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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Oral. Health</journal-id>
<journal-title>Frontiers in Oral Health</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Oral. Health</abbrev-journal-title>
<issn pub-type="epub">2673-4842</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/froh.2024.1360340</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Oral Health</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Fungal footprints in oral cancer: unveiling the oral mycobiome</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author"><name><surname>Monteiro</surname><given-names>Jessica Sonal</given-names></name>
<xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:href="https://loop.frontiersin.org/people/2612327/overview"/><role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
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<contrib contrib-type="author"><name><surname>Kaushik</surname><given-names>Kriti</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
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<contrib contrib-type="author"><name><surname>de Arruda</surname><given-names>Jos&#x00E9; Alcides Almeida</given-names></name>
<xref ref-type="aff" rid="aff3"><sup>3</sup></xref><uri xlink:href="https://loop.frontiersin.org/people/1550643/overview" /><role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/></contrib>
<contrib contrib-type="author"><name><surname>Georgakopoulou</surname><given-names>Eleni</given-names></name>
<xref ref-type="aff" rid="aff4"><sup>4</sup></xref>
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<contrib contrib-type="author"><name><surname>Vieira</surname><given-names>Angelica Thomaz</given-names></name>
<xref ref-type="aff" rid="aff5"><sup>5</sup></xref><uri xlink:href="https://loop.frontiersin.org/people/110931/overview" /><role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/></contrib>
<contrib contrib-type="author"><name><surname>Silva</surname><given-names>Tarcilia A.</given-names></name>
<xref ref-type="aff" rid="aff6"><sup>6</sup></xref><uri xlink:href="https://loop.frontiersin.org/people/903395/overview" /><role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/></contrib>
<contrib contrib-type="author"><name><surname>Devadiga</surname><given-names>Darshana</given-names></name>
<xref ref-type="aff" rid="aff7"><sup>7</sup></xref>
<role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/></contrib>
<contrib contrib-type="author"><name><surname>Anyanechi</surname><given-names>Charles E.</given-names></name>
<xref ref-type="aff" rid="aff8"><sup>8</sup></xref><uri xlink:href="https://loop.frontiersin.org/people/2641614/overview" /><role content-type="https://credit.niso.org/contributor-roles/writing-review-editing/"/></contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Shetty</surname><given-names>Sameep</given-names></name>
<xref ref-type="aff" rid="aff2"><sup>2</sup></xref>
<xref ref-type="corresp" rid="cor1">&#x002A;</xref><uri xlink:href="https://loop.frontiersin.org/people/947825/overview" />
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<aff id="aff1"><label><sup>1</sup></label><institution>Department of Oral and Maxillofacial Surgery, Manipal College of Dental Sciences Mangalore, Manipal Academy of Higher Education</institution>, <addr-line>Manipal</addr-line>, <country>India</country></aff>
<aff id="aff2"><label><sup>2</sup></label><institution>Department of Oral and Maxillofacial Surgery, Manipal College of Dental Sciences</institution>, <addr-line>Mangalore</addr-line>, <country>India</country></aff>
<aff id="aff3"><label><sup>3</sup></label><institution>Department of Oral Diagnosis and Pathology, School of Dentistry, Universidade Federal do Rio de Janeiro</institution>, <addr-line>Rio de Janeiro</addr-line>, <country>Brazil</country></aff>
<aff id="aff4"><label><sup>4</sup></label><institution>Laboratory of Histology-Embryology, Molecular Carcinogenesis Group, Medical School, National and Kapodistrian University of Athens</institution>, <addr-line>Athens</addr-line>, <country>Greece</country></aff>
<aff id="aff5"><label><sup>5</sup></label><institution>Laboratory of Microbiota and Immunomodulation, Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais</institution>, <addr-line>Belo Horizonte</addr-line>, <country>Brazil</country></aff>
<aff id="aff6"><label><sup>6</sup></label><institution>Department of Oral Surgery, Pathology and Clinical Dentistry, School of Dentistry, Universidade Federal de Minas Gerais</institution>, <addr-line>Belo Horizonte</addr-line>, <country>Brazil</country></aff>
<aff id="aff7"><label><sup>7</sup></label><institution>Department of Conservative Dentistry and Endodontics, AB Shetty Memorial Institute of Dental Sciences, NITTE (Deemed to be University)</institution>, <addr-line>Mangalore</addr-line>, <country>India</country></aff>
<aff id="aff8"><label><sup>8</sup></label><institution>Department of Oral and Maxillofacial Surgery, University of Calabar/University of Calabar Teaching Hospital</institution>, <addr-line>Calabar</addr-line>, <country>Nigeria</country></aff>
<author-notes>
<fn fn-type="edited-by"><p><bold>Edited by:</bold> Ronell Bologna-Molina, Universidad de la Rep&#x00FA;blica, Uruguay</p></fn>
<fn fn-type="edited-by"><p><bold>Reviewed by:</bold> Divyashri Baraniya, Temple University, United States</p>
<p>Xiang Wang, Nanjing University, China</p></fn>
<corresp id="cor1"><label>&#x002A;</label><bold>Correspondence:</bold> Sameep Shetty <email>sameep.shetty@manipal.edu</email></corresp>
</author-notes>
<pub-date pub-type="epub"><day>14</day><month>03</month><year>2024</year></pub-date>
<pub-date pub-type="collection"><year>2024</year></pub-date>
<volume>5</volume><elocation-id>1360340</elocation-id>
<history>
<date date-type="received"><day>22</day><month>12</month><year>2023</year></date>
<date date-type="accepted"><day>14</day><month>02</month><year>2024</year></date>
</history>
<permissions>
<copyright-statement>&#x00A9; 2024 Monteiro, Kaushik, de Arruda, Georgakopoulou, Vieira, Silva, Devadiga, Anyanechi and Shetty.</copyright-statement>
