by the host<a class="elsevierStyleCrossRef" href="#bib0840"><span class="elsevierStyleSup">70</span></a>&#46; The central regulator of fungal adherence is the transcription factor Bcr1 whose target genes are <span class="elsevierStyleItalic">ALS3&#44; ALS1&#44; ECE1</span>&#44; and <span class="elsevierStyleItalic">HWP1</span> that also favor biofilm formation<a class="elsevierStyleCrossRef" href="#bib0800"><span class="elsevierStyleSup">62</span></a>&#46; Among the most studied adhesins are agglutinin-like sequence proteins &#40;ALS&#41;&#46; Of the ALS family proteins &#40;Als1-9&#41;&#44; Als 5-7 and 9 are found on the surface of yeast cells&#46; Als3 is expressed exclusively in the hyphae and binds E-cadherins on epithelial cells and N-cadherins on endothelial cells&#46; Als3 and Als1 are involved in <span class="elsevierStyleItalic">C&#46; albicans</span> biofilm formation&#46; Hosseini et al&#46;<a class="elsevierStyleCrossRef" href="#bib0675"><span class="elsevierStyleSup">37</span></a> reported clinical isolates of <span class="elsevierStyleItalic">C&#46; albicans</span> expressing Als1 and Als3 that were resistant to fluconazole&#59; adherence was more substantial than in the controls &#40;cells that do not express Als1 and Als3&#41;&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Another protein capable of binding epithelial E-cadherins is Ssa1 &#40;Hsp70-like heat shock protein&#41;&#46; Als3 and Ssa1 induce endocytosis of <span class="elsevierStyleItalic">C&#46; albicans</span> in host cells&#46; However&#44; the active penetration generated by hyphae is the primary mechanism implemented by <span class="elsevierStyleItalic">C&#46; albicans</span> to invade tissue<a class="elsevierStyleCrossRefs" href="#bib0775"><span class="elsevierStyleSup">57&#44;59</span></a>&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Another crucial virulence protein is hyphal wall protein 1 &#40;Hwp1&#41;&#58; The N-terminal region of Hwp1 serves as a substrate for epithelial cell transglutaminase&#44; thus resulting in covalent binding of <span class="elsevierStyleItalic">C&#46; albicans</span> to epithelial cell proteins&#44; which appears to be essential in the development of oropharyngeal candidiasis but not for disseminated candidiasis&#46; The adhesion of <span class="elsevierStyleItalic">Candida</span> cells by the action of the mentioned adhesins can induce endocytosis and active penetration into the host cells to later spread in the tissues&#44; bloodstream&#44; and organs<a class="elsevierStyleCrossRef" href="#bib0750"><span class="elsevierStyleSup">52</span></a>&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Pleomorphic transition</span><p id="par0085" class="elsevierStylePara elsevierViewall">The morphological change from unicellular yeast to filamentous hyphae form is crucial in the virulence of <span class="elsevierStyleItalic">C&#46; albicans</span>&#46; The virulence capacity of hyphae is not produced by their morphology per se but by the expression of specific genes&#46; For example&#44; the Csa2 protein participates in the utilization of iron from hemoglobin and favors the growth of hyphae<a class="elsevierStyleCrossRef" href="#bib0680"><span class="elsevierStyleSup">38</span></a>&#46; Another protein involved in the regulation of morphogenesis and biofilm formation is Hgc&#44; which is related to cyclin G1 and the deletion of the gene encoding <span class="elsevierStyleItalic">HGC1</span> attenuates the virulence of <span class="elsevierStyleItalic">C&#46; albicans</span> in systemic infections in mice<a class="elsevierStyleCrossRef" href="#bib0980"><span class="elsevierStyleSup">98</span></a>&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Various studies indicate that in an infectious process&#44; the <span class="elsevierStyleItalic">C&#46; albicans</span> yeast cells spread to other regions of the organism via a phagocyte-dependent mechanism&#44; where neutrophils and macrophages can be vehicles for dissemination&#44; while the hypha invades and damages host tissue by directing growth in response to contact with a solid surface&#44; a process called thigmotropism<a class="elsevierStyleCrossRefs" href="#bib0630"><span class="elsevierStyleSup">28&#44;36</span></a>&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">Macrophages phagocytize fungal cells in animal models of <span class="elsevierStyleItalic">C&#46; albicans</span> infection&#46; Hypha