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HPV-Associated Benign Squamous Cell Papillomas in the Upper Aero-Digestive Tract and Their Malignant Potential

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HPV-Associated Benign Squamous Cell Papillomas in the Upper Aero-Digestive Tract and Their Malignant Potential viruses Review HPV-Associated Benign Squamous Cell Papillomas in the Upper Aero-Digestive Tract and Their Malignant Potential Stina Syrjänen 1,2,* and Kari Syrjänen 3 1 Department of Oral Pathology and Oral Radiology, Institute of Dentistry, Faculty of Medicine, University of Turku, 20520 Turku, Finland 2 Department of Pathology, Turku University Hospital, 20521 Turku, Finland 3 Department of Clinical Research, Biohit Oyj, 00880 Helsinki, Finland; kasyrja@sci.fi * Correspondence: stina.syrjanen@utu.fi Abstract: Squamous cell papilloma (SCP) in the upper aero-digestive tract is a rare disease entity with bimodal age presentation both at childhood and in adults. It originates from stratified squamous and/or respiratory epithelium. Traditionally, SCPs have been linked to chemical or mechanical irritation but, since the 1980s, they have also been associated with human papillomavirus (HPV) infection. Approximately 30% of the head and neck SCPs are associated with HPV infection, with this association being highest for laryngeal papillomas (76–94%), followed by oral (27–48%), sinonasal (25–40%), and oropharyngeal papillomas (6–7%). There is, however, a wide variation in HPV prevalence, the highest being in esophageal SCPs (11–57%). HPV6 and HPV11 are the two main HPV genotypes present, but these are also high-risk HPVs as they are infrequently detected. Some 20% of the oral and oropharyngeal papillomas also contain cutaneous HPV genotypes. Despite their Citation: Syrjänen, S.; Syrjänen, K. benign morphology, some SCPs tend to recur and even undergo malignant transformation. The HPV-Associated Benign Squamous highest malignant potential is associated with sinonasal inverted papillomas (7–11%). This review Cell Papillomas in the Upper discusses the evidence regarding HPV etiology of benign SCPs in the upper aero-digestive tract Aero-Digestive Tract and Their and their HPV-related malignant transformation. In addition, studies on HPV exposure at an early Malignant Potential. Viruses 2021, 13, age are discussed, as are the animal models shedding light on HPV transmission, viral latency, and 1624. https://doi.org/10.3390/ its reactivation. v13081624 Keywords: papilloma; oral cavity; paranasal sinus; sinonasal; oropharynx; nasopharynx; larynx; Academic Editors: Christian esophagus; human papillomavirus; malignant transformation; risk factor; aneuploidy; transmission von Buchwald, Tina Dalianis and Anders Näsman Received: 14 June 2021 1. Introduction Accepted: 13 August 2021 Published: 17 August 2021 The upper aero-digestive tract is composed of the nasal cavity, paranasal sinuses, nasopharynx, oral cavity, oropharynx, hypopharynx, larynx, trachea, and esophagus. Publisher’s Note: MDPI stays neutral Squamous cell papillomas (SCPs) are histologically benign growths encountered practically with regard to jurisdictional claims in at all body sites where squamous epithelium exists (e.g., skin, eye conjunctiva, paranasal published maps and institutional affil- sinuses, pharynx, oral cavity, larynx, esophagus, bronchus, genital tract, urinary tract) [1]. iations. SCPs are composed of either exophytic and/or papillary fronds with fibrovascular cores or endophytic epithelial invaginations lined by stratified squamous or respiratory epithelium, depending on their anatomic site of origin. In the aero-digestive tract, the most common sites of SCPs are the oral cavity and Copyright: © 2021 by the authors. the larynx, while sinonasal and esophageal areas are less commonly involved. Only few Licensee MDPI, Basel, Switzerland. SCPs have been described in the naso- and oropharynx (especially base of the tongue and This article is an open access article tonsils) [1–8]. This might relate, however, to the ease of detection of these lesions, as oral distributed under the terms and papillomas are visible to the naked eye and even tiny laryngeal lesions can cause clinical conditions of the Creative Commons symptoms (hoarseness) earlier than SCPs at other anatomic sites. Attribution (CC BY) license (https:// The etiology of SCP is not universally confirmed but mechanical and chemical irrita- creativecommons.org/licenses/by/ tion and/or infection with human papillomaviruses (HPV) have been prime culprits [1]. 