<copyright-year>2024</copyright-year><copyright-holder>Monteiro, Kaushik, de Arruda, Georgakopoulou, Vieira, Silva, Devadiga, Anyanechi and Shetty</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License (CC BY)</ext-link>. The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p></license>
</permissions>
<abstract>
<p>Oral squamous cell carcinoma (OSCC) is the most common type of head and neck cancer, with a high mortality rate. There is growing evidence supporting a link between oral cancer and the microbiome. The microbiome can impact various aspects of cancer, such as pathogenesis, diagnosis, treatment, and prognosis. While there is existing information on bacteria and its connection to oral cancer, the fungi residing in the oral cavity represent a significant component of the microbiome that remains in its early stages of exploration and understanding. Fungi comprise a minuscule part of the human microbiome called the mycobiome. Mycobiome is ubiquitous in the human body but a weakened immune system offers a leeway space for fungi to showcase its virulence. The role of mycobiome as a colonizer, facilitator, or driver of carcinogenesis is still ambiguous. Reactivating the mycobiome that undergoes collateral damage associated with cancer treatment can be watershed event in cancer research. The coordinated, virulent, non-virulent behavior of the fungi once they reach a critical density must be hacked, considering its diagnostic, prognostic and therapeutic implications in cancer. This review highlights the diversity of the mycobiome and its potential role in oral cancer.</p>
</abstract>
<kwd-group>
<kwd>fungi</kwd>
<kwd>microbiota</kwd>
<kwd>mycobiome</kwd>
<kwd>oral cancer</kwd>
<kwd>oral mucosa</kwd>
<kwd>oral oncology</kwd>
</kwd-group><counts>
<fig-count count="4"/>
<table-count count="2"/><equation-count count="0"/><ref-count count="113"/><page-count count="0"/><word-count count="0"/></counts><custom-meta-wrap><custom-meta><meta-name>section-at-acceptance</meta-name><meta-value>Oral Cancers</meta-value></custom-meta></custom-meta-wrap>
</article-meta>
</front>
<body><sec id="s1" sec-type="intro"><label>1</label><title>Introduction</title>
<p>Oral squamous cell carcinoma (OSCC) is a well-recognized malignant neoplasm, responsible for more than 90&#x0025; of malignancies of the head and neck region (<xref ref-type="bibr" rid="B1">1</xref>). The main factors that contribute to the development of OSCC are alcohol and tobacco (<xref ref-type="bibr" rid="B2">2</xref>). Oral potentially malignant disorders (OPMD) are a group of heterogeneous lesions associated with the risk of transformation into OSCC (<xref ref-type="bibr" rid="B3">3</xref>). Malignant transformation across all OPMD groups is about 8&#x0025; and it is generally related to genetic, geographic, and lifestyle factors (<xref ref-type="bibr" rid="B4">4</xref>).</p>
<p>Several studies using animal models have indicated a potential causal relationship between the microbiome and the development of cancer. These findings have demonstrated that the microbiome can influence cancer progression through a variety of processes, which include the production of chemical metabolites implicated in carcinogenesis, inducing DNA damage, and regulating inflammation (<xref ref-type="bibr" rid="B5">5</xref>). The oral cavity contains approximately 700 different species of bacteria and nurtures a diverse community of bacteria, fungi, viruses, and protozoa (<xref ref-type="bibr" rid="B6">6</xref>). These microorganisms have a beneficial and harmonious relationship, working together to prevent the entry and attachment of harmful pathogens in the oral cavity. Dysbiosis, an imbalance in the microbial community, disrupts the control of pathogenic microorganisms and leads to an abnormal inflammatory or immune response against commensals. Dysbiosis has been proposed as a significant factor in the development of cancer, contributing to tissue changes associated with the disease. It has also been identified as a potential &#x201C;hallmark of cancer&#x201D; (<xref ref-type="bibr" rid="B5">5</xref>, <xref ref-type="bibr" rid="B7">7</xref>).</p>
<p>When one microbial community is knocked out of the body (bacteria), another (fungi) takes a lead, can flourish and cause illness. If the communities are undisturbed, the fungal inhabitants appear to be harmless or perhaps even beneficial. Tumors are areas where the immune system has no access, thus fungi can naturally grow and flourish expanding its territory.</p>
<p>In the present article, we provide a comprehensive overview of the relationship between the oral mycobiome and oral cancer. The prevailing evidence on the involvement of fungi in oral cancer and their impending ability to facilitate, initiate, or promote the disease through different mechanisms is discussed.</p>
</sec>
<sec id="s2"><label>2</label><title>OPMD and oral cancer: epidemiology and risk factors</title>
<p>OPMD, such as leukoplakia and erythroplakia, have a risk of progressing to OSCC. They may present a variety of characteristics, such as a change in the color of the mucosa (i.e., white, red, or a mixture of white and red), change in size, change in morphology (i.e., smooth, corrugated, granular, verrucous, atrophic, and/or plaque) (<xref ref-type="bibr" rid="B3">3</xref>). Epithelial dysplasia in OPMD may be contingent upon architectural changes, exhibiting minimal or no cytological abnormalities. Moreover, while definitive features may be elusive, the amalgamation of molecular, clinical, and microscopic characteristics contributes to an increased risk of developing an OSCC (<xref ref-type="bibr" rid="B8">8</xref>).</p>