formation within the macrophages is related to damage to the phagosome&#46; This process induces metabolic starvation and the evasion of the acidic environment by changing the pH value to neutral due to the production of neutralizing metabolites<a class="elsevierStyleCrossRef" href="#bib0710"><span class="elsevierStyleSup">44</span></a>&#46; Hyphal formation and &#946;-glucan masking inhibit phagosome acidification of macrophages&#44; thus leading to intracellular hyphal formation and causing macrophage cell death due to physical forces<a class="elsevierStyleCrossRef" href="#bib0505"><span class="elsevierStyleSup">3</span></a>&#46; The binding of Staphylococcus aureus cells to the hyphae of <span class="elsevierStyleItalic">C&#46; albicans</span> facilitates the dissemination of bacteria through mucosal barriers&#46; These are often isolated simultaneously in cases of infections associated with biofilms<a class="elsevierStyleCrossRef" href="#bib0680"><span class="elsevierStyleSup">38</span></a>&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050"><span class="elsevierStyleItalic">Candida albicans</span> biofilms</span><p id="par0100" class="elsevierStylePara elsevierViewall">Microbial biofilms are communities of cells that adhere to solid surfaces or are present at liquid&#8211;air interfaces&#46; They are the most common growth stage of growth for many microbial species and are often more resistant to drugs and physical insults<a class="elsevierStyleCrossRef" href="#bib0745"><span class="elsevierStyleSup">51</span></a>&#46; The cellular composition of <span class="elsevierStyleItalic">C&#46; albicans</span> biofilms includes two main types of cells&#58; yeast &#40;small&#44; oval cells&#41; and long&#44; tubular hyphal cells<a class="elsevierStyleCrossRef" href="#bib0625"><span class="elsevierStyleSup">27</span></a>&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">As the structure of <span class="elsevierStyleItalic">C&#46; albicans</span> biofilm matures&#44; its outer layers release yeast cells&#44; which are thought to disperse and mediate the spread of <span class="elsevierStyleItalic">C&#46; albicans</span> to other tissues&#59; therefore&#44; they are an essential part of the infection process<a class="elsevierStyleCrossRef" href="#bib0965"><span class="elsevierStyleSup">95</span></a>&#46; Various studies show that the <span class="elsevierStyleItalic">Candida</span> biofilm matrix comprises carbohydrates&#44; proteins&#44; nucleic acids&#44; hexosamine&#44; phosphorus&#44; and uronic acid<a class="elsevierStyleCrossRef" href="#bib0500"><span class="elsevierStyleSup">2</span></a>&#46; This matrix controls cell dispersion&#44; protects against the immune system&#44; and participates in developing resistance to azoles&#44; polyenes&#44; and pyrimidine analogs by not allowing the passage of these antimycotics<a class="elsevierStyleCrossRef" href="#bib0895"><span class="elsevierStyleSup">81</span></a>&#46; One of the main components of the extracellular biofilm matrix is &#946;-1&#44;3 glucan&#46; Different genes &#40;<span class="elsevierStyleItalic">BGL2&#44; PHR1</span>&#44; and <span class="elsevierStyleItalic">XOG1</span>&#41; are involved in crosslinking during planktonic cell growth&#44; remodeling&#44; and elongation of glucan chains<a class="elsevierStyleCrossRef" href="#bib0930"><span class="elsevierStyleSup">88</span></a>&#46; The extracellular polysaccharide matrix of <span class="elsevierStyleItalic">Candida</span> biofilms facilitates adhesion to surfaces and other biopolymers&#44; thus generating biofilms with structural integrity<a class="elsevierStyleCrossRef" href="#bib0655"><span class="elsevierStyleSup">33</span></a>&#46; <span class="elsevierStyleItalic">C&#46; albicans</span> has two transcriptional regulators of extracellular matrix generation in biofilms&#58; Rlm1 and Zap1&#46; Experimental evidence indicates that deletion of Rlm1 decreases matrix levels&#46; Conversely&#44; Zap1 deletion leads to the accumulation of excess extracellular matrix<a class="elsevierStyleCrossRef" href="#bib0805"><span class="elsevierStyleSup">63</span></a>&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">The life cycle of <span class="elsevierStyleItalic">C&#46; albicans</span> biofilms begins when planktonic yeast cells adhere to the substrate&#44; i&#46;e&#46;&#44; either hard &#40;such as biomaterials that are part of a prosthetic device or the surface of