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HPV in the Head and Neck Region 2.0

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Human Virology and Viral Diseases".

Deadline for manuscript submissions: closed (30 December 2022) | Viewed by 22395

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Prof. Dr. Tina Dalianis

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Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden
Interests: human papillomaviruses and cancer; especially in head and neck cancer; targeted therapy in head and neck cancer and pediatric cancer
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Prof. Dr. Christian von Buchwald

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Department of Otorhinolaryngology— Head and Neck Surgery and Audiology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark
Interests: human papillomavirus and head and neck cancer; biomarkers: circulating tumor DNA including circulating HPV DNA; reduction of treatment morbidity (trans-oral robotic surgery); sinonasal pathology; stem cells
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Dr. Anders Näsman

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Department of Oncology-Pathology, Karolinska Institutet, Stockholm, Sweden
Interests: head and neck cancer; tonsillar; base of tongue cancer; salivary gland cancer; clinical pathology; diagnostics and biomarkers
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Prof. Dr. Stina Syrjänen

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1. Emerita Professor, Department of Oral Pathology, Institute of Dentistry, Faculty of Medicine, University of Turku, Lemminkäisenkatu 2, 20520 Turku, Finland
2. Emerita Chief Physician (Co-affiliation), Department of Pathology, University of Turku, Turku University Hospital, Turku, Finland
Interests: human papillomaviruses; cancer; oral mucosa; upper aero-digestive tract; genital mucosa
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

There are more than 100 human papillomaviruses (HPVs), 13 of which are considered to be carcinogenic. Of those types, HPV 16 is associated with roughly 90% of HPV+ head and neck cancers, and the incidences of HPV+ tonsillar and base-of-tongue cancer have been increasing in many Western countries. Notably, HPV+ tonsillar and base of tongue cancer also have a considerably better prognosis than the corresponding HPV- tonsillar and base-of-tongue cancers. In addition, other HPV members can cause benign tumors of the head and neck region.

In this Special Issue, we wish to explore current research in HPV in the head and neck region. Topics of interest include, but are not limited to, the following:

The role of human papillomaviruses in cancer, benign tumors, and lesions in the head and neck region;
Diagnosis of human papillomavirus in cancer of the head and neck region;
Epidemics of human-papillomavirus-induced cancer in the head and neck region;
Therapeutic approaches including immune responses and/or targeted therapy and biomarkers in human-papillomavirus-positive cancer of the head and neck region;
HPV vaccination and it’s effects.

Prof. Dr. Tina Dalianis
Prof. Dr. Christian von Buchwald
Dr. Anders Näsman
Dr. Stina Syrjänen
Guest Editors

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

HPV head and neck cancer
HPV head and neck cancer diagnosis
HPV head and neck cancer epidemiology
HPV head and neck cancer therapy
HPV head and neck cancer vaccination

Published Papers (11 papers)

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Editorial

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3 pages, 192 KiB

Open AccessEditorial

Special Issue “HPV in the Head and Neck Region 2.0”

by Tina Dalianis, Christian von Buchwald, Anders Näsman and Stina Syrjanen

Viruses 2023, 15(5), 1119; https://doi.org/10.3390/v15051119 - 06 May 2023

Viewed by 895

Abstract

Members of the human papillomavirus (HPV) family have been known for causing cancers and condylomas in the anogenital tract for some time, as reflected by the Nobel Prize in Medicine given to Professor Harald zur Hausen 2008 [...] Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

Research

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12 pages, 1422 KiB

Open AccessArticle

Pretreatment Neutrophil-to-Lymphocyte Ratio as a Prognostic Marker for the Outcome of HPV-Positive and HPV-Negative Oropharyngeal Squamous Cell Carcinoma

by Marius Meldgaard Justesen, Kathrine Kronberg Jakobsen, Simone Kloch Bendtsen, Martin Garset-Zamani, Christine Mordhorst, Amanda-Louise Fenger Carlander, Anita Birgitte Gothelf, Christian Grønhøj and Christian von Buchwald