<p>OSCC stands as a prominent malignancy in the head and neck region, originating specifically from the lips, oral cavity, and oropharynx (<xref ref-type="bibr" rid="B9">9</xref>). The worldwide prevalence of OSCC has been escalating, notably in regions such as Southeast and South Asia, Western and Eastern Europe, the Pacific, the Caribbean, and Latin America (<xref ref-type="bibr" rid="B10">10</xref>, <xref ref-type="bibr" rid="B11">11</xref>). Oral and oropharyngeal cancer pose a significant global health challenge, with an annual incidence of 476,000 cases and an unfortunate mortality rate of approximately half of those affected (<xref ref-type="bibr" rid="B12">12</xref>). In 2023, it was projected that there would be 54,540 new cases of oral and oropharyngeal cancer in the United States (<xref ref-type="bibr" rid="B13">13</xref>). According to GLOBOCAN 2020, India holds the third position worldwide in terms of cancer incidence, and projections indicate a substantial increase to 2.08 million cases by 2040, representing a 57&#x0025; rise from 2020 (<xref ref-type="bibr" rid="B12">12</xref>). In India, the oral cavity and pharynx are potential sites for cancer, accounting for a burden of 198,438 cases (<xref ref-type="bibr" rid="B14">14</xref>).</p>
<p>Alcohol and tobacco are some of the risk factors for OSCC (<xref ref-type="bibr" rid="B9">9</xref>). Tobacco impairs oral immunity, favoring gingivitis/periodontitis and oral cancer (<xref ref-type="bibr" rid="B15">15</xref>). <italic>Porphyromonas gingivalis</italic> and <italic>Fusobacterium nucleatum</italic> are widely studied bacteria known for their association with the onset of gingivitis and periodontitis. Additionally, these bacteria have been identified as contributors to carcinogenesis in mice (<xref ref-type="bibr" rid="B16">16</xref>). Furthermore, <italic>P. gingivalis</italic> has been suggested to be involved in oral-digestive cancer (<xref ref-type="bibr" rid="B17">17</xref>). Alcohol, specifically ethanol, serves as both a local and systemic risk factor, increasing the permeability of the oral mucosa, causing the dissolution of epithelial lipids, inducing epithelial atrophy, and disrupting DNA synthesis and repair. Chronic alcohol use exerts genotoxic and mutagenic effects, along with a potential decrease in both innate and acquired immunity (<xref ref-type="bibr" rid="B18">18</xref>). Human papillomavirus (HPV) and ultraviolet (UV) exposure represent additional risk factors for oral cancer (<xref ref-type="bibr" rid="B19">19</xref>, <xref ref-type="bibr" rid="B20">20</xref>), accounting for 2&#x0025;&#x2013;8&#x0025; of OSCC (<xref ref-type="bibr" rid="B21">21</xref>).</p>
</sec>
<sec id="s3"><label>3</label><title>Relationship of oral and systemic fungi with oral cancer</title>
<sec id="s3a"><label>3.1</label><title>Occurrence of fungi in the oral cavity in states of health and disease</title>
<p>The term &#x201C;fungi&#x201D; encompasses a diverse array of eukaryotic microbes that collectively constitute the human microbiota, referred to as &#x201C;mycobiota&#x201D;, coexisting harmoniously in virtually any anatomical location (<xref ref-type="bibr" rid="B22">22</xref>). Within the oral cavity, more than 75 genera, such as <italic>Candida</italic>, <italic>Cladosporium</italic>, <italic>Aureobasidium</italic>, and <italic>Aspergillus</italic>, contribute to this fungal community (<xref ref-type="bibr" rid="B23">23</xref>). Recent metagenomics studies have unveiled previously unidentified fungal species. Ghannoum et al. (<xref ref-type="bibr" rid="B23">23</xref>), in their molecular profiling study, identified a total of 85 species in the oral cavities of 20 healthy individuals, encompassing 11 non-culturable and 74 culturable fungi. Another study identified the cultivation of 101 different genera of fungi, with the number of species per individual ranging from nine to 23. Furthermore, using sequencing techniques, <italic>Malassezia</italic> sp. was identified as an additional pathogenic species commonly inhabiting the oral cavity (<xref ref-type="bibr" rid="B24">24</xref>). Similarly, a systematic review has documented the presence of <italic>Candida</italic> spp. and <italic>Malassezia</italic> spp. on mucous membranes, further emphasizing the diverse fungal composition within the oral environment (<xref ref-type="bibr" rid="B25">25</xref>).</p>
<p>The oral mycobiota exhibits remarkable diversity, primarily composed of organisms affiliated with the phylum <italic>Ascomycota</italic>, with <italic>Candida</italic> species standing out as a particularly prominent group. Culture-independent methods have unveiled an expanded spectrum that encompasses numerous general within the <italic>Saccharomycetaceae</italic> family. Notable members of this diverse group include, but not limited to, <italic>C</italic>. <italic>albicans</italic>, <italic>Fusarium</italic> species, <italic>Pichia</italic> species, <italic>C</italic>. <italic>dubliniensis</italic>, <italic>Saccharomyces cerevisiae</italic>, <italic>C</italic>. <italic>rugose</italic>, and <italic>Hanseniaspora uvarum</italic>. Collectively, these species represent the majority of fungi populating the oral cavity (<xref ref-type="bibr" rid="B26">26</xref>) (<xref ref-type="table" rid="T1">Table&#x00A0;1</xref>).</p>
<table-wrap id="T1" position="float"><label>Table 1</label>
<caption><p>Prevalence of oral mycobiome in healthy individuals.</p></caption>
<table frame="hsides" rules="groups">
<colgroup>
<col align="left"/>
<col align="left"/>
</colgroup>
<thead>
<tr>
<th valign="top" align="left">Study</th>
<th valign="top" align="center">Most prevalent fungi</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Urz&#x00FA;a et al. (<xref ref-type="bibr" rid="B27">27</xref>)</td>
<td valign="top" align="left"><italic>Candida albicans</italic><break/><italic>Saccharomyces cerevisiae</italic><break/><italic>Candida dubliniensis</italic><break/><italic>Candida guillermondii</italic><break/><italic>Kluyveromyces lactis</italic></td>
</tr>
<tr>
<td valign="top" align="left">Ghannoum et al. (<xref ref-type="bibr" rid="B23">23</xref>)</td>
<td valign="top" align="left"><italic>Candida</italic><break/><italic>Cladosporium</italic><break/><italic>Aureobasidium</italic><break/><italic>Saccharomycetales</italic><break/><italic>Aspergillus</italic></td>
</tr>
<tr>
<td valign="top" align="left">Dupuy et al. (<xref ref-type="bibr" rid="B24">24</xref>)</td>
<td valign="top" align="left"><italic>Malassezia</italic><break/><italic>Aspergilllus</italic><break/><italic>Candida</italic><break/><italic>Pichia</italic><break/><italic>Cladosporium</italic></td>
</tr>
<tr>
<td valign="top" align="left">Monteiro-da-Silva et al. (<xref ref-type="bibr" rid="B28">28</xref>)</td>