a denture&#41; or soft &#40;such as a layer of mucosal epithelium in the oral or vaginal cavity&#41; to then proliferate and mature into a structured biofilm composed of layers of yeast&#44; pseudohyphae&#44; and hyphae&#46; The cells that make up the biofilm then disperse or their disintegration occurs at the end of the cycle<a class="elsevierStyleCrossRefs" href="#bib0645"><span class="elsevierStyleSup">31&#44;92</span></a>&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">One of the main problems in hospital environments is the formation of biofilms on the surface of medical devices implemented in patients&#8217; treatment&#46; For example&#44; the formation of biofilms on catheters&#44; heart valves and dentures have a high capacity to promote infections that progressively spread to the bloodstream and generate systemic infections<a class="elsevierStyleCrossRefs" href="#bib0740"><span class="elsevierStyleSup">50&#44;63</span></a>&#46; Current estimates of the biofilm development risk on catheters is 30&#37;&#59; however&#44; this depends on the location of the device<a class="elsevierStyleCrossRef" href="#bib0755"><span class="elsevierStyleSup">53</span></a>&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">Biofilms are characterized by drug resistance&#44; and thus&#44; removing the device that exhibits biofilm formation ends up being the most viable and effective option to reduce the risk of systemic infection&#46; However&#44; it is problematic if the patients are in a severe state of the disease or need a surgical procedure for their removal<a class="elsevierStyleCrossRef" href="#bib0740"><span class="elsevierStyleSup">50</span></a>&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Secreted hydrolytic enzymes</span><p id="par0125" class="elsevierStylePara elsevierViewall">Various hydrolytic enzymes &#40;proteases&#44; phospholipases&#44; lipases&#44; and hemolysins&#41; secreted by <span class="elsevierStyleItalic">C&#46; albicans</span> contribute to the host invasion process&#46; Secreted aspartic proteases &#40;Saps&#41; encoded by a family of genes &#40;SAP1 to SAP10&#41; are factors associated with the virulence of <span class="elsevierStyleItalic">C&#46; albicans</span>&#46; They degrade human proteins such as hemoglobin&#44; albumin&#44; keratin&#44; collagen&#44; laminin&#44; fibronectin&#44; mucin&#44; and almost all immunoglobulins&#46; Sap9 and Sap10 remain bound to the cell surface and are strongly involved in biofilm formation by <span class="elsevierStyleItalic">C&#46; albicans</span> unlike other members of the family<a class="elsevierStyleCrossRef" href="#bib0695"><span class="elsevierStyleSup">41</span></a>&#46; However&#44; experimental evidence suggests that Sap1 to Sap6 do not play a significant role in the virulence of <span class="elsevierStyleItalic">C&#46; albicans</span> in a murine model of disseminated candidiasis<a class="elsevierStyleCrossRef" href="#bib0555"><span class="elsevierStyleSup">13</span></a>&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">Phospholipases &#40;PLs&#41; play an essential role in tissue invasion by <span class="elsevierStyleItalic">Candida</span>&#46; PLs are enzymes that hydrolyze one or more ester bonds in glycerophospholipids&#46; Studies have evaluated the importance of phospholipase B &#40;PLB&#41; in pathogenicity via the disruption of the host membranes&#59; they allow the tip of the hypha to enter the cytoplasm&#44; thus indicating that the null mutant of the same &#40;PLB<span class="elsevierStyleSup">&#8722;&#47;&#8722;</span>&#41; exhibited attenuated virulence in animal models<a class="elsevierStyleCrossRef" href="#bib0815"><span class="elsevierStyleSup">65</span></a>&#46; Other PLs including <span class="elsevierStyleItalic">PLC1&#44; PLC2&#44;</span> and <span class="elsevierStyleItalic">PLC3</span> subtypes are involved in the virulence of <span class="elsevierStyleItalic">C&#46; albicans</span> because the heterozygous <span class="elsevierStyleItalic">plc1&#47;PLC1</span> mutant and the mutants lacking <span class="elsevierStyleItalic">PLC2</span> and <span class="elsevierStyleItalic">PLC3</span> were deficient in hyphae formation<a class="elsevierStyleCrossRef" href="#bib0830"><span class="elsevierStyleSup">68</span></a>&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">Lipases are another class of lipolytic enzymes that contribute to the virulence of <span