Viruses 2023, 15(1), 198; https://doi.org/10.3390/v15010198 - 10 Jan 2023

Cited by 5 | Viewed by 1779

Abstract

The incidence of oropharyngeal squamous cell carcinoma (OPSCC) has increased in the past decades due to carcinogenic HPV infection. As this patient group suffers from considerable mortality and treatment morbidity it is important to improve prognostic strategies in OPSCC. Inflammation plays a key role in cancer and the neutrophil-to-lymphocyte ratio (NLR) in blood has been suggested as a prognostic factor for OPSCC. This study aimed to investigate the prognostic impact of NLR on overall survival (OS) and recurrence-free survival (RFS) in a retrospective cohort of 1370 patients. Included patients had pretreatment neutrophil and lymphocyte counts available, as well as a known HPV status. Patients were treated with curative intent according to Danish national guidelines. We stratified patients in groups by NLR < 2, NLR 2–4, or NLR > 4 and analyzed the influence of the NLR tertile on OS and RFS. Kaplan–Meier curves illustrated survival probability in OS and RFS in the general cohort and were stratified by HPV status. We found that an increasing NLR was associated with inferior OS (HR = 1.5 for NLR > 4) and RFS (HR = 1.6 for NLR 2–4; HR = 1.8 for NLR > 4) in multivariable analysis. The Kaplan–Meier curves displayed inferior OS and RFS with an increasing NLR for both HPV+ and HPV− patients. In conclusion, we showed that an increasing NLR is prognostic for a worse outcome of OPSCC independently of HPV status. There are possible uses of NLR in prognostication and treatment de-escalation although further studies are warranted to determine the clinical utility. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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13 pages, 1192 KiB

Open AccessArticle

The Incidence, Survival, and HPV Impact of Second Primary Cancer following Primary Oropharyngeal Squamous Cell Carcinoma: A 20-Year Retrospective and Population-Based Study

by Lasse Andersen, Kathrine Kronberg Jakobsen, Amanda-Louise Fenger Carlander, Martin Garset-Zamani, Jeppe Friborg, Katalin Kiss, Rasmus L. Marvig, Caroline Olsen, Finn Cilius Nielsen, Elo Andersen, Christian Grønhøj and Christian von Buchwald

Viruses 2023, 15(1), 34; https://doi.org/10.3390/v15010034 - 22 Dec 2022

Cited by 5 | Viewed by 1432

Abstract

Second primary cancer (SPC) is the second most common cause of death among patients diagnosed with head and neck cancer. This study examined the risk of SPC following oropharyngeal squamous cell carcinoma (OPSCC) and the impact of human papillomavirus (HPV) on survival following SPC. The study was a population-based, retrospective study including all patients diagnosed with OPSCC in eastern Denmark from 2000–2020 who received curative intended treatment. The incidence rate ratio (IRR), age-adjusted incidence rates (AAIR), and hazard ratios (HR) were calculated. A total of 2584 patients with primary OPSCC were included (median follow-up time: 3.1 years), with 317 patients (12.3%) diagnosed with SPC. The risk of SPC was approximately five times the occurrence of cancer in the general population (IRR: 4.96). The median time to SPC after a primary OPSCC was 2.0 years (interquartile range (IQR) = 0.6–4.2 years). HPV-positive (HPV+) patients had a significantly longer median time to SPC, and a significant better survival compared to HPV-negative (HPV-) patients. SPC was most frequently found in lungs, head, and neck (LHN) for HPV- OPSCC patients and lungs followed by gender-specific (prostate, ovaries, or endometrium) for HPV+ OPSCC. There was a significant difference between the two groups when distributed between “within” or “outside” LHN. Patients with SPC outside LHN had a significant better overall survival. This knowledge should be considered during post-treatment surveillance and might guide targeted imaging. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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10 pages, 1384 KiB

Open AccessArticle

Longitudinal Dynamics of HPV16 Antibodies in Saliva and Serum among Pregnant Women

by Tiina Pirttilä, Stina Syrjänen, Karolina Louvanto and Vuokko Loimaranta

Viruses 2022, 14(11), 2567; https://doi.org/10.3390/v14112567 - 20 Nov 2022

Cited by 2 | Viewed by 1323

Abstract

Oral infections with high-risk (hr)HPV genotypes are associated with a subset of head and neck squamous cell carcinomas. Oral hrHPV infections may result from having oral sex, but also from horizontal infection from mouth to mouth. In such cases, saliva can serve as a vehicle for HPV transmission. Still, the prevalence and dynamics of salivary HPV antibodies in healthy non-vaccinated individuals are poorly known and the role of the salivary antibodies in protection from oral HPV infection is unclear. We used an ELISA assay to evaluate the dynamics and correlation of oral HPV16 infection and HPV16L1 and E7 specific antibody levels in saliva and serum samples among 39 women, 13 of which had persistent oral HPV16 infection. The women were mothers-to-be, sampled before delivery and followed up for 36 months postpartum. HPV16L1 IgG and sIgA antibodies were regularly detected in saliva. Antibody levels in serum remained stable during the 36-month follow-up, while antibody levels in saliva fluctuated. There was considerable individual variation in salivary HPV16L1 antibody levels, and some women had persistent oral HPV16 infection but no salivary antibodies. No differences in salivary HPV16L1 levels were found between the women with persistent or transient oral HPV16 infection. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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10 pages, 1130 KiB