<td valign="top" align="left"><italic>Candida</italic><break/><italic>Rhodotorula</italic><break/><italic>Penicillium</italic><break/><italic>Aspergillus</italic><break/><italic>Cladosporium</italic></td>
</tr>
<tr>
<td valign="top" align="left">Peters et al. (<xref ref-type="bibr" rid="B29">29</xref>)</td>
<td valign="top" align="left"><italic>Candida</italic><break/><italic>Aspergillus</italic><break/><italic>Pencillium</italic><break/><italic>Schizophyllum</italic><break/><italic>Rhodortorula</italic></td>
</tr>
<tr>
<td valign="top" align="left">Baraniya et al. (<xref ref-type="bibr" rid="B30">30</xref>)</td>
<td valign="top" align="left"><italic>Malassezia</italic><break/><italic>Candida</italic><break/><italic>Cryptococcus</italic><break/><italic>Saccharomyces</italic><break/><italic>Trichoderma</italic></td>
</tr>
<tr>
<td valign="top" align="left">Khadija et al. (<xref ref-type="bibr" rid="B31">31</xref>)</td>
<td valign="top" align="left"><italic>Candida</italic><break/><italic>Kluyveromyces</italic><break/><italic>Nakaseomyces</italic><break/><italic>Alternaria</italic><break/><italic>Aspergillus</italic></td>
</tr>
</tbody>
</table>
</table-wrap>
<p>Fungi exhibit the characteristic ability to enhance cell density and promote the growth of hyphae, forming the structural framework for multispecies biofilms. Moreover, fungi stand out among eukaryotes due to their potent impact on the host immune system, exerting diverse immunological effects (<xref ref-type="bibr" rid="B32">32</xref>). Interactions between fungi and the host underscore the presence of a robust host immune mechanism (<xref ref-type="bibr" rid="B22">22</xref>, <xref ref-type="bibr" rid="B32">32</xref>&#x2013;<xref ref-type="bibr" rid="B34">34</xref>). In the realm of microbial ecology, fungi have been proposed as &#x201C;keystone species&#x201D;, playing a pivotal role in influencing the overall microbiota (<xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B36">36</xref>).</p>
<p><italic>Candida</italic> is known for its cross-kingdom relationships, its near-ubiquitous nature, and ease of cultivation (<xref ref-type="bibr" rid="B35">35</xref>, <xref ref-type="bibr" rid="B36">36</xref>). Observations indicate that <italic>C. albicans</italic> is frequently detected species among individuals with OPMD and OSCC (<xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B38">38</xref>). In a recent study assessing 100 patients with OSCC using biochemical methods, <italic>Candida</italic> species were identified in 74&#x0025; of the samples, with <italic>C. albicans</italic> being the predominant species in 84&#x0025; (<xref ref-type="bibr" rid="B38">38</xref>). Similarly, another study reported elevated levels of <italic>C. albicans</italic> in the saliva of individuals with head and neck squamous cell carcinoma (<xref ref-type="bibr" rid="B39">39</xref>). A study using molecular profiling techniques investigated the co-occurrence network of <italic>C. albicans</italic> in the oral rinse of cancer patients (<xref ref-type="bibr" rid="B40">40</xref>). The findings revealed variations in the prevalence of certain subtypes of <italic>C. albicans</italic>, with some exhibiting higher prevalence and others lower (<xref ref-type="bibr" rid="B40">40</xref>). In contrast, oral rinse samples from individuals without cancer showed a higher prevalence of <italic>C. dubliniensis</italic>, <italic>Schizophyllum commune</italic>, and organisms belonging to the <italic>Agaricomycetes</italic> class (<xref ref-type="bibr" rid="B40">40</xref>) (<xref ref-type="table" rid="T2">Table&#x00A0;2</xref>).</p>
<table-wrap id="T2" position="float"><label>Table 2</label>
<caption><p>Prevalence of oral mycobiome in oral cancer.</p></caption>
<table frame="hsides" rules="groups">
<colgroup>
<col align="left"/>
<col align="left"/>
</colgroup>
<thead>
<tr>
<th valign="top" align="left">Study</th>
<th valign="top" align="center">Most prevalent fungi</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left">Ayuningtyas et al. (<xref ref-type="bibr" rid="B41">41</xref>)</td>
<td valign="top" align="left"><italic>Candida albicans</italic></td>
</tr>
<tr>
<td valign="top" align="left">Theofilou et al. (<xref ref-type="bibr" rid="B42">42</xref>)</td>
<td valign="top" align="left"><italic>Candida spp</italic></td>
</tr>
<tr>
<td valign="top" align="left">&#x0130;lhan B et al. (<xref ref-type="bibr" rid="B43">43</xref>)</td>
<td valign="top" align="left"><italic>Candida albicans</italic><break/><italic>Candida glabarata</italic><break/><italic>Candida kruseii</italic><break/><italic>Candida tropicalis</italic><break/><italic>Candida parapsilosis</italic></td>
</tr>
<tr>
<td valign="top" align="left">Murugan et al. (<xref ref-type="bibr" rid="B44">44</xref>)</td>
<td valign="top" align="left"><italic>Candida spp</italic></td>
</tr>
<tr>
<td valign="top" align="left">Fan et al. (<xref ref-type="bibr" rid="B45">45</xref>)</td>
<td valign="top" align="left"><italic>Candida</italic><break/><italic>Aspergillus</italic><break/><italic>Alternaria</italic><break/><italic>Cryptococcus</italic></td>
</tr>
<tr>
<td valign="top" align="left">Tasso et al. (<xref ref-type="bibr" rid="B46">46</xref>)</td>
<td valign="top" align="left"><italic>Candida albicans</italic><break/><italic>C. dubliniensis</italic><break/><italic>C. tropicalis</italic><break/><italic>C. glabrata</italic><break/><italic>C. parapsilosis</italic></td>
</tr>
<tr>
<td valign="top" align="left">Talapko et al. (<xref ref-type="bibr" rid="B47">47</xref>)</td>
<td valign="top" align="left"><italic>Candida albicans</italic></td>
</tr>
<tr>
<td valign="top" align="left">Wang et al. (<xref ref-type="bibr" rid="B48">48</xref>)</td>
<td valign="top" align="left"><italic>Candida albicans</italic></td>
</tr>
<tr>
<td valign="top" align="left">Wang et al. (<xref ref-type="bibr" rid="B49">49</xref>)</td>
<td valign="top" align="left"><italic>Candida albicans</italic></td>
</tr>
<tr>
<td valign="top" align="left">He et al. (<xref ref-type="bibr" rid="B50">50</xref>)</td>
<td valign="top" align="left"><italic>Verruconis gallopava</italic><break/><italic>Syncephalastrum racemosum</italic><break/><italic>Dimargaris cristalligena</italic><break/><italic>Lichteimia corymbifera</italic><break/><italic>Malassezia sympodialis</italic></td>