class="elsevierStyleItalic">C&#46; albicans</span>&#46; These enzymes catalyze the hydrolysis of the ester bonds of triglycerides&#44; thus releasing fatty acids&#46; Paraje et al&#46;<a class="elsevierStyleCrossRef" href="#bib0825"><span class="elsevierStyleSup">67</span></a> demonstrated in vitro that the lipase released from <span class="elsevierStyleItalic">C&#46; albicans</span> induces cytotoxicity and favors the accumulation of lipid droplets in the cytoplasm of macrophages and hepatocytes<a class="elsevierStyleCrossRef" href="#bib0825"><span class="elsevierStyleSup">67</span></a>&#46; During systemic infection&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> produces hemolysins that lyse erythrocytes to obtain iron&#8212;an essential element for the growth and metabolism of this fungus&#46; A comparative analysis of the ability of <span class="elsevierStyleItalic">C&#46; albicans</span> and non-albicans <span class="elsevierStyleItalic">Candida</span> isolates from the oral cavity of human immunodeficiency virus &#40;HIV&#41;-positive patients showed that 92&#37; of the species produce hemolysins with 58&#37; of the strains exhibiting intense hemolytic activity<a class="elsevierStyleCrossRef" href="#bib0880"><span class="elsevierStyleSup">78</span></a>&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">Another virulence factor of <span class="elsevierStyleItalic">C&#46; albicans</span> is the cytolytic exotoxin &#8220;candidalysin&#8221; that is only produced by the hyphae&#46; It is essential during mucosal and systemic infection<a class="elsevierStyleCrossRefs" href="#bib0780"><span class="elsevierStyleSup">58&#44;61</span></a>&#46; Candidalysin is an amphipathic molecule that takes on an &#945;-helical structure and facilitates the permeability of host cell membranes&#44; thus resulting in the efflux of lactate dehydrogenase protein and destabilizing the host cell membranes<a class="elsevierStyleCrossRef" href="#bib0920"><span class="elsevierStyleSup">86</span></a>&#46; The host may recognize <span class="elsevierStyleItalic">C&#46; albicans</span> as a potentially pathogenic agent and initiate an immune response at this stage&#46; Candidalysin is an immunostimulatory molecule and favors the influx of cytokines into the epithelium when <span class="elsevierStyleItalic">C&#46; albicans</span> infection occurs<a class="elsevierStyleCrossRef" href="#bib0665"><span class="elsevierStyleSup">35</span></a>&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">In the oral infection&#44; epithelial cells respond directly to the presence of candidalysin due to the activation of the epidermal growth factor receptor &#40;EGFR&#41;&#44; which is essential in the infection process<a class="elsevierStyleCrossRef" href="#bib0665"><span class="elsevierStyleSup">35</span></a>&#46; This activation triggers the mitogen-activated protein kinase &#40;MAPK&#41; signaling pathway&#44; which comprises ERK1&#47;2 &#40;extracellular signal-regulated kinase 1&#47;2&#41;&#44; JNK &#40;c-Jun N-terminal kinase&#41;&#44; and p38<a class="elsevierStyleCrossRef" href="#bib0795"><span class="elsevierStyleSup">61</span></a>&#46; This leads to the production of interleukins 1 and 36 &#40;IL-1 and IL-36&#41; to promote the proliferation of innate TCR&#43; T cells as well as the expression of IL-17A&#44; which is essential for antifungal defense in the oral mucosa<a class="elsevierStyleCrossRef" href="#bib0960"><span class="elsevierStyleSup">94</span></a>&#46; Candidalysin can also induce the production of IL-1&#946;&#44; IL-36&#44; and the NLRP3 inflammasome proinflammatory substances that help IL-17-mediated diseases<a class="elsevierStyleCrossRef" href="#bib0660"><span class="elsevierStyleSup">34</span></a>&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Immune response</span><p id="par0150" class="elsevierStylePara elsevierViewall">The first step in the host defense against <span class="elsevierStyleItalic">C&#46; albicans</span> is the innate immune system&#8212;particularly neutrophils&#44; dendritic cells&#44; and macrophages<a class="elsevierStyleCrossRef" href="#bib0770"><span class="elsevierStyleSup">56</span></a>&#46; These phagocytes detect pathogen-associated molecular patterns &#40;PMAPs&#41; through pattern recognition receptors &#40;PRRs&#41;&#44; thus resulting in signal-mediated transcription and subsequent secretion of inflammatory mediators such as chemokines and cytokines that recruit other