4.0/). Viruses 2021, 13, 1624. https://doi.org/10.3390/v13081624 https://www.mdpi.com/journal/viruses Viruses 2021, 13, x FOR PEER REVIEW 2 of 27 Viruses 2021, 13, 1624 2 of 26 The most widely studied entities are sinonasal papillomas and recurrent respiratory pap- The most widely studied entities are sinonasal papillomas and recurrent respiratory papil- illoma (RRP) of the larynx. This is because of their more aggressive behavior and potential loma (RRP) of the larynx. This is because of their more aggressive behavior and potential for malignant transformation. Aggressive clinical course (i.e., recurrence) of the disease is for malignant transformation. Aggressive clinical course (i.e., recurrence) of the disease is foundfound inin 20% 20% of of the the juvenile-onset-RRP juvenile-onset-RRP (JO-RRP) (JO-RRP) patients, patients, while while malignant malignant transformation transfor- ismation most prevalentis most prevalent among patientsamong patients with inverted with inverted sinonasal sinonasal papillomas papillomas (7–11%), (7–11%), followed fol- by adult-onsetlowed by adult-onset RRP (AO-RRP) RRP (AO-RRP) (3–6%). (3–6%). TheThe twotwo mostmost frequentfrequent HPVHPV genotypesgenotypes associatedassociated with SCPs are HPV6HPV6 and HPV11,HPV11, butbut high-riskhigh-risk HPV16HPV16 andand 18,18, andand otherother mucosalmucosal alpha-HPVs,alpha-HPVs, havehave beenbeen detecteddetected atat aa lowerlower frequency [1,2,9–11]. [1,2,9–11]. Import Importantly,antly, recent recent evidence evidence also also indicates indicates the the presence presence of cu- of cutaneoustaneous HPVs HPVs of ofthe the beta-and/or beta-and/or gamma gamma gene generara in oral, in oral, oro-, oro-, and and hypopharyneal hypopharyneal papil- pa- pillomas,lomas, as well as well as anecdotally as anecdotally in laryngeal in laryngeal papillomas papillomas [12,13]. [12 Based,13]. on Based the animal on the studies, animal studies,papillomavirus papillomavirus (PV)-associated (PV)-associated SCPs are SCPs highly are contagious highly contagious lesions that lesions produce that viral produce par- viralticles, particles, which are which shed are via shed the saliva via the and saliva other and secretions, other secretions, allowing allowing for the forautoinoculation the autoinoc- ulationor horizontal or horizontal transmission transmission of the virus of the [14]. virus In [ 14autoinoculation,]. In autoinoculation, viral particles viral particles can infect can infectadjacent adjacent traumatized traumatized mucosa, mucosa, resulting resulting in multiple in multiple lesions lesionsand/or and/orthe spreading the spreading of infec- oftion infection to other to body other sites body (e.g., sites from (e.g., sinonasal from sinonasal tract and/or tract oral and/or cavity oral to cavitynaso- and to naso- orophar- and oropharynx,ynx, larynx or larynx vice versa). or vice Maternal versa). Maternal HPV transmission HPV transmission is closely is associated closely associated only with only JO- withRRP JO-RRPbut is not but widely is not discussed widely discussed in the contex in thet context of pediatric of pediatric SCPs located SCPs located elsewhere elsewhere in the inaero-digestive the aero-digestive tract [15,16]. tract [15 ,16]. ThisThis reviewreview summarizessummarizes thethe keykey featuresfeatures ofof SCPsSCPs inin thethe upperupper aero-digestiveaero-digestive tracttract (Figure(Figure1 1),), including including the the trachea trachea and and esophagus. esophagus. WeWe discuss discuss the the causative causative role role of of HPV HPV infectioninfection andand the the site-specific site-specific differences differences in in its its aggressive aggressive behaviors behaviors and and malignant malignant potential poten- fortial eachfor each anatomic anatomic location location separately, separately, highlighting highlighting the gaps the ingaps our in knowledge. our knowledge. In addition, In ad- adition, brief accounta brief account is examined is examined in relation in torelation animal to models, animal HPV models, latency, HPV and latency, the successful and the eradicationsuccessful eradication of RRP in Australia of RRP in by Australia the nationwide by the nationwide HPV vaccination HPV vaccination program. program. FigureFigure 1. AA schematic schematic presentation presentation of of the the upper upper aero-diges aero-digestivetive tract. tract. This This review review also also includes includes the themore more distally distally located located trachea trachea and andesophagus. esophagus. The fi Thegure figure is modified is modified from fromthe original the original figure figure pub- lished as Figure 3.1, page 16, Report 2/2019, Should boys’ HPV vaccinations be included in the na- published as Figure 3.1, page 16, Report 2/2019, Should boys’ HPV vaccinations be included in tional vaccination programme? the National Institute for Health and Welfare. https://www.jul- the national vaccination programme? the National Institute for Health and Welfare. https://www. kari.fi/handle/10024/137477, accessed on 23 January 2019. Permission accessed 10 May 2021. julkari.fi/handle/10024/137477, accessed on 23 January 2019. Permission accessed 10 May 2021. 2.2. Sinonasal Papilloma (SNP) SinonasalSinonasal papilloma (SNPs), identifiedidentified in thethe 1850s1850s hashas frequentlyfrequently
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