</tr>
<tr>
<td valign="top" align="left">Wang et al. (<xref ref-type="bibr" rid="B51">51</xref>)</td>
<td valign="top" align="left"><italic>Candida albicans</italic></td>
</tr>
</tbody>
</table>
</table-wrap>
<p>The progression of OSCC is marked by a significant increase in the presence of <italic>Acremonium</italic> and <italic>Aspergillus</italic>, both known for their detrimental health effects (<xref ref-type="bibr" rid="B52">52</xref>, <xref ref-type="bibr" rid="B53">53</xref>). Conversely, <italic>Morchella</italic>, recognized for its potent inhibitory activity against harmful bacteria, experiences a noteworthy reduction in reduction in individuals with premalignant and malignant conditions. The polysaccharide FMP-1 derived from <italic>Morchella esculenta</italic> is attributed with prebiotic benefits and potential anti-tumor activity owing to its antioxidant capabilities (<xref ref-type="bibr" rid="B54">54</xref>, <xref ref-type="bibr" rid="B55">55</xref>). The decline in <italic>Morchella</italic> levels suggests the potential emergence of invasive oral niches, heightening the risk of oral disorders. These findings offer a compelling perspective on the prevention and treatment of OSCC, underscoring the crucial roles played by distinct fungal species, including <italic>Aspergillus fumigatus</italic>, <italic>C</italic>. <italic>tropicalis</italic>, and <italic>Acremonium exuviarum</italic>, all labelled as &#x201C;oncogenic fungi&#x201D; (<xref ref-type="bibr" rid="B56">56</xref>). The mitochondrial toxicity of acrebol produced by <italic>Acremonium exuviarum</italic> (<xref ref-type="bibr" rid="B57">57</xref>), the ability of <italic>A. fumigatus</italic> to generate reactive oxygen species linked to oral cancer (<xref ref-type="bibr" rid="B58">58</xref>, <xref ref-type="bibr" rid="B59">59</xref>), and the collaborative biofilm formation of <italic>C. tropicalis</italic> with bacteria such as <italic>Escherichia coli</italic> and <italic>Serratia marcescens</italic> (<xref ref-type="bibr" rid="B60">60</xref>) exemplify the significant health consequences demonstrated by these fungi.</p>
<p>According to Banerjee et al. (<xref ref-type="bibr" rid="B61">61</xref>), <italic>Rhodotorula</italic>, <italic>Geotrichum</italic>, and <italic>Pneumocystis</italic> were exclusively found in specimens collected from cancer patients, while <italic>Fonsecaea</italic> was absent in oral tissues from healthy participants. Intriguingly, <italic>Fonsecaea</italic> was present in cancer samples and tissues adjacent to malignancy from the same patients. Another study revealed that the only fungal species in tumor samples experiencing a significant decrease in matching non-tumor tissues was <italic>Glomeromycota</italic>. Notably, high T-stage tumor samples exhibited a higher fungal population compared to low T-stage samples (<xref ref-type="bibr" rid="B62">62</xref>). An important observation from the study by Perera et al. (<xref ref-type="bibr" rid="B63">63</xref>) is the overgrowth of <italic>C. albicans</italic> in OSCC tissue.</p>
</sec>
<sec id="s3b"><label>3.2</label><title>Role of fungi as drivers in oral cancer</title>
<p>It is well documented that candidiasis triggers type 3 responses initiated by activated IL-17-secreting cells These responses have been linked to tumor-promoting infiltrates of inflammatory cells and pose an antagonistic action to interferon-gamma (IFN-&#x03B3;), a recognized anti-cancer defense mechanism (<xref ref-type="bibr" rid="B64">64</xref>). Conversely, candidalysin, a toxic epithelium-damaging substance produced by <italic>Candida</italic>, has been postulated to enhance tumor-promoting immunity (<xref ref-type="bibr" rid="B65">65</xref>&#x2013;<xref ref-type="bibr" rid="B67">67</xref>). Despite this, the direct link between candidalysin and oral carcinogenesis remains unestablished. This recently identified <italic>Candida</italic> virulence factor has been demonstrated to activate additional oncogenic pathways within epithelial elements, involving the epidermal growth factor receptor/mitogen-activated protein kinase axis (<xref ref-type="bibr" rid="B42">42</xref>, <xref ref-type="bibr" rid="B68">68</xref>, <xref ref-type="bibr" rid="B69">69</xref>).</p>
<p>In a study on pancreatic cancer, the mannose-binding lectin, which binds specifically to the glycans on the fungal wall, was activated mainly by the <italic>Malassezia</italic> genus, showing potential for tumor formation (<xref ref-type="bibr" rid="B70">70</xref>). On the other hand, the presence of <italic>Malassezia</italic> sp. in OSCC is associated with a favorable prognosis (<xref ref-type="bibr" rid="B71">71</xref>).</p>
<p>While the oral mycobiome has demonstrated carcinogenic implications, substantial proof is currently lacking to establish whether these findings can be replicated for oral epithelial dysplasia. An alternative explanation posits that while these occurrences do exist in oral cancer growth, the associated changes may be insufficient to solely induce dysplastic alterations in oral epithelial tissue, serving more as accelerators rather that primary causes (<xref ref-type="bibr" rid="B72">72</xref>).</p>
<p>To mimic experimental oral carcinogenesis development, 4-nitrioquinolone-1-oxide (4NQO) has been used. This compound induces mutagenic changes in DNA similar to those triggered by tobacco (<xref ref-type="bibr" rid="B73">73</xref>). Live <italic>C. albicans</italic> has been found to enhance the migration potential, induce matrix metalloproteinase, and release associated metabolites via epithelial-mesenchymal shift, along with the upregulation of metastasis-associated genes (<xref ref-type="bibr" rid="B74">74</xref>). The same study explored the capacity of <italic>Candida</italic> to facilitate sequential cancer in 4NQO mice (<xref ref-type="bibr" rid="B74">74</xref>). These pre-neoplastic growths are supported by dysbiosis in the oral mycobiota, allowing them to progress into cancer (<xref ref-type="bibr" rid="B75">75</xref>). Antifungal therapy alone proves inadequate in treating the affected area and addressing this complex process; hence, the lesion should be treated as an OPMD (<xref ref-type="bibr" rid="B76">76</xref>).</p>