immune cells to eliminate the pathogen at the site of infection and activate the adaptive immune response<a class="elsevierStyleCrossRef" href="#bib0790"><span class="elsevierStyleSup">60</span></a>&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">C&#46; albicans</span> PMAPs responsible for the inflammatory response reside in the outer and inner layers of the cell wall<a class="elsevierStyleCrossRef" href="#bib0605"><span class="elsevierStyleSup">23</span></a>&#46; The main PAMPs that trigger cytokine production and phagocytosis are mannoses and glucan&#44; which are recognized by a variety of receptors<a class="elsevierStyleCrossRef" href="#bib0790"><span class="elsevierStyleSup">60</span></a>&#46; The main PRR groups that recognize <span class="elsevierStyleItalic">C&#46; albicans</span> are C-type lectin receptors&#44; RIG I-type receptors&#44; NOD-type receptors&#44; and &#8220;Toll&#8221;-type receptors<a class="elsevierStyleCrossRef" href="#bib0515"><span class="elsevierStyleSup">5</span></a>&#46; In the case of candidalysin&#44; an activation of EGFR signaling is induced in a PAMP-independent manner promoting the secretion of neutrophil-targeted chemokines<a class="elsevierStyleCrossRef" href="#bib0665"><span class="elsevierStyleSup">35</span></a>&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">As a consequence of the hostile action of <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; the epithelium in which the infection is found will tend to induce an innate immune response through the release of alarmins &#40;also called damage-associated molecular patterns&#44; DAMP&#41;&#44; adenosine monophosphate &#40;AMP&#41;&#44; and chemokines of immune cells&#46; The alarmins may be recognized by the receptors of the innate immune cells with subsequent activation<a class="elsevierStyleCrossRefs" href="#bib0570"><span class="elsevierStyleSup">16&#44;34</span></a>&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall">In the case of secondary infection by <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; a synergy occurs between the activation of phagocytic cells through dectin-1&#47;CARF9 or Toll 2 receptor-like pathways with T-helper 17 &#40;Th17&#41; lymphocytes that recognize <span class="elsevierStyleItalic">Candida</span><a class="elsevierStyleCrossRef" href="#bib0730"><span class="elsevierStyleSup">48</span></a>&#46; Individuals with mutations in genes that disrupt the T-helper 17 cells &#40;Th17&#41; or interleukin-17 receptor &#40;IL-17R&#41; signaling pathway are highly capable of becoming infected and developing chronic mucocutaneous candidiasis<a class="elsevierStyleCrossRef" href="#bib0955"><span class="elsevierStyleSup">93</span></a>&#46;</p><p id="par0170" class="elsevierStylePara elsevierViewall">High-risk people currently receive antifungal prophylaxis&#46; Although it effectively prevents <span class="elsevierStyleItalic">Candida</span> infections&#44; its prolonged use can lead to the development of strains resistant to available antifungals<a class="elsevierStyleCrossRef" href="#bib0600"><span class="elsevierStyleSup">22</span></a>&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Clinical aspects</span><p id="par0175" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">C&#46; albicans</span> is believed to enter the gastrointestinal tract and colonize human skin as it passes through the birth canal during childbirth<a class="elsevierStyleCrossRef" href="#bib0970"><span class="elsevierStyleSup">96</span></a>&#46; In healthy people&#44; the presence of this microorganism is benign&#59; however&#44; immunosuppressed patients can frequently suffer from infections of the oral cavity called &#8220;oral candidiasis&#8221; &#40;OC&#41;&#46; Immunosuppressive infections such as HIV are a significant risk factor for developing OC in addition to the use of dentures and being very young or very old<a class="elsevierStyleCrossRef" href="#bib0760"><span class="elsevierStyleSup">54</span></a>&#46; Pseudomembranous candidiasis is the classic presentation of OC&#46; It manifests as white plaques that can be found on the tongue&#44; buccal mucosa&#44; oral pharynx and soft and hard palates&#46; These lesions are caused by yeast overgrowth on the oral mucosa with desquamation of epithelial cells and accumulation of fungal hyphae&#44; keratin&#44; fibrin&#44; and necrotic tissue<a class="elsevierStyleCrossRef" href="#bib0765"><span