Open AccessArticle

Analysis of Human Papilloma Virus Content and Integration in Mucoepidermoid Carcinoma

by Wenjin Gu, Apurva Bhangale, Molly E. Heft Neal, Josh D. Smith, Collin Brummel, Jonathan B. McHugh, Matthew E. Spector, Ryan E. Mills and J. Chad Brenner

Viruses 2022, 14(11), 2353; https://doi.org/10.3390/v14112353 - 26 Oct 2022

Cited by 3 | Viewed by 1609

Abstract

Mucoepidermoid Carcinomas (MEC) represent the most common malignancies of salivary glands. Approximately 50% of all MEC cases are known to harbor CRTC1/3-MAML2 gene fusions, but the additional molecular drivers remain largely uncharacterized. Here, we sought to resolve controversy around the role of human papillomavirus (HPV) as a potential driver of mucoepidermoid carcinoma. Bioinformatics analysis was performed on 48 MEC transcriptomes. Subsequent targeted capture DNA sequencing was used to annotate HPV content and integration status in the host genome. HPV of any type was only identified in 1/48 (2%) of the MEC transcriptomes analyzed. Importantly, the one HPV16+ tumor expressed high levels of p16, had high expression of HPV16 oncogenes E6 and E7, and displayed a complex integration pattern that included breakpoints into 13 host genes including PIK3AP1, HIPI, OLFM4,SIRT1, ARAP2, TMEM161B-AS1, and EPS15L1 as well as 9 non-genic regions. In this cohort, HPV is a rare driver of MEC but may have a substantial etiologic role in cases that harbor the virus. Genetic mechanisms of host genome integration are similar to those observed in other head and neck cancers. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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9 pages, 243 KiB

Open AccessArticle

Post-Treatment Neck Dissection of Tonsillar and Base of Tongue Squamous Cell Carcinoma in the Era of PET-CT, HPV, and p16

by David Landin, Anders Näsman, Sara Jonmarker Jara, Lalle Hammarstedt-Nordenvall, Eva Munck-Wikland, Tina Dalianis and Linda Marklund

Viruses 2022, 14(8), 1693; https://doi.org/10.3390/v14081693 - 30 Jul 2022

Cited by 3 | Viewed by 1795

Abstract

Human-papillomavirus (HPV)-positive tonsillar and base of tongue carcinomas (TSCC/BOTSCC) are rising in incidence and treatments with radiotherapy, chemoradiotherapy (RT/CRT), and neck dissections (NDs) have several side effects. Therefore, an improved selection of patients needing salvage NDs would be beneficial. We examined the prevalence and localisations of viable tumour cells in neck lymph nodes in patients post-RT/CRT, identified by fluorodeoxyglucose positron-emission tomography with computer-tomography (FDG PET-CT), with a focus on HPV-associated tumours. Patients with 217 TSCC/BOTSCC with tumours assessed for HPV-DNA and p16^INK4a undergoing FDG PET-CT 12 weeks after treatment and/or an ND were included. The FDG PET-CT data were compared with the findings in the pathology report after the ND. In total, 36/217 (17%) patients were selected for an ND due to positive findings in post-treatment FDG PET-CT. Of these, 35/36 were HPV-associated, 10/36 (28%) had viable tumour cells in the pathology reports of the neck specimen, and 8/10 (80%) were consistent with the FDG PET-CT findings, while 2/36 (5%) were missed by FDG PET-CT. We conclude that FDG PET-CT 12 weeks after RT/CRT is useful, but not completely reliable for finding all the metastases of HPV-associated TSCC/BOTSCC. Nonetheless, our data indicate that an ND could be more selectively guided by FDG PET-CT. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

18 pages, 3734 KiB

Open AccessArticle

Targeted Therapy of HPV Positive and Negative Tonsillar Squamous Cell Carcinoma Cell Lines Reveals Synergy between CDK4/6, PI3K and Sometimes FGFR Inhibitors, but Rarely between PARP and WEE1 Inhibitors

by Ourania N. Kostopoulou, Mark Zupancic, Mariona Pont, Emma Papin, Monika Lukoseviciute, Borja Agirre Mikelarena, Stefan Holzhauser and Tina Dalianis