<p>Data from an exploratory study indicated that OSCC patients with <italic>Candida</italic> may experience lesser overall survival, serving as indirect proof for the potential tumor-promoting actions of mycobiome dysbiosis (<xref ref-type="bibr" rid="B71">71</xref>). In a recent metaproteomic analysis, a total of 196 fungal proteins demonstrated significant changes in abundance across different forms of OSCC. Most of the detected fungi had not been thoroughly investigated, and researchers were unaware of their toxicity or lethal associations in the oral cavity of humans (<xref ref-type="bibr" rid="B50">50</xref>). However, other fungi, including <italic>Verruconis gallopava</italic> (<xref ref-type="bibr" rid="B77">77</xref>), <italic>Dimargaris cristalligena</italic> (<xref ref-type="bibr" rid="B78">78</xref>, <xref ref-type="bibr" rid="B79">79</xref>), and <italic>Syncephalastrum racemosum</italic> (<xref ref-type="bibr" rid="B80">80</xref>), were found to be more frequently present in OSCC lesions and linked to opportunistic infections.</p>
<p>Additionally, other well-known fungi species such as <italic>Paracoccidioides brasiliensis</italic>, <italic>Malassezia sympodialis</italic>, and <italic>Lichteimia corymbifera</italic> were detected. In an investigation comparing tissue from tumors with non-tumor controls, <italic>L. corymbifera</italic> showed an association with OSCC of the tongue (<xref ref-type="bibr" rid="B81">81</xref>). <italic>P. brasiliensis</italic>, a fungal yeast causing paracoccidioidomycosis leading to oral manifestations, has been associated with OSCC (<xref ref-type="bibr" rid="B82">82</xref>). Coexistence of oral paracoccidioidomycosis and OSCC has been reported (<xref ref-type="bibr" rid="B83">83</xref>), suggesting a potential role of fungi in cancer development, possibly due to continuous stimulation of epithelial cells increasing susceptibility to malignant transformation (<xref ref-type="bibr" rid="B84">84</xref>). Nonetheless, this association is not confirmed due to the limited number of experimental and clinical studies investigating this effect.</p>
</sec>
</sec>
<sec id="s4"><label>4</label><title>Cross-realm alliance: fungi and other microbes</title>
<p>The ability of <italic>C. albicans</italic> to form alliances with <italic>F. nucleatum</italic>, circumventing host defenses (<xref ref-type="bibr" rid="B85">85</xref>), and its interaction with <italic>Streptococcus mutans</italic> (<xref ref-type="bibr" rid="B86">86</xref>, <xref ref-type="bibr" rid="B87">87</xref>), or <italic>S. oralis</italic> (<xref ref-type="bibr" rid="B88">88</xref>, <xref ref-type="bibr" rid="B89">89</xref>) to exacerbate oral candidiasis or dental caries, respectively, underscores the importance of inter-kingdom associations in the development of polymicrobial conditions widely recognized today (<xref ref-type="bibr" rid="B72">72</xref>). Some authors propose that, as new research methods advance, the relationship between <italic>C. albicans</italic> and bacteria may emerge as a model for understanding fungal-bacterial interactions in the oral cavity (<xref ref-type="bibr" rid="B72">72</xref>) (<xref ref-type="fig" rid="F1">Figure&#x00A0;1</xref>).</p>
<fig id="F1" position="float"><label>Figure 1</label>
<caption><p>Model of fungal-bacteria relationship. (<bold>A</bold>) In contrast to when each species is grown independently, <italic>Streptococcus oralis</italic> and <italic>Candida albicans</italic> grow to a greater number when the two are combined in a biofilm. (<bold>B</bold>) The growth of glucan is one of the factors contributing to the virulence of <italic>S. mutans</italic> that is facilitated by the inclusion of <italic>C. albicans. C. albicans</italic> and <italic>S. mutans</italic> progress more densely than when cultured alone. (<bold>C</bold>) Growing <italic>C. albicans</italic> in combination with <italic>Fusobacterium nucleatum</italic> considerably reduces its capacity to produce hyphae.</p></caption>
<graphic xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="froh-05-1360340-g001.tif"/>
</fig>
<p>Soluble factors released by biofilms of <italic>C. albicans</italic> and <italic>S. aureus</italic> have been shown to induce variations in the expression of cell cycle genes and proto-oncogenes in both malignant and normal oral epithelial cell lines. This reveals how biofilm metabolites can influence gene expression and tumor cell survival based on cell-specific characteristics (<xref ref-type="bibr" rid="B90">90</xref>). In a study by Bertolini et al. (<xref ref-type="bibr" rid="B91">91</xref>) using animal models to target <italic>Enterococcus faecalis</italic> with antibiotics, the post-chemotherapy pathological effects of <italic>C. albicans</italic> infection on oral microorganisms were examined, uncovering the role of bacterial community changes in influencing the virulence of <italic>C. albicans</italic> in oropharyngeal candidiasis. Interactions among polymicrobial communities, particularly biofilm formation involving <italic>C. albicans</italic>, <italic>Actinomyces naeslundii</italic>, and <italic>S. mutans</italic>, were found to significantly enhance the adhesion of OSCC cells to extracellular matrix (ECM) and elevate the release of pro-inflammatory cytokines (<xref ref-type="bibr" rid="B92">92</xref>).</p>
</sec>
<sec id="s5"><label>5</label><title>Role of the mycobiota in oral cancer</title>
<sec id="s5a"><label>5.1</label><title>Inflammatory responses</title>