class="elsevierStyleSup">55</span></a>&#46;</p><p id="par0180" class="elsevierStylePara elsevierViewall">Another type of candidiasis that affects millions of women each year is vulvovaginal candidiasis &#40;VVC&#41;&#46; It is estimated that approximately 75&#37; of all women suffer from VVC at least once in their lives<a class="elsevierStyleCrossRef" href="#bib0915"><span class="elsevierStyleSup">85</span></a>&#46; Predisposing factors for developing VVC are less well-defined than for OC and include uncontrolled diabetes mellitus&#44; use of antibiotics&#44; oral contraception&#44; pregnancy&#44; hormonal therapy&#44; immunosuppression&#44; corticosteroids&#44; and genetic predisposition<a class="elsevierStyleCrossRef" href="#bib0635"><span class="elsevierStyleSup">29</span></a>&#46; The main symptoms of VVC include itching&#44; burning&#44; and pain in the vaginal and vulvar tissue&#59; these are commonly accompanied by odorless vaginal discharge<a class="elsevierStyleCrossRef" href="#bib0915"><span class="elsevierStyleSup">85</span></a>&#46; Recent evidence shows that VVC is an immunopathology in which the immune response specifically involving the patient&#39;s neutrophils and related cytokines exacerbates the symptoms of the disease without adequately controlling the growth of <span class="elsevierStyleItalic">Candida</span><a class="elsevierStyleCrossRef" href="#bib0870"><span class="elsevierStyleSup">76</span></a>&#46;</p><p id="par0185" class="elsevierStylePara elsevierViewall">A complication caused by <span class="elsevierStyleItalic">C&#46; albicans</span> is systemic candidiasis&#59; its dissemination begins with the invasion of mucosal surfaces and subsequent entry into the bloodstream<a class="elsevierStyleCrossRef" href="#bib0925"><span class="elsevierStyleSup">87</span></a>&#46; This infection is difficult to diagnose because the symptoms are similar to systemic bacterial infections&#46; Systemic candidiasis is associated with a high mortality rate&#44; neutropenia&#44; and damage to the gastrointestinal mucosa<a class="elsevierStyleCrossRef" href="#bib0760"><span class="elsevierStyleSup">54</span></a>&#46; Other factors that promote the development of disseminated candidiasis include central venous catheters that allow direct access of the fungus to the bloodstream&#44; the application of broad-spectrum antibiotics &#40;that favor antifungal resistance&#41;&#44; and disrupted mucosal barriers including gastrointestinal barriers during trauma or surgery<a class="elsevierStyleCrossRef" href="#bib0760"><span class="elsevierStyleSup">54</span></a>&#46; During systemic candidiasis&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> has to break through the endothelial lining of blood vessels at the site of infection&#46; Likewise&#44; once disseminated&#44; it must go back through the endothelium of the blood vessels to leave the circulation<a class="elsevierStyleCrossRef" href="#bib0640"><span class="elsevierStyleSup">30</span></a>&#46; When <span class="elsevierStyleItalic">C&#46; albicans</span> leaves the circulatory system&#44; it spreads to virtually any organ including the brain&#44; kidney&#44; liver&#44; and lung often leading to death<a class="elsevierStyleCrossRef" href="#bib0705"><span class="elsevierStyleSup">43</span></a>&#46;</p><p id="par0190" class="elsevierStylePara elsevierViewall">Infection by SARS-CoV-2 &#40;a type of respiratory coronavirus&#41; causes COVID-19&#46; This is mainly transmitted by respiratory droplets through close contact between people<a class="elsevierStyleCrossRef" href="#bib0550"><span class="elsevierStyleSup">12</span></a>&#46; Between 5 and 30&#37; of patients with COVID-19 develop a critical illness and require admission to the ICU where they may undergo mechanical ventilation&#44; parenteral nutrition&#44; broad-spectrum antibacterial therapy&#44; indwelling central venous catheters&#44; and administration of corticosteroids &#40;due to their immunosuppressive capacity&#41;&#46; These conditions favor the development of secondary infections<a class="elsevierStyleCrossRef" href="#bib0835"><span class="elsevierStyleSup">69</span></a>&#46; COVID-19 is not a cause of&#8212;nor does it imply a direct association with&#8212;infection caused by <span class="elsevierStyleItalic">C&#46; albicans</span>&#46; This is because the immune system cells&#44; which are the most important in the defense against <span class="elsevierStyleItalic">C&#46; albicans</span> are