Viruses 2022, 14(7), 1372; https://doi.org/10.3390/v14071372 - 23 Jun 2022

Cited by 7 | Viewed by 2040

Abstract

Human papillomavirus positive (HPV⁺) tonsillar and base of tongue squamous cell carcinoma (TSCC/BOTSCC) have a favorable outcome, but upon relapse, survival is poor and new therapeutical options are needed. Recently, we found synergistic effects by combining the food and drug administration approved (FDA) phosphoinositide 3-kinase (PI3K) and fibroblast-growth-factor-receptor (FGFR) inhibitors BYL719 and JNJ-42756493 on TSCC cell lines. Here this approach was extended and Cyclin-Dependent-Kinase-4/6 (CDK4/6) and Poly-ADP-ribose-polymerase (PARP) and WEE1 inhibitors PD-0332991, and MK-1775 respectively were also examined. HPV⁺ CU-OP-2, -3, -20, and HPV⁻ CU-OP-17 TSCC cell lines were treated with either BYL719 and JNJ-42756493, PD-0332991 BMN-673 and MK-1775 alone or in different combinations. Viability, proliferation, and cytotoxicity were followed by WST-1 assays and the IncuCyte S3 Live^® Cell Analysis System. All inhibitors presented dose-dependent inhibitory effects on tested TSCC lines. Synergy was frequently obtained when combining CDK4/6 with PI3K inhibitors, but only sometimes or rarely when combining CDK4/6 with FGFR inhibitors or PARP with WEE1 inhibitors. To conclude, using CDK4/6 with PI3K or FGFR inhibitors, especially PD-0332991 with BYL719 presented synergy and enhanced the decrease of viability considerably, while although dose dependent responses were obtained with PARP and WEE1 inhibitors (BMN-673 and MK-1775 resp.), synergy was rarely disclosed. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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11 pages, 2235 KiB

Open AccessArticle

Human Papillomavirus Detected in Oropharyngeal Cancers from Chilean Subjects

by Carolina Oliva, Diego Carrillo-Beltrán, Paul Boettiger, Iván Gallegos and Francisco Aguayo

Viruses 2022, 14(6), 1212; https://doi.org/10.3390/v14061212 - 02 Jun 2022

Cited by 7 | Viewed by 1669

Abstract

High-risk human papillomaviruses (HR-HPV) are the causal agents of an important subset of oropharyngeal cancers that has increased considerably in incidence in recent years. In this study, we evaluated the presence of HPV in 49 oropharyngeal cancers from Chilean subjects. The presence of HPV DNA was analyzed by conventional PCR, the genotypes were identified through sequencing, and the expression of E6/E7 transcripts was evaluated by a reverse transcriptase polymerase chain reaction (RT-PCR). Additionally, to determine p16 expression—a surrogate marker for oncogenic HPV infection—a tissue array was constructed for immunohistochemistry (IHC). HPV was detected in 61.2% of oropharyngeal carcinomas, the most prevalent genotype being HPV16 (80%). E6 and E7 transcripts were detected in 91.6% and 79.1% of the HPV16-positive specimens, respectively, demonstrating functional HPV infections. Furthermore, p16 expression was positive in 58.3% of cases. These findings show a high prevalence of HR-HPV in oropharyngeal tumors from Chile, suggesting the necessity of additional studies to address this growing public health concern. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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9 pages, 2608 KiB

Open AccessArticle

Analysis of Human Papillomavirus (HPV) and Polyomaviruses (HPyVs) in Adenoid Cystic Carcinoma (AdCC) of the Head and Neck Region Reveals Three HPV-Positive Cases with Adenoid Cystic-like Features

by Mark Zupancic, Stefan Holzhauser, Liquin Cheng, Torbjörn Ramqvist, Juan Du, Signe Friesland, Anders Näsman and Tina Dalianis