<p>Several inflammatory diseases including ulcerative colitis, inflammatory bowel disease, and pancreatitis have been linked to cancer due to the inflammatory response elicited (<xref ref-type="bibr" rid="B93">93</xref>). The robust immune response elicited by fungal infection raises the possibility of its involvement, increasing the risk of oral cancer (<xref ref-type="bibr" rid="B22">22</xref>). Pattern recognition receptors (PRR) recognize pathogen-associated molecular patterns (PAMP) composed of carbohydrates in the fungal cell wall during fungal invasion, which initiates signaling cascades across multiple pathways such as <italic>MYD88</italic> (myeloid differentiation primary response gene 88), <italic>SYK-CARD9</italic> (spleen tyrosine kinase-caspase recruitment domain 9), and <italic>TRIF</italic> (Toll/IL-1R domain-containing adaptor-inducing interferon) pathways. Following the activation of these pathways numerous signaling molecules are secreted, such as interleukin (IL)-1, IL-6, IL-12, IL-23, transforming growth factor (TGF), and interferon (IFN). These signaling molecules regulate the antifungal response of T helper cell 1 (Th1) and T helper cell 17 (Th17) along with phagocyte stimulation and neutrophil recruitment (<xref ref-type="bibr" rid="B94">94</xref>) (<xref ref-type="fig" rid="F2">Figure&#x00A0;2</xref>).</p>
<fig id="F2" position="float"><label>Figure 2</label>
<caption><p>Mechanism by which fungi aid in cancer development. Pathogen-associated molecular patterns (PAMP), biofilm formation, and fungal metabolites such as acetaldehyde are the three major components involved in the development of cancer.</p></caption>
<graphic xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="froh-05-1360340-g002.tif"/>
</fig>
</sec>
<sec id="s5b"><label>5.2</label><title>Formation of oral biofilm</title>
<p>Microbial biofilms are significant in a wide range of medical disorders (<xref ref-type="bibr" rid="B95">95</xref>&#x2013;<xref ref-type="bibr" rid="B97">97</xref>). Existing research indicates that bacterial and fungal biofilms are equally significant. Few studies have highlighted that fungus and bacteria can work together to create biofilms that aggravate inflammation (<xref ref-type="bibr" rid="B98">98</xref>). It has been established that the disease-causing bacterial agent <italic>Fusobacterium nucleatum</italic>, which resides in the oral cavity and digestive system, plays a role in the emergence of colorectal cancer (<xref ref-type="bibr" rid="B99">99</xref>). Moreover, it has been shown that <italic>F. nucleatum</italic> and <italic>C. albicans</italic> co-aggregate by interacting between genetic and morphological cellular elements (<xref ref-type="bibr" rid="B100">100</xref>).</p>
<p>Mukherjee et al. (<xref ref-type="bibr" rid="B62">62</xref>) performed inter-kingdom analysis for fungi and bacteria in 39 samples which included oral tongue cancer and non-tumor samples. <italic>Lichtheimia</italic>, a fungal species, has demonstrated a constructive relationship with bacterial species such as <italic>Campylobacter</italic>, <italic>Porphyromonas</italic>, and <italic>Fusobacterium</italic>. Earlier studies have highlighted the role of gut bacteria, especially <italic>F. nucleatum</italic>, in the development of colorectal cancer (<xref ref-type="bibr" rid="B101">101</xref>). This type of cancer exhibits molecular gene silencing through CpG island methylation that has been associated with <italic>F. nucleatum</italic> (<xref ref-type="bibr" rid="B102">102</xref>).</p>
</sec>
<sec id="s5c"><label>5.3</label><title>Metabolites of fungus origin</title>
<p>Few studies have shown that the alcohol dehydrogenase enzyme found in different <italic>Candida</italic> species enables them to produce acetaldehyde (<xref ref-type="bibr" rid="B103">103</xref>&#x2013;<xref ref-type="bibr" rid="B105">105</xref>) that is highly toxic, mutagenic, and carcinogenic (<xref ref-type="bibr" rid="B106">106</xref>). For example, Asian subjects lacking aldehyde dehydrogenase-2, an enzyme that aids in the body&#x0027;s elimination of the compound by oxidizing it to acetate, have higher salivary acetaldehyde levels and a 10-fold greater chance of oral cancer (<xref ref-type="bibr" rid="B107">107</xref>).</p>
<p>The mutagenic properties of the metabolic product of <italic>Candida</italic> alcohol dehydrogenase enzyme, i.e., acetaldehyde raise its possible implication in carcinogenesis (<xref ref-type="bibr" rid="B64">64</xref>). <italic>Candida</italic> has been demonstrated to exhibit higher metabolic rates and acetaldehyde synthesis in oral cancer compared to healthy controls (<xref ref-type="bibr" rid="B108">108</xref>). Moreover, <italic>Candida</italic> has pronounced nitrosation potential due to the production of nitrosamine compounds that have a significant role in oral carcinogenesis (<xref ref-type="bibr" rid="B75">75</xref>).</p>
<p>Mitochondrial aldehyde dehydrogenase-2 is beneficial in eliminating acetaldehyde. However, dysbiosis with an increase in <italic>Candida</italic> may cause an elevated level in its production, especially in frequent drinkers (<xref ref-type="bibr" rid="B109">109</xref>, <xref ref-type="bibr" rid="B110">110</xref>) (<xref ref-type="fig" rid="F3">Figure&#x00A0;3</xref>).</p>
<fig id="F3" position="float"><label>Figure 3</label>
<caption><p>Acetaldehyde can be involved in the oral carcinogenesis through a variety of mechanisms. In addition to altering the framework and functionality of proteins and DNA by binding, this compound also reduces glutathione&#x0027;s antioxidant activity, which raises the amounts of reactive oxygen species (ROS).</p></caption>
<graphic xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="froh-05-1360340-g003.tif"/>
</fig>
</sec>
</sec>
<sec id="s6"><label>6</label><title>Future directions</title>
<p>Cancer occurs when normal cells in the body expand, and divide exponentially. Certain immune cells are essential for tracing and destroying these tumor cells. This immune response is influenced, at least in part, by the microbiota. Immune cells have sensors that may identify specific microorganisms, triggering various reactions. A crucial component in the body&#x0027;s capacity to recognize fungi is a protein called dectin-1. It is found on the surface of some immune cells and functions as a transmembrane pattern-recognition receptor through its ability to bind &#x03B2;-glucan carbohydrates (<xref ref-type="bibr" rid="B111">111</xref>). It has been discovered to be associated with tumor growth and survival rates in both mouse and human breast tumors (<xref ref-type="bibr" rid="B112">112</xref>) and melanomas (<xref ref-type="bibr" rid="B54">54</xref>, <xref ref-type="bibr" rid="B113">113</xref>). The effectiveness of cancer treatments, particularly radiotherapy, and its impact on the immune system, gut microbiota, and the other collateral damage it induces on the body may have a causal link with an overgrowth of specific fungi (<xref ref-type="bibr" rid="B113">113</xref>). This further emphasizes the potential relevance of the combination of standard chemotherapy or radiotherapy with therapies that regulate the oral microbiota.</p>