not committed&#44; e&#46;g&#46;&#44; monocytes&#44; macrophages&#44; and neutrophils&#46; However&#44; the use of indwelling central venous catheters &#40;because of their propensity to form biofilms&#41; and the administration of corticosteroids in patients with COVID-19 present a risk of producing a nosocomial infection caused by <span class="elsevierStyleItalic">C&#46; albicans</span>&#46; In fact&#44; it has become a major concern because the transition from superficial to invasive candidiasis produces a lethality rate of 70&#37; in patients with COVID-19 in critical condition<a class="elsevierStyleCrossRefs" href="#bib0585"><span class="elsevierStyleSup">19&#44;24</span></a>&#46; In a recent report of 989 Italian individuals with COVID-19&#44; 21 candidemia cases were detected&#44; indicating a marked prevalence among these patients versus a historical cohort<a class="elsevierStyleCrossRef" href="#bib0810"><span class="elsevierStyleSup">64</span></a>&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Drugs used to treat infections caused by <span class="elsevierStyleItalic">C&#46; albicans</span></span><p id="par0195" class="elsevierStylePara elsevierViewall">Fungal resistance to currently used drugs is a growing problem&#44; and although <span class="elsevierStyleItalic">C&#46; albicans</span> is the most common species of <span class="elsevierStyleItalic">Candida</span> that causes severe infections&#44; other species such as <span class="elsevierStyleItalic">C&#46; auris</span>&#44; <span class="elsevierStyleItalic">C&#46; glabrata</span> and <span class="elsevierStyleItalic">C&#46; parapsilosis</span><a class="elsevierStyleCrossRef" href="#bib0530"><span class="elsevierStyleSup">8</span></a> have developed vast antifungal resistance&#46; The antifungals mainly used to treat infections caused by <span class="elsevierStyleItalic">Candida</span> species are the azoles&#44; echinocandins&#44; and polyenes&#59; however&#44; these drugs tend to not be successful when the infection involves the <span class="elsevierStyleItalic">C&#46; albicans</span> biofilm<a class="elsevierStyleCrossRefs" href="#bib0560"><span class="elsevierStyleSup">14&#44;26</span></a>&#46; Unfortunately&#44; these treatment options have become unsatisfactory due to the increased development of resistance&#44; selective pressure&#44; the unavailability of conventional antifungals for systemic administration&#44; and adverse effects at higher drug concentrations<a class="elsevierStyleCrossRef" href="#bib0690"><span class="elsevierStyleSup">40</span></a>&#46;</p><p id="par0200" class="elsevierStylePara elsevierViewall">Resistance to antifungal drugs can be divided into two forms&#58; clinical and mycological resistance&#46; Clinical resistance is the incomplete eradication of the fungus in a patient who was administered a drug with antifungal activity in vitro against the fungus in question&#46; Mycological resistance allows the fungus to grow and reproduce despite the presence of the drug with antifungal activity demonstrated in vitro<a class="elsevierStyleCrossRef" href="#bib0845"><span class="elsevierStyleSup">71</span></a>&#46; Antifungals currently used to treat candidiasis have certain deficiencies&#44; for example&#44; polyenes that cause nephrotoxicity&#44; echinocandins with an exclusive intravenous route&#44; and some thiazoles that have toxicity and difficulties in their absorption<a class="elsevierStyleCrossRef" href="#bib0715"><span class="elsevierStyleSup">45</span></a>&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Azoles</span><p id="par0205" class="elsevierStylePara elsevierViewall">Azoles are responsible for inhibiting the growth and replication of fungi by inhibiting the enzyme lanosterol 14-&#945;-demethylase &#40;Erg11p&#41;&#46; This enzyme is responsible for the conversion of lanosterol into ergosterol&#8212;a limiting step in the biosynthesis of ergosterol&#44; which is the most abundant fungal cell membrane<a class="elsevierStyleCrossRef" href="#bib0525"><span class="elsevierStyleSup">7</span></a>&#46; Fluconazole&#44; itraconazole&#44; and voriconazole are azole drugs that are used to treat <span class="elsevierStyleItalic">C&#46; albicans</span> infections due to their high bioavailability<a class="elsevierStyleCrossRef" href="#bib0615"><span class="elsevierStyleSup">25</span></a>&#46; Fluconazole is the most widely used antifungal drug&#59; however&#44; the