Viruses 2022, 14(5), 1040; https://doi.org/10.3390/v14051040 - 13 May 2022

Cited by 4 | Viewed by 2036

Abstract

An aetiological role of human papillomavirus (HPV) and/or human polyomaviruses (HPyVs) has been proposed in adenoid cystic carcinoma (AdCC). Moreover, HPV-related multiphenotypic carcinoma (HMSC) was recently introduced as an emerging entity of the sinonasal region. Here, we primarily want to study the role of HPV/HPyV in a large AdCC cohort and, secondly, possibly identify and characterize HMSC. Tumour DNA from 68 patients initially diagnosed with AdCC between 2000 and 2012 was, therefore, tested for 27 HPV types and 10 HPyVs. HPV DNA-positive samples were micromorphologically re-evaluated, further stained for p16^INK4a, S100, p63 and CD117 and tested for the presence of the MYB-NFIB fusion transcript. Notably, no samples were HPyV-positive, while one sinonasal and two tonsillar carcinomas were HPV- and p16-positive. After re-evaluating the micromorphology, immunohistochemistry and presence of fusion transcripts, all tumours had the same appearance and fitted within the diagnosis of HMSC, but in all these three cases, the morphology of the HMSC and basaloid squamous cell carcinoma was overlapping. We conclude that HPV and HPyV have no major role in AdCC. However, based on our data, we also suggest that HMSC should be considered as a basaloid variant of squamous cell carcinoma, and not its own entity, until better characterized. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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Review

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20 pages, 1136 KiB

Open AccessReview

Advanced Nanomedicine for High-Risk HPV-Driven Head and Neck Cancer

by Qiang Xu, Ye Chen, Yuan Jin, Zhiyu Wang, Haoru Dong, Andreas M. Kaufmann, Andreas E. Albers and Xu Qian

Viruses 2022, 14(12), 2824; https://doi.org/10.3390/v14122824 - 19 Dec 2022

Cited by 3 | Viewed by 2624

Abstract

The incidence of high-risk Human Papillomavirus (HR-HPV)-driven head and neck squamous cell carcinoma (HNSCC) is on the rise globally. HR-HPV-driven HNSCC displays molecular and clinical characteristics distinct from HPV-uninvolved cases. Therapeutic strategies for HR-HPV-driven HNSCC are under investigation. HR-HPVs encode the oncogenes E6 and E7, which are essential in tumorigenesis. Meanwhile, involvement of E6 and E7 provides attractive targets for developing new therapeutic regimen. Here we will review some of the recent advancements observed in preclinical studies and clinical trials on HR-HPV-driven HNSCC, focusing on nanotechnology related methods. Materials science innovation leads to great improvement for cancer therapeutics including HNSCC. This article discusses HPV-E6 or -E7- based vaccines, based on plasmid, messenger RNA or peptide, at their current stage of development and testing as well as how nanoparticles can be designed to target and access cancer cells and activate certain immunology pathways besides serving as a delivery vehicle. Nanotechnology was also used for chemotherapy and photothermal treatment. Short interference RNA targeting E6/E7 showed some potential in animal models. Gene editing by CRISPR-CAS9 combined with other treatments has also been assessed. These advancements have the potential to improve the outcome in HR-HPV-driven HNSCC, however breakthroughs are still to be awaited with nanomedicine playing an important role. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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Other

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16 pages, 1057 KiB

Open AccessSystematic Review

The Prevalence of HPV in Oral Cavity Squamous Cell Carcinoma

by Seyed Keybud Katirachi, Mathias Peter Grønlund, Kathrine Kronberg Jakobsen, Christian Grønhøj and Christian von Buchwald

Viruses 2023, 15(2), 451; https://doi.org/10.3390/v15020451 - 06 Feb 2023

Cited by 18 | Viewed by 4180

Abstract

Human papillomavirus (HPV) is an important risk factor in a subset of head and neck squamous cell carcinomas (HNSCC), but the association with oral cavity squamous cell carcinomas (OCSCC) remains controversial. This study aimed to identify the prevalence of HPV infection in OCSCC. A systematic search on PubMed and EMBASE was performed, including articles assessing the prevalence of HPV-positive (HPV+) OCSCC published from January 2017 to December 2022. OCSCC was considered HPV+ by the detection of HPV DNA, HPV RNA, and/or p16 overexpression in the tumor mass. A meta-analysis was made determining the overall HPV+ OCSCC prevalence. We included 31 studies comprising 5007 patients from 24 countries. The study size ranged from 17 to 940 patients. The HPV+ OCSCC proportion variated widely and ranged from 0% to 37%. Tumors in the tongue were the predominant sublocation for HPV in the oral cavity. The meta-analysis revealed that the overall HPV+ OCSCC prevalence is 6% (95% CI; 3–10%), and only one study found HPV and OCSCC significantly associated. Thus, HPV may not be a necessary or a strong risk factor in OCSCC oncogenesis, and the possibility of a site misclassification of a mobile tongue with the root of the tongue cannot be excluded. Full article

(This article belongs to the Special Issue HPV in the Head and Neck Region 2.0)

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