<p>The discovery of a distinct fungal pattern that points to the involvement of fungal communities in tumor development highlights the need to attain traction and stretch the scope of microbiome research beyond bacterial communities. Earlier studies have illuminated the interplay between distinct microbial communities, implying that these joint communities contribute to dysbiosis or the preservation of a healthy microbiome (<xref ref-type="bibr" rid="B72">72</xref>). While there is a range of data on the role of <italic>Candida</italic> in oral carcinogenesis (<xref ref-type="bibr" rid="B37">37</xref>, <xref ref-type="bibr" rid="B41">41</xref>, <xref ref-type="bibr" rid="B114">114</xref>), other species such as <italic>Aspergillus</italic>, <italic>Penicillium</italic>, and <italic>Malassezzia</italic> require additional investigation (<xref ref-type="fig" rid="F4">Figure&#x00A0;4</xref>). Overall, the study of the oral mycobiome is still in its infancy, and further research aiming at exploring the potential role of fungi in tuning and modulating the host immunity is essential to open up new possibilities for the prevention and adjunctive treatment of oral cancer.</p>
<fig id="F4" position="float"><label>Figure 4</label>
<caption><p>Role of fungi, bacteria and virus in carcinogenic process. Representation of the mechanisms involved in cancer progression by microorganisms through a Venn diagram. Fungi and bacteria produce metabolites like acetaldehyde and nitrosamine, induce inflammatory response through T helper cells. Fungi and virus mimic the molecular structure similar to that of the host thereby activating the immune system. Fungi, bacteria and virus all have the common mechanism of causing inflammation, cell alteration and metastasis which ultimately contributes to the development of cancer.</p></caption>
<graphic xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="froh-05-1360340-g004.tif"/>
</fig>
</sec>
<sec id="s7"><label>7</label><title>Concluding remarks</title>
<p>The microbial communities, driven by their survival instincts within the host, employ cooperative evolutionary strategies that lead to the formation of robust biofilms. Fungi enhance their virulence through filamentation and increased secretion of aspartyl proteinases, strengthening their ability to invade the host (<xref ref-type="bibr" rid="B115">115</xref>). Conversely, bacteria develop antibacterial tolerance while residing under the protective fungal matrix umbrella. <italic>C. albicans</italic>, for instance, produces mucolytic enzymes that degrade the protective mucin layer of the epithelium, contributing to the formation of lesions, tumors, and other pathological conditions. This interkingdom cooperation significantly influences the host immune system (<xref ref-type="bibr" rid="B116">116</xref>).</p>
<p>The oral microbiome, comprising a diverse array of fungi, bacteria, and viruses living in biofilms, can pose a threat to immunocompromised oral cancer patients. While guidelines and protocols exist to control oral infections, they often rely more on clinical observations than robust evidence. Increased microbial load, especially in cancer patients, can be potentially fatal. Thus, maintaining good oral health and seeking regular treatment from oral health professionals is crucial. Although some components of the oral mycobiome can metabolize substances into carcinogens, their exact role in the development of oral cancer remains uncertain. For example, the involvement of mycobiota in alcohol metabolism can lead to the formation of acetaldehyde, a known carcinogen. The combination of poor oral hygiene, inadequate nutrition, and established risk factors such as alcohol and tobacco can amplify the risk of developing oral cancer.</p>
<p>The application of novel molecular methods is enabling the identification and understanding of the mycobiome&#x0027;s role in both healthy individuals and those immunosuppressed individuals. The inter-kingdom relationships between fungi and bacteria add another layer of complexity to this exploration. The detection of newly identified proteins closely associated with fungal overload allows for the assessment cancer treatment effectiveness and exploration of novel approaches. Thus, it is important to include the mycobiome&#x2014;the concealed realm of potential biohackers&#x2014;in research efforts. Decoding its molecular signature and evaluating its connection to oral cancer can have significant implications in prevention, diagnosis, and treatment, opening new horizons in cancer research.</p>
</sec>
</body>
<back>
<sec id="s8" sec-type="author-contributions"><title>Author contributions</title>
<p>JM: Writing &#x2013; original draft, Writing &#x2013; review &#x0026; editing. KK: Writing &#x2013; original draft, Writing &#x2013; review &#x0026; editing. JA: Writing &#x2013; original draft, Writing &#x2013; review &#x0026; editing. EG: Writing &#x2013; original draft, Writing &#x2013; review &#x0026; editing. AV: Writing &#x2013; review &#x0026; editing. TS: Writing &#x2013; review &#x0026; editing. DD: Writing &#x2013; review &#x0026; editing. CA: Writing &#x2013; review &#x0026; editing. SS: Writing &#x2013; original draft, Writing &#x2013; review &#x0026; editing.</p>
</sec>
<sec id="s9" sec-type="funding-information"><title>Funding</title>
<p>The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.</p>
</sec>
<sec id="s10" sec-type="COI-statement"><title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
<p>The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.</p>
</sec>
<sec id="s11" sec-type="disclaimer"><title>Publisher&#x0027;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
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