current antifungal resistance exhibited by many fungal species has caused a limitation in its use<a class="elsevierStyleCrossRef" href="#bib0940"><span class="elsevierStyleSup">90</span></a>&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Echinocandins</span><p id="par0210" class="elsevierStylePara elsevierViewall">Echinocandins are the drugs of choice for most cases of candidemia and invasive candidiasis<a class="elsevierStyleCrossRef" href="#bib0890"><span class="elsevierStyleSup">80</span></a>&#46; The mechanism of action of echinocandins is the non-competitive inhibition of &#40;1&#44;3&#41;-&#946;-<span class="elsevierStyleSmallCaps">d</span>-glucan synthase&#8212;this molecule synthesizes the polysaccharide 1&#44;3-&#946;-<span class="elsevierStyleSmallCaps">d</span>-glucan&#44; which is part of the cell wall&#46; It causes osmotic deregulation of the fungus and subsequent lysis&#46; There are currently three molecules that work under this concept&#58; caspofungin&#44; micafungin&#44; and anidulafungin<a class="elsevierStyleCrossRefs" href="#bib0720"><span class="elsevierStyleSup">46&#44;91</span></a>&#46; Resistance to these drugs is developed thanks to mutations in the FKS gene that encodes the enzyme glucan synthase<a class="elsevierStyleCrossRef" href="#bib0510"><span class="elsevierStyleSup">4</span></a>&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Polyenes</span><p id="par0215" class="elsevierStylePara elsevierViewall">Fungicidal polyenes are amphipathic drugs&#46; The main mechanism of action of these chemicals is their binding to the fungal cell membrane ergosterol to form transmembrane channels&#44; thus acting as an exit gate for the cell contents &#40;including K<span class="elsevierStyleSup">&#43;</span> and Na<span class="elsevierStyleSup">&#43;</span> ions&#41; until the cell lyses<a class="elsevierStyleCrossRefs" href="#bib0905"><span class="elsevierStyleSup">83&#44;84</span></a>&#46; However&#44; due to the similarity between ergosterol and cholesterol and the low solubility of polyenes&#44; the latter compounds tend to have substantial adverse effects in patients&#44; leading to further limiting their use&#46; Some examples of polyenes are amphotericin B and nystatin<a class="elsevierStyleCrossRef" href="#bib0540"><span class="elsevierStyleSup">10</span></a>&#46;</p><p id="par0220" class="elsevierStylePara elsevierViewall">Resistance to polyenes is due to changes in ergosterol molecules or plasma membrane content as well as the exchange between ergosterol&#44; cholesterol&#44; or stigmasterol &#40;components of the cell membrane&#41; for 3-hydroxy or 3-oxo sterols&#44; which have less affinity for polyenes<a class="elsevierStyleCrossRef" href="#bib0495"><span class="elsevierStyleSup">1</span></a>&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Conclusions</span><p id="par0225" class="elsevierStylePara elsevierViewall">There has been a significant increase in potentially fatal infections caused by <span class="elsevierStyleItalic">Candida</span>&#46; As the main pathogenic fungus of humans&#44; <span class="elsevierStyleItalic">C&#46; albicans</span> is characterized by a complex interaction with host cells&#44; the bacterial microbiome&#44; and the immune system&#46; The increase in people facing predisposing conditions such as cancer chemotherapy&#44; organ transplants&#44; or HIV infections is becoming a greater risk for developing yeast infections&#46; These infections could be managed more effectively if more rapid and specific diagnostic and therapeutic alternatives were available as well as the development of new therapeutic alternatives for the timely identification of fungal species and species with multi-drug resistance in patients undergoing long-term therapies&#46; Therefore&#44; understanding how the interactions of virulence factors&#44; the microbiome&#44; and the host response contribute to a <span class="elsevierStyleItalic">Candida</span> infection is of clinical relevance&#46; There is also a need for laboratories to perform routine in vitro susceptibility testing in isolates from immunocompromised patients&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Conflict of interests</span><p id="par0230" class="elsevierStylePara elsevierViewall">The authors declare no conflict of interest&#46;</p></span></span>"
